Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases
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Abstract
PURPOSE: The purpose of this study was to determine the accuracy, precision, and linearity of the CellSearch system and evaluate the number of circulating tumor cells (CTCs) per 7.5 mL of blood in healthy subjects, patients with nonmalignant diseases, and patients with a variety of metastatic carcinomas. EXPERIMENTAL DESIGN: The CellSearch system was used to enumerate CTCs in 7.5 mL of blood. Blood samples spiked with cells from tumor cell lines were used to establish analytical accuracy, reproducibility, and linearity. Prevalence of CTCs was determined in blood from 199 patients with nonmalignant diseases, 964 patients with metastatic carcinomas, and 145 healthy donors. RESULTS: Enumeration of spiked tumor cells was linear over the range of 5 to 1,142 cells, with an average recovery of >/=85% at each spike level. Only 1 of the 344 (0.3%) healthy and nonmalignant disease subjects had >/=2 CTCs per 7.5 mL of blood. In 2,183 blood samples from 964 metastatic carcinoma patients, CTCs ranged from 0 to 23,618 CTCs per 7.5 mL (mean, 60 +/- 693 CTCs per 7.5 mL), and 36% (781 of 2,183) of the specimens had >/=2 CTCs. Detection of >/=2 CTCs occurred at the following rates: 57% (107 of 188) of prostate cancers, 37% (489 of 1,316) of breast cancers, 37% (20 of 53) of ovarian cancers, 30% (99 of 333) of colorectal cancers, 20% (34 of 168) of lung cancers, and 26% (32 of 125) of other cancers. CONCLUSIONS: The CellSearch system can be standardized across multiple laboratories and may be used to determine the clinical utility of CTCs. CTCs are extremely rare in healthy subjects and patients with nonmalignant diseases but present in various metastatic carcinomas with a wide range of frequencies.
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NSCLC patient CTCs cannot always be reliably identified.
“While circulating tumor cells (CTCs) are considered a form of liquid biopsy, and we (31) and others (47) have reported on approaches for molecular analysis of CTCs, NSCLC patient CTCs cannot always be reliably identified (44, 48, 49).”
Cites
National Committee for Clinical Laboratory Standards
Bruck, E. (1980) · PEDIATRICS · doi:10.1542/peds.65.1.187 · Cited by 14,736 · see citing works
Addelman, S., Box, G. E. P., Hunter, W. G., & Hunter, J. S. (1979) · Technometrics · doi:10.2307/1267766 · Cited by 6,753 · see citing works
Circulating Tumor Cells, Disease Progression, and Survival in Metastatic Breast Cancer
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. M. M., et al. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa040766 · Cited by 4,602 · see citing works
Detection and characterization of carcinoma cells in the blood
Racila, E. V., Euhus, D., Weiss, A. J., Rao, C., McConnell, J. D., Terstappen, L. W. M. M., & Uhr, J. W. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.8.4589 · Cited by 713 · see citing works
Ross, A., Cooper, B., Lazarus, H. M., Mackay, W., Moss, T., Ciobanu, N., Tallman, M. S., Kennedy, M., Davidson, N., & Sweet, D. (1993) · Blood · doi:10.1182/blood.v82.9.2605.bloodjournal8292605 · Cited by 487 · see citing works
Brugger, W., Bross, K., Glatt, M., Weber, F., Mertelsmann, R. H., & Kanz, L. (1994) · Blood · doi:10.1182/blood.v83.3.636.636 · Cited by 440 · see citing works
Brugger, W., Bross, K., Glatt, M., et al. (1994) · Blood · doi:10.1182/blood.v83.3.636.bloodjournal833636 · Cited by 357 · see citing works
Momburg, F., Moldenhauer, G., Hämmerling, G. J., & Möller, P. (1987) · PubMed · Cited by 328 · see citing works
Kugaya, A., Akechi, T., Okuyama, T., Nakano, T., Mikami, I., Okamura, H., & Uchitomi, Y. (2000) · Cancer · doi:10.1002/1097-0142(20000615)88:12 · Cited by 309 · see citing works
Borgen, E., Naume, B., Nesland, J. M., Kvalheim, G., Beiske, K., Fodstad, Ø., Diel, I., Solomayer, E., Theocharous, P., Coombes, R. C., et al. (1999) · Cytotherapy · doi:10.1080/0032472031000141283 · Cited by 263 · see citing works
Circulating tumor cell clusters in the peripheral blood of colorectal cancer patients.
Molnar, B. A., Ladányi, A., Tanko, L. M., Sreter, L., & Tulassay, Z. (2001) · PubMed · Cited by 241 · see citing works
Circulating Breast Cancer Cells Are Frequently Apoptotic
Méhes, G., Witt, A., Kubista, E., & Ambros, P. F. (2001) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)61667-7 · Cited by 237 · see citing works
Pierga, J., Bonneton, C., Vincent‐Salomon, A., de Crémoux, P., Nos, C., Blin, N., Pouillart, P., Thiery, J. P., & Magdelénat, H. (2004) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-0102-03 · Cited by 223 · see citing works
Molecular detection of micrometastases and circulating tumor cells in solid tumors.
Ghossein, R. A., Bhattacharya, S., & Rosaí, J. (1999) · PubMed · Cited by 223 · see citing works
Hayes, D. F., Walker, T., Singh, B., Vitetta, E. S., Uhr, J. W., Gross, S., Rao, C., Doyle, G. V., & Terstappen, L. W. M. M. (2002) · International Journal of Oncology · doi:10.3892/ijo.21.5.1111 · Cited by 158 · see citing works
Witzig, T. E., Bossy, B., Kimlinger, T. K., Roche, P. C., Ingle, J. N., Grant, C. S., Donohue, J. H., Suman, V. J., Harrington, D. S., de la Torre-Bueno, J., et al. (2002) · PubMed · Cited by 156 · see citing works
Moreno, J. G., O'Hara, S. M., Gross, S., Doyle, G. V., Fritsche, H. A., Gomella, L. G., & Terstappen, L. W. M. M. (2001) · Urology · doi:10.1016/s0090-4295(01)01191-8 · Cited by 154 · see citing works
Apoptosis of circulating tumor cells in prostate cancer patients
Larson, C. J., Moreno, J. G., Pienta, K. J., Gross, S., Repollet, M., O'Hara, S. M., Russell, T. B., & Terstappen, L. W. M. M. (2004) · Cytometry Part A · doi:10.1002/cyto.a.20073 · Cited by 151 · see citing works
Gaforio, J. J., Serrano, M. J., Sánchez‐Rovira, P., Sirvent, A., Delgado‐Rodríguez, M., Campos, M., de la Torre, N., Algarra, I., Dueñas, R., & Lozano, A. M. (2003) · International Journal of Cancer · doi:10.1002/ijc.11479 · Cited by 133 · see citing works
Optimization of ferrofluids and protocols for the enrichment of breast tumor cells in blood
Liberti, P. A., Rao, C., & Terstappen, L. W. M. M. (2001) · Journal of Magnetism and Magnetic Materials · doi:10.1016/s0304-8853(00)01254-3 · Cited by 133 · see citing works
Tumor Markers : Physiology, Pathobiology, Technology, and Clinical Applications
Fritsche, H. A., Diamandis, E. P., & Lilja, H. G. (2002) · Cited by 126 · see citing works
Hardingham, J. E., Kotasek, D., Farmer, B. J., Butler, R. N., Mi, J.-J., Sage, R. E., & Dobrovic, A. (1993) · PubMed · Cited by 119 · see citing works
Detection and isolation of prostate cancer cells from peripheral blood and bone marrow
Ellis, W. J., Pfitzenmaier, J., Colli, J. L., Arfman, E. W., Lange, P. H., & Vessella, R. L. (2003) · Urology · doi:10.1016/s0090-4295(02)02291-4 · Cited by 117 · see citing works
Naume, B., Borgen, E., Beiske, K., Herstad, T. K., Ravnås, G., Renolen, A., Trachsel, S., Thrane-Steen, K., Funderud, S., & Kvalheim, G. (1997) · Journal of Hematotherapy · doi:10.1089/scd.1.1997.6.103 · Cited by 113 · see citing works
Gomella, L. G., Raj, G. V., & Moreno, J. G. (1997) · The Journal of Urology · doi:10.1016/s0022-5347(01)64472-0 · Cited by 97 · see citing works
Bilkenroth, U., Taubert, H. W., Riemann, D., Rebmann, U., Heynemann, H., & Meye, A. (2001) · International Journal of Cancer · doi:10.1002/ijc.1217 · Cited by 89 · see citing works
O'Hara, S. M., Moreno, J. G., Zweitzig, D. R., Gross, S., Gomella, L. G., & Terstappen, L. W. M. M. (2004) · Clinical Chemistry · doi:10.1373/clinchem.2003.028563 · Cited by 73 · see citing works
Gao, C., Rawal, S. K., Sun, L. L., Ali, A., Connelly, R. R., Bañez, L. L., Sesterhenn, I. A., McLeod, D. G., Moul, J. W., & Srivastava, S. K. (2003) · PubMed · Cited by 39 · see citing works
Molecular detection of micro-metastasis in breast cancer
Jiang, W. G. (2002) · Critical Reviews in Oncology/Hematology · doi:10.1016/s1040-8428(01)00181-0 · Cited by 37 · see citing works
Zigeuner, R. E., Riesenberg, R., Pohla, H., Hofstetter, A. G., & Oberneder, R. (2000) · The Journal of Urology · doi:10.1016/s0022-5347(05)67116-9 · Cited by 33 · see citing works
Evaluation of Grafts for Occult Tumor Cells
Moss, T. J., To, L. B., & Pantel, K. (1994) · Journal of Hematotherapy · doi:10.1089/scd.1.1994.3.163 · Cited by 8 · see citing works
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Cited by
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Circulating Tumor Cells, Disease Progression, and Survival in Metastatic Breast Cancer
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. M. M., et al. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa040766 · Cited by 4,602 · see citing works
Isolation of rare circulating tumour cells in cancer patients by microchip technology
Nagrath, S., Sequist, L. V. D., Maheswaran, S., Bell, D. W., Irimia, D., Ulkus, L., Smith, M. R., Kwak, E. L., Digumarthy, S. R., Muzikansky, A., et al. (2007) · Nature · doi:10.1038/nature06385 · Cited by 3,565 · see citing works
Bono, J. S. D., Scher, H. I., Montgomery, B., Parker, C. C., Miller, M. C., Tissing, H., Doyle, G. V., Terstappen, L. W. M. M., Pienta, K. J., & Raghavan, D. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-0872 · Cited by 2,189 · see citing works
Integrating liquid biopsies into the management of cancer
Siravegna, G., Marsoni, S., Siena, S., & Bardelli, A. (2017) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2017.14 · Cited by 1,941 · see citing works
Cohen, S. J., Punt, C. J. A., Iannotti, N. O., Saidman, B. H., Sabbath, K. D., Gabrail, N. Y., Picus, J., Morse, M., Mitchell, E. P., Miller, M. C., et al. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2007.15.8923 · Cited by 1,843 · see citing works
Detection of Mutations in <i>EGFR</i> in Circulating Lung-Cancer Cells
Maheswaran, S., Sequist, L. V., Nagrath, S., Ulkus, L., Brannigan, B., Collura, C. V., Inserra, E., Diederichs, S., Iafrate, A. J., Bell, D. W., et al. (2008) · New England Journal of Medicine · doi:10.1056/nejmoa0800668 · Cited by 1,617 · see citing works
Riethdorf, S., Fritsche, H. A., Müller, V., Rau, T., Schindlbeck, C., Rack, B. K., Janni, W., Coith, C., Beck, K., Jänicke, F., et al. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-1695 · Cited by 1,342 · see citing works
Circulating Tumor Cells: A Novel Prognostic Factor for Newly Diagnosed Metastatic Breast Cancer
Cristofanilli, M., Hayes, D. F., Budd, G. T., Ellis, M. J., Stopeck, A., Reuben, J. M., Doyle, G. V., Matera, J., Allard, W. J., Miller, M. C., et al. (2005) · Journal of Clinical Oncology · doi:10.1200/jco.2005.08.140 · Cited by 1,134 · see citing works
Sturgeon, C. M., Duffy, M. J., Stenman, U., Lilja, H. G., Brünner, N., Chan, D. W., Babaian, R. J., Bast, R. C., Dowell, B. L., Esteva, F. J., et al. (2008) · Clinical Chemistry · doi:10.1373/clinchem.2008.105601 · Cited by 1,135 · see citing works
Circulating tumor cells: approaches to isolation and characterization
Yu, M., Stott, S. L., Toner, M., Maheswaran, S., & Haber, D. A. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201010021 · Cited by 1,085 · see citing works
Emre Özkumur, A., Shah, A. M., Ciciliano, J. C., Emmink, B. L., Miyamoto, D. T., Brachtel, E. F., Yu, M., Chen, P.-I., Morgan, B., Trautwein, J., et al. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3005616 · Cited by 1,087 · see citing works
Hayes, D. F., Cristofanilli, M., Budd, G. T., Ellis, M. J., Stopeck, A., Miller, M. C., Matera, J., Allard, W. J., Doyle, G. V., & Terstappen, L. W. M. M. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-2821 · Cited by 1,032 · see citing works
Scher, H. I., & Sawyers, C. L. (2005) · Journal of Clinical Oncology · doi:10.1200/jco.2005.03.4777 · Cited by 1,025 · see citing works
Circulating tumor cells: biology and clinical significance
Lin, D., Shen, L., Luo, M., Zhang, K., Li, J., Yang, Q., Zhu, F., Zhou, D., Zheng, S. S., Chen, Y., et al. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00817-8 · Cited by 1,018 · see citing works
Circulating tumor cells (CTC) detection: Clinical impact and future directions
Paterlini-Bréchot, P., & Benali, N. L. (2007) · Cancer Letters · doi:10.1016/j.canlet.2006.12.014 · Cited by 953 · see citing works
Long-term patient survival in ANCA-associated vasculitis
Floßmann, O., Berden, A. E., de Groot, K., Hagen, C., Harper, L., Heijl, C., Höglund, P., Jayne, D. R. W., Luqmani, R. A., Mahr, A., et al. (2010) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2010.137778 · Cited by 940 · see citing works
Krebs, M., Sloane, R. A. S., Priest, L. J. C., Lancashire, L., Hou, J., Greystoke, A., Ward, T. H., Ferraldeschi, R., Hughes, A. M., Clack, G., et al. (2011) · Journal of Clinical Oncology · doi:10.1200/jco.2010.28.7045 · Cited by 870 · see citing works
Hou, J., Krebs, M., Lancashire, L., Sloane, R. A. S., Backen, A. C., Swain, R. K., Priest, L. J. C., Greystoke, A., Zhou, C., Morris, K. L., et al. (2012) · Journal of Clinical Oncology · doi:10.1200/jco.2010.33.3716 · Cited by 844 · see citing works
Bidard, F., Peeters, D. J. E., Fehm, T. N., Nolè, F., Gisbert‐Criado, R., Mavroudis, D., Grisanti, S., Generali, D., García-Sáenz, J. Á., Stebbing, J., et al. (2014) · The Lancet Oncology · doi:10.1016/s1470-2045(14)70069-5 · Cited by 842 · see citing works
Circulating Tumor Cells versus Imaging—Predicting Overall Survival in Metastatic Breast Cancer
Budd, G. T., Cristofanilli, M., Ellis, M. J., Stopeck, A., Borden, E. C., Miller, M. C., Matera, J., Repollet, M., Doyle, G. V., Terstappen, L. W. M. M., et al. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-1769 · Cited by 776 · see citing works
Microfluidic, marker-free isolation of circulating tumor cells from blood samples
Karabacak, M., Spuhler, P. S., Fachin, F., Lim, E. J., Pai, V., Emre Özkumur, A., Martel, J. M., Kojić, N., Smith, K., Chen, P.-I., et al. (2014) · Nature Protocols · doi:10.1038/nprot.2014.044 · Cited by 760 · see citing works
Miller, M. C., Doyle, G. V., & Terstappen, L. W. M. M. (2009) · Journal of Oncology · doi:10.1155/2010/617421 · Cited by 752 · see citing works
Liquid biopsy in cancer: current status, challenges and future prospects
Ma, L., Guo, H., Zhao, Y., Liu, Z., Wang, C., Bu, J., Sun, T., & Wei, J. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-024-02021-w · Cited by 785 · see citing works
Blood-Based Analyses of Cancer: Circulating Tumor Cells and Circulating Tumor DNA
Haber, D. A., & Velculescu, V. E. (2014) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-1014 · Cited by 697 · see citing works
Tumorigenicity and genetic profiling of circulating tumor cells in small-cell lung cancer
Hodgkinson, C. L., Morrow, C. J., Li, Y., Metcalf, R. L., Rothwell, D. G., Trapani, F., Polański, R., Burt, D. J., Simpson, K., Morris, K. L., et al. (2014) · Nature Medicine · doi:10.1038/nm.3600 · Cited by 695 · see citing works
Circulating Tumor Cell Number and Prognosis in Progressive Castration-Resistant Prostate Cancer
Danila, D. C., Heller, G., Gignac, G. A., Gonzalez-Espinoza, R., Anand, A., Tanaka, E., Lilja, H. G., Schwartz, L. B., Larson, S. M., Fleisher, M., et al. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-1506 · Cited by 665 · see citing works
Circulating Tumor Cells and Response to Chemotherapy in Metastatic Breast Cancer: SWOG S0500
Smerage, J. B., Barlow, W. E., Hortobágyi, G. N., Winer, E. P., Leyland-Jones, B. R., Srkalović, G., Tejwani, S., Schott, A. F., O’Rourke, M. A., Lew, D. L., et al. (2014) · Journal of Clinical Oncology · doi:10.1200/jco.2014.56.2561 · Cited by 649 · see citing works
Tie, J., Kinde, I., Wang, Y., Wong, H., Roebert, J. K., Christie, M., TACEY, M. A., Wong, R., Singh, M., Karapetis, C. S., et al. (2015) · Annals of Oncology · doi:10.1093/annonc/mdv177 · Cited by 632 · see citing works
Molecular analysis of circulating tumour cells—biology and biomarkers
Krebs, M., Metcalf, R. L., Carter, L., Brady, G., Blackhall, F. H., & Dive, C. (2014) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2013.253 · Cited by 620 · see citing works
Circulating Tumor Cells Predict Survival in Early Average-to-High Risk Breast Cancer Patients
Rack, B., Schindlbeck, C., Jückstock, J., Andergassen, U., Hepp, P., Zwingers, T., Friedl, T. W. P., Lorenz, R., Tesch, H., Fasching, P. A., et al. (2014) · JNCI: Journal of the National Cancer Institute · doi:10.1093/jnci/dju066 · Cited by 615 · see citing works
Scher, H. I., Jia, X., Bono, J. S. D., Fleisher, M., Pienta, K. J., Raghavan, D., & Heller, G. (2009) · The Lancet Oncology · doi:10.1016/s1470-2045(08)70340-1 · Cited by 611 · see citing works
Slanted spiral microfluidics for the ultra-fast, label-free isolation of circulating tumor cells
Warkiani, M. E., Guan, G., Luan, K. B., Lee, W. C., Bhagat, A. A. S., Chaudhuri, P. K., Tan, D. S.-W., Lim, C. T., Lee, S. C., Chen, P. C. Y., et al. (2013) · Lab on a Chip · doi:10.1039/c3lc50617g · Cited by 573 · see citing works
Tumor Heterogeneity in Breast Cancer
Turashvili, G., & Brogi, E. (2017) · Frontiers in Medicine · doi:10.3389/fmed.2017.00227 · Cited by 571 · see citing works
The biology of circulating tumor cells
Pantel, K., & Speicher, M. R. (2015) · Oncogene · doi:10.1038/onc.2015.192 · Cited by 544 · see citing works
Whole-exome sequencing of circulating tumor cells provides a window into metastatic prostate cancer
Lohr, J. G., Adalsteinsson, V. A., Cibulskis, K., Choudhury, A. D., Rosenberg, M. W., Cruz‐Gordillo, P., Francis, J. M., Zhang, C.-Z., Shalek, A. K., Satija, R., et al. (2014) · Nature Biotechnology · doi:10.1038/nbt.2892 · Cited by 534 · see citing works
Powell, A. A., Talasaz, A. H., Zhang, H., Coram, M., Reddy, A., Deng, G. Y., Telli, M. L., Advani, R. H., Carlson, R. W., Mollick, J. A., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033788 · Cited by 531 · see citing works
Prognostic significance of circulating tumor cells in patients with metastatic colorectal cancer
Cohen, S. J., Punt, C. J. A., Iannotti, N. O., Saidman, B. H., Sabbath, K. D., Gabrail, N., Picus, J., Morse, M. A., Mitchell, E. P., Miller, M. C., et al. (2009) · Annals of Oncology · doi:10.1093/annonc/mdn786 · Cited by 513 · see citing works
Circulating tumor cell technologies
Ferreira, M. M., Ramani, V. C., & Jeffrey, S. S. (2016) · Molecular Oncology · doi:10.1016/j.molonc.2016.01.007 · Cited by 515 · see citing works
Three‐Dimensional Nanostructured Substrates toward Efficient Capture of Circulating Tumor Cells
Wang, S., Wang, H., Jiao, J., Chen, K., Owens, G. E., Kamei, K., Sun, J., Sherman, D. J., Behrenbruch, C. P., Wu, H., et al. (2009) · Angewandte Chemie International Edition · doi:10.1002/anie.200901668 · Cited by 512 · see citing works
Eyles, J., Puaux, A.-L., Wang, X., Toh, B., Prakash, C., Hong, M., Tan, T. G., Zheng, L., Ong, L. C., Jin, Y., et al. (2010) · Journal of Clinical Investigation · doi:10.1172/jci42002 · Cited by 506 · see citing works
Circulating tumour cells in non-metastatic breast cancer: a prospective study
Lucci, A., Hall, C. S., Lodhi, A., Bhattacharyya, A., Anderson, A. E., Xiao, L., Bedrosian, I., Kuerer, H. M., & Krishnamurthy, S. (2012) · The Lancet Oncology · doi:10.1016/s1470-2045(12)70209-7 · Cited by 507 · see citing works
Riethdorf, S., Müller, V., Zhang, L., Rau, T., Loibl, S., Komor, M., Roller, M., Huober, J., Fehm, T. N., Schrader, I., et al. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-2042 · Cited by 487 · see citing works
Talasaz, A. H., Powell, A. A., Huber, D. E., Berbee, J. G., Roh, K., Yu, W., Xiao, W., Davis, M. M., Pease, R. F. W., Mindrinos, M. N., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813188106 · Cited by 480 · see citing works
Biomarkers of gastric cancer: Current topics and future perspective
Matsuoka, T., & Yashiro, M. (2018) · World Journal of Gastroenterology · doi:10.3748/wjg.v24.i26.2818 · Cited by 476 · see citing works
Krebs, M. G., Hou, J.-M., Sloane, R., Lancashire, L., Priest, L., Nonaka, D., Ward, T. H., Backen, A., Clack, G., Hughes, A., et al. (2012) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e31823c5c16 · Cited by 463 · see citing works
A conduit to metastasis: circulating tumor cell biologyPreprint
Micalizzi, D. S., Maheswaran, S., & Haber, D. A. (2017) · Genes & Development · doi:10.1101/gad.305805.117 · Cited by 446 · see citing works
Marrugo-Ramírez, J., Mir, M., & Samitier, J. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19102877 · Cited by 388 · see citing works
Moon, H.-S., Kwon, K., Kim, S. I., Han, H., Sohn, J., Lee, S. H., & Jung, H. (2011) · Lab on a Chip · doi:10.1039/c0lc00345j · Cited by 438 · see citing works
Recent advances in gastric cancer early diagnosis
Necula, L. G., Matei, L., Dragu, D., Neagu, A. I., Mambet, C., Nedeianu, S., Bleoţu, C., Diaconu, C. C., & Chivu‐Economescu, M. (2019) · World Journal of Gastroenterology · doi:10.3748/wjg.v25.i17.2029 · Cited by 432 · see citing works
Sieuwerts, A. M., Kraan, J., Bolt, J., van der Spoel, P., Elstrodt, F., Schutte, M. E. M., Martens, J. W. M., Gratama, J.-W. C., Sleijfer, S., & Foekens, J. A. (2008) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djn419 · Cited by 435 · see citing works
Cellular Image Analysis and Imaging by Flow Cytometry
Basiji, D. A., Ortyn, W. E., Liang, L., Vidya Venkatachalam, A., & Morrissey, P. (2007) · Clinics in Laboratory Medicine · doi:10.1016/j.cll.2007.05.008 · Cited by 427 · see citing works
3D microfilter device for viable circulating tumor cell (CTC) enrichment from blood
Zheng, S., Lin, H. K., Lü, B., Williams, A. J., Datar, R. H., Côté, R. J., & Tai, Y. (2010) · Biomedical Microdevices · doi:10.1007/s10544-010-9485-3 · Cited by 421 · see citing works
Punnoose, E. A., Atwal, S., Liu, W., Raja, R., Fine, B. M., Hughes, B. G. M., Hicks, R. J., Hampton, G. M., Amler, L. C., Pirzkall, A., et al. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-3148 · Cited by 415 · see citing works
Danila, D. C., Morris, M. J., de Bono, J. S., Ryan, C. J., Denmeade, S. R., Smith, M. R., Taplin, M.-E., Bubley, G. J., Kheoh, T., Haqq, C., et al. (2010) · Journal of Clinical Oncology · doi:10.1200/jco.2009.25.9259 · Cited by 410 · see citing works
Farace, F., Massard, C., Vimond, N., Drusch, F., Jacques, N., Billiot, F., Laplanche, A., Chauchereau, A., Lacroix, L., Planchard, D., et al. (2011) · British Journal of Cancer · doi:10.1038/bjc.2011.294 · Cited by 408 · see citing works
Sun, Y., Xu, Y., Yang, X., Guo, W., Zhang, X., Qiu, S., Shi, R.-Y., Hu, B., Zhou, J., & Fan, J. (2012) · Hepatology · doi:10.1002/hep.26151 · Cited by 405 · see citing works
Microchip-based immunomagnetic detection of circulating tumor cells
Hoshino, K., Huang, Y.-Y., Lane, N., Huebschman, M., Uhr, J. W., Frenkel, E. P., & Zhang, X. (2011) · Lab on a Chip · doi:10.1039/c1lc20270g · Cited by 400 · see citing works
Kelley, S. O., Mirkin, C. A., Walt, D. R., Ismagilov, R. F., Toner, M., & Sargent, E. H. (2014) · Nature Nanotechnology · doi:10.1038/nnano.2014.261 · Cited by 398 · see citing works
Unravelling the complexity of metastasis — molecular understanding and targeted therapies
Sethi, N. S., & Kang, Y. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3125 · Cited by 396 · see citing works
Reid, A. H. M., Attard, G., Danila, D. C., Oommen, N. B., Olmos, D., Fong, P. C., Molife, L. R., Hunt, J., Messiou, C., Parker, C., et al. (2010) · Journal of Clinical Oncology · doi:10.1200/jco.2009.24.6819 · Cited by 394 · see citing works
Self-citationGleghorn, J. P., Pratt, E. D., Denning, D., Liu, H., Bander, N. H., Tagawa, S. T., Nanus, D. M., Giannakakou, P., & Kirby, B. J. (2009) · Lab on a Chip · doi:10.1039/b917959c · Cited by 396 · see citing works
Single Cell Isolation and Analysis
Hu, P., Zhang, W., Xin, H., & Deng, G. Y. (2016) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2016.00116 · Cited by 381 · see citing works
Gupta, V., Jafferji, I., Garza, M., Melnikova, V. O., Hasegawa, D. K., Pethig, R., & Davis, D. W. (2012) · Biomicrofluidics · doi:10.1063/1.4731647 · Cited by 384 · see citing works
A new device for rapid isolation by size and characterization of rare circulating tumor cells.
Desitter, I., Guerrouahen, B. S., Benali-Furet, N., Wechsler, J., Janne, P. A., Kuang, Y., Yanagita, M., Wang, L., Berkowitz, J. A., Distel, R. J., et al. (2011) · PubMed · Cited by 377 · see citing works
Targeting the PI3K/AKT Pathway for the Treatment of Prostate Cancer
Sarker, D., Reid, A. H. M., Yap, T. A., & de Bono, J. S. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-0125 · Cited by 366 · see citing works
Pierga, J., Bidard, F., Mathiot, C., Brain, E. G. C., Delaloge, S., Giachetti, S., de Crémoux, P., Salmon, R. J., Vincent‐Salomon, A., & Marty, M. E. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-0030 · Cited by 369 · see citing works
Lecharpentier, A., Vielh, P. R., Perez-Moreno, P., Planchard, D., Soria, J., & Farace, F. (2011) · British Journal of Cancer · doi:10.1038/bjc.2011.405 · Cited by 367 · see citing works
Challenges in circulating tumor cell detection by the CellSearch system
Andree, K., van Dalum, G., & Terstappen, L. W. M. M. (2015) · Molecular Oncology · doi:10.1016/j.molonc.2015.12.002 · Cited by 365 · see citing works
Microdevice for the isolation and enumeration of cancer cells from blood
Tan, S. J., Yobaş, L., Lee, G. Y. H., Ong, C. N., & Lim, C. T. (2009) · Biomedical Microdevices · doi:10.1007/s10544-009-9305-9 · Cited by 363 · see citing works
Pooled Analysis of the Prognostic Relevance of Circulating Tumor Cells in Primary Breast Cancer
Janni, W., Rack, B. K., Terstappen, L. W. M. M., Pierga, J., Taran, F., Fehm, T. N., Hall, C. S., de Groot, M. R., Bidard, F., Friedl, T. W. P., et al. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-15-1603 · Cited by 363 · see citing works
Technologies for circulating tumor cell separation from whole blood
Bankó, P., Lee, S. Y., Nagygyörgy, V., Zrínyi, M., Chae, C. H., Cho, D. H., & Telekes, A. (2019) · Journal of Hematology & Oncology · doi:10.1186/s13045-019-0735-4 · Cited by 358 · see citing works
Microfluidic, Label-Free Enrichment of Prostate Cancer Cells in Blood Based on Acoustophoresis
Augustsson, P., Magnusson, C., Antfolk, M., Lilja, H. G., & Laurell, T. (2012) · Analytical Chemistry · doi:10.1021/ac301723s · Cited by 352 · see citing works
Detecting Circulating Tumor Cells: Current Challenges and New Trends
Hong, B., & Zu, Y. (2013) · Theranostics · doi:10.7150/thno.5195 · Cited by 352 · see citing works
Xu, H., Aguilar, Z. P., Yang, L., Kuang, M., Duan, H., Xiong, Y., Wei, H., & Wang, A. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.08.076 · Cited by 381 · see citing works
Size-Selective Microcavity Array for Rapid and Efficient Detection of Circulating Tumor Cells
Hosokawa, M., Hayata, T., Fukuda, Y., Arakaki, A., Yoshino, T., Tanaka, T., & Matsunaga, T. (2010) · Analytical Chemistry · doi:10.1021/ac101222x · Cited by 344 · see citing works
Prognostic and Predictive Biomarkers in Gliomas
Śledzińska, P., Bebyn, M. G., Furtak, J., Kowalewski, J., & Lewandowska, M. A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910373 · Cited by 347 · see citing works
Ahn, J. C., Teng, P., Chen, P., Posadas, E. M., Tseng, H., Lu, S. C.-L., & Yang, J. D. (2020) · Hepatology · doi:10.1002/hep.31165 · Cited by 341 · see citing works
Microfluidic sorting and multimodal typing of cancer cells in self-assembled magnetic arrays
Saliba, A., Saïas, L., Psychari, E., Minc, N., Simon, D., Bidard, F., Mathiot, C., Pierga, J., Fraisier, V., Salamero, J., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1001515107 · Cited by 338 · see citing works
Circulating Tumor Cell Analysis in Patients with Progressive Castration-Resistant Prostate Cancer
Shaffer, D. R., Leversha, M. A., Danila, D. C., Lin, O., Gonzalez-Espinoza, R., Gu, B., Anand, A., Smith, K., Maslak, P. G., Doyle, G. V., et al. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-2701 · Cited by 338 · see citing works
Circulating Tumor Cell as a Diagnostic Marker in Primary Lung Cancer
Tanaka, F., Yoneda, K., Kondo, N., Hashimoto, M., Takuwa, T., Matsumoto, S., Okumura, Y., Rahman, S., Tsubota, N., Tsujimura, T., et al. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-1095 · Cited by 333 · see citing works
Zhang, N., Deng, Y., Tai, Q., Cheng, B., Zhao, L., Shen, Q., He, R., Hong, L., Liu, W., Guo, S., et al. (2012) · Advanced Materials · doi:10.1002/adma.201200155 · Cited by 331 · see citing works
Biology, vulnerabilities and clinical applications of circulating tumour cells
Ring, A., Nguyen-Sträuli, B. D., WICKI, A. N., & Aceto, N. (2022) · Nature reviews. Cancer · doi:10.1038/s41568-022-00536-4 · Cited by 334 · see citing works
Global Gene Expression Profiling of Circulating Tumor Cells
Smirnov, D. A., Zweitzig, D. R., Foulk, B. W., Miller, M. C., Doyle, G. V., Pienta, K. J., Meropol, N. J., Weiner, L. M., Cohen, S. J., Moreno, J. G., et al. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-4330 · Cited by 330 · see citing works
Thompson, J. C., Yee, S. S., Troxel, A. B., Savitch, S. L., Fan, R., Balli, D., Lieberman, D. B., Morrissette, J. D., Evans, T. L., Bauml, J., et al. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-1231 · Cited by 325 · see citing works
Considerations in the development of circulating tumor cell technology for clinical use
Parkinson, D. R., Dracopoli, N. C., Petty, B. G., Compton, C. C., Cristofanilli, M., Deisseroth, A., Hayes, D. F., Kapke, G. F., Kumar, P. K. M., Lee, J. S. H., et al. (2012) · Journal of Translational Medicine · doi:10.1186/1479-5876-10-138 · Cited by 323 · see citing works
Goldkorn, A., Ely, B., Quinn, D. I., Tangen, C. M., Fink, L. M., Xu, T., Twardowski, P. W., Veldhuizen, P. J. V., Agarwal, N., Carducci, M. A., et al. (2014) · Journal of Clinical Oncology · doi:10.1200/jco.2013.51.7417 · Cited by 321 · see citing works
Circulating Tumor Cells: A Useful Predictor of Treatment Efficacy in Metastatic Breast Cancer
Liu, M., Shields, P. G., Warren, R. D., Cohen, P., Wilkinson, M. J., Ottaviano, Y. L., Rao, S. B., Eng‐Wong, J., Seillier‐Moiseiwitsch, F., Noone, A., et al. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2008.20.6664 · Cited by 319 · see citing works
Cancer genomics: one cell at a time
Navin, N. E. (2014) · Genome biology · doi:10.1186/s13059-014-0452-9 · Cited by 311 · see citing works
Circulating tumor cells: a window into cancer biology and metastasis
Maheswaran, S., & Haber, D. A. (2010) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2009.12.002 · Cited by 316 · see citing works
Fundamentals and application of magnetic particles in cell isolation and enrichment: a review
Plouffe, B. D., Murthy, S. K., & Lewis, L. H. (2015) · Reports on Progress in Physics · doi:10.1088/0034-4885/78/1/016601 · Cited by 334 · see citing works
cke, K. L. ⁄. (2012) · International Journal of Oncology · doi:10.3892/ijo.2012.1557 · Cited by 314 · see citing works
Review: Biological relevance of disseminated tumor cells in cancer patients
Riethdorf, S., Wikman, H., & Pantel, K. (2008) · International Journal of Cancer · doi:10.1002/ijc.23825 · Cited by 310 · see citing works
Hepatocellular carcinoma: old friends and new tricks
Kim, E., & Viatour, P. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-00527-1 · Cited by 309 · see citing works
Hofman, V., Ilié, M., Long-Mira, É., Selva, É., Bonnetaud, C., Molina, T. J., Vénissac, N., Mouroux, J., Vielh, P. R., & Hofman, P. M. (2010) · International Journal of Cancer · doi:10.1002/ijc.25819 · Cited by 305 · see citing works
Qi, L., Xiang, B., Wu, F., Ye, J., Zhong, J., Wang, Y., Chen, Y., Chen, Z.-S., Ma, L., Chen, J., et al. (2018) · Cancer Research · doi:10.1158/0008-5472.can-17-2459 · Cited by 304 · see citing works
Fluid biopsy in patients with metastatic prostate, pancreatic and breast cancers
Marrinucci, D. C., Bethel, K. J., Kolatkar, A. R., Luttgen, M. S., Malchiodi, M., Baehring, F., Voigt, K., Lazar, D. C., Nieva, J. J., Bazhenova, L. A., et al. (2012) · Physical Biology · doi:10.1088/1478-3975/9/1/016003 · Cited by 303 · see citing works
The detection of EpCAM+ and EpCAM– circulating tumor cells
de Wit, S., van Dalum, G., Lenferink, A. T. M., Tibbe, A. G. J., Hiltermann, T. J. N., Groen, H. J. M., van Rijn, C. J. M., & Terstappen, L. W. M. M. (2015) · Scientific Reports · doi:10.1038/srep12270 · Cited by 294 · see citing works
Molecular Biomarker Analyses Using Circulating Tumor Cells
Punnoose, E. A., Atwal, S. K., Spoerke, J. M., Savage, H. M., Pandita, A., Yeh, R., Pirzkall, A., Fine, B. M., Amler, L. C., Chen, D. S., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012517 · Cited by 294 · see citing works
Double spiral microchannel for label-free tumor cell separation and enrichment
Sun, J., Li, M., Liu, C., Zhang, Y., Liu, D., Liu, W., Hu, G., & Jiang, X. (2012) · Lab on a Chip · doi:10.1039/c2lc40679a · Cited by 293 · see citing works
Scully, O. J., Bay, B., Yip, G., & Yu, Y. (1926) · The American Journal of Surgery · doi:10.1016/s0002-9610(26)90068-8 · Cited by 293 · see citing works
- Authors
- Allard, W. J., Matera, J., Miller, M. C., Repollet, M., Connelly, M. C., Rao, C., Tibbe, A. G. J., Uhr, J. W., & Terstappen, L. W. M. M.
- Affiliations
- 1Immunicon Corporation, Huntingdon Valley, Pennsylvania; and
- The University of Texas Southwestern Medical Center (US)
- Venue
- Clinical Cancer Research
- Published
- 2004-10-15
- Volume
- 10
- Issue
- 20
- Pages
- 6897-6904
- ISSN
- 1078-0432 (ISSN-L)
- 1557-3265
- OpenAlex
- W2116483002
- Cited by
- 2,542
- References
- 30
- Citations by year
- 2026: 66 · 2025: 81 · 2024: 87 · 2023: 135 · 2022: 117 · 2021: 158 · 2020: 169 · 2019: 166 · 2018: 171 · 2017: 193 · 2016: 197 · 2015: 165 · 2014: 177 · 2013: 161 · 2012: 132
- FWCI
- 7.52
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Clinical Cancer Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Physical Sciences › Engineering › Biomedical Engineering › Microfluidic and Bio-sensing Technologies
- Keywords
- circulating tumor cells, CellSearch, metastatic carcinoma, prostate cancer, breast cancer, ovarian cancer, colorectal cancer, lung cancer, liquid biopsy
- MeSH terms
- Adult, Automation, Biological Assay, Carcinoma, Cytological Techniques, Female, Humans, Male, Middle Aged, Neoplastic Cells, Circulating, Neoplasm Metastasis, Sensitivity and Specificity, Reproducibility of Results, Case-Control Studies
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