Isolation of rare circulating tumor cells in cancer patients: Technical aspects and clinical implications

Expert Review of Molecular Diagnostics

Volumn 11, Issue 5, 2011, Pages 473-485

  Danova, Marco ^a   Torchio, Martina ^a   Mazzini, Giuliano ^b  

^a Ospedale Civile   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

Author keywords

biological characterization; biomarker; circulating tumor cell; detection method; metastasis; solid tumor

Indexed keywords

ANTIBODY; EPITHELIAL CELL ADHESION MOLECULE; TUMOR MARKER;

CANCER DIAGNOSIS; CANCER PATIENT; CANCER STAGING; CELL DENSITY; CELL ISOLATION; CELL SEPARATION; CIRCULATING TUMOR CELL; ENRICHMENT CULTURE; EPITHELIUM TUMOR; HUMAN; IMMUNOMAGNETIC SEPARATION; MEDICAL TECHNOLOGY; METASTASIS; METHODOLOGY; ONCOLOGY; REVIEW; TECHNIQUE; TECHNOLOGY;

ANTIBODIES, NEOPLASM; CELL SEPARATION; DISEASE PROGRESSION; GENE EXPRESSION PROFILING; HUMANS; MOLECULAR DIAGNOSTIC TECHNIQUES; NEOPLASM METASTASIS; NEOPLASMS; NEOPLASTIC CELLS, CIRCULATING; PROGNOSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 79959781149     PISSN: 14737159     EISSN: 17448352     Source Type: Journal    
DOI: 10.1586/erm.11.33     Document Type: Review

References (109)

1. Gerges N, Jabado N. Biomarkers in cancer micrometastasis: where are we at? Bioanalysis 2, 881-899 (2010
2. Criscitiello C, Sotirou C, Ignatiadis M. Circulating cancer cells and emerging blood biomarkers in breast cancer. Curr. Opin. Oncol. 22, 552-558 (2010
3. Allard WJ, Matera J, Miller MC et al. Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin. Cancer Res. 10, 6897-6904 (2004
4. Elshimali YI, Grody WW. The clinical significance of circulating tumor cells in the peripheral blood. Diagn. Mol. Pathol. 15, 187-194 (2006
5. Paterlini-Brechot P, Benali NL. Circulating tumor cells (CTC) detection: clinical impact and future directions. Cancer Lett. 253, 180-204 (2007
6. Andreopoulov E, Cristofanilli M. Circulating tumor cells as prognostic markers in metastatic breast cancer. Exp. Rev. Anticancer Therapy 10, 171-177 (2010
7. Mavroudis D. Circulating cancer cells. Ann. Oncol. 21(Suppl. 7), vii95-vii100 (2011
8. Cristofanilli M, Braun S. Circulating tumor cells revisited. JAMA 303, 1092-1093 (2010
9. Jacob K, Sollier C, Jabado N. Circulating tumor cells: detection, molecular profiling and future prospects. Expert Rev. Proteomics 4, 741-756 (2007
10. Mata M, Raponi M. Circulating tumor cells: utility for predicting response to anti-EGFR therapies? Expert Rev. Mol. Diagn. 9, 115-119 (2009
11. Stakeborg T, Liu C, Henry O et al. Automated genotyping of circulating tumor cells. Expert Rev. Mol. Diagn. 10, 723-729 (2010
12. Ignatiadis M, Rothè F, Chaboteaux C et al. HER-positive circulating tumor cells in breast cancer. PLoS One 6, 1-6 (2011
13. Den Tonder, J. Circulating tumor cells: the Grand Challenge. Lab. Chip 11, 375-377 (2011
14. Sieuwerts AM, Kraan J, Bolt J et al. Anti-epithelial cell adhesion molecule antibodies and the detection of circulating normal-like breast tumour cells. J. Natl Cancer Inst. 101, 61-66 (2009
15. Dotan E, Cohen SJ, Alpaugh KR, Meropol NJ. Circulating tumor cells: evolving evidence and future challenges. Oncologist 14, 1070-1082 (2009
16. Barok M, Szollosi J. Steps in metastasis research: analyzing, collecting and culturing circulating tumor cells. Cytometry Part A 79A, 93-94 (2011
17. Yu M, Stott S, Toner M, Maheswaran S, Haber DA. Circulating tumor cells: approaches to isolation and characterization. J. Cell. Biol. 192, 373-382 (2011
18. Nelson NJ. Circulating tumor cells: will they be clinically useful? J. Natl Cancer Inst. 102, 146-148 (2010
19. Riethdorf S, Pantel K. Advancing personalized cancer therapy by detection and characterization of circulating carcinoma cells. Ann. NY Acad. Sci. 1210, 66-77 (2010
20. Lin H, Balic M, Zheng S, Datar R, Cote RJ. Disseminated and circulating tumor cells: role in effective cancer management. Crit. Rev. Oncol. Hematol. 77, 1-11 (2011).
21. Alunni-Fabbroni M, Sandri MT. Circulating tumour cells in clinical practice: methods of detection and possible characterization. Methods 50, 289-297 (2010
22. Gerges N, Rak J, Jabado N. New technologies for the detection of circulating tumor cells. Br. Med. Bull. 94, 49-64 (2010
23. Rosenberg R, Gertler R, Friederichs J et al. Comparison of two density gradient centrifugation systems for the enrichment of disseminated tumor cells in blood. Cytometry 49, 150-158 (2002
24. Gertler R, Rosenberg R, Fuehrer K et al. Detection of circulating tumor cells in blood using an optimized density gradient centrifugation. Recent Results Cancer Res. 162, 149-155 (2003
25. Zheng S, Lin H, Liu JQ et al. Membrane microfilter device for selective capture, electrolysis and genomic analysis of human circulating tumor cells. J. Chromatogr. A. 1162, 154-161 (2007
26. Wong NS, Kahn HJ, Zhang L et al. Prognostic significance of circulating tumour cells enumerated after filtration enrichment in early and metastatic breast cancer patients. Breast Cancer Res. Treat. 99, 63-69 (2006
27. De Giorgi V, Pinzani P, Salvianti F et al. Application of a filtration- and isolation-by-size tehcnique for the detection of circulating tumor cells in cutaneous melanoma. J. Invest. Dermatol. 130, 2440-2447 (2010
28. Xu T, Lu B, Tai YC, Goldkorn A. A cancer detection platform which measures telomerase activity from live circulating tumor cells captured on a microfilter. Cancer Res. 70, 6420-6426 (2010
29. Zheng S, Lin HK, Lu et al. 3D microfilter device for viable circulating tumor cell (CTC) enrichment from blood. Biomed. Microdevices 13, 203-213 (2011
30. Martin VM, Siewert C, Scharl A et al. Immunomagnetic enrichment of disseminated epithelial tumor cells from peripheral blood by MACS. Exp. Hematol. 26, 252-264 (1998
31. Königsberg R, Gneist M, Jahn-Kuch D et al. Circulating tumor cells in metastatic colorectals cancer: efficacy and feasibility of different enrichment methods. Cancer Lett. 293, 117-123 (2010
32. Talasaz AH, Powell AA, Huber DE et al. Isolating highly enriched populations of circulating epithelial cells and other rare cells from blood using a magnetic sweeper device. PNAS 106, 3970-3975 (2009
33. Cristofanilli M, Budd GT, Ellis MJ et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N. Engl. J. Med. 351, 781-791 (2004
34. Miller MC, Doyle GV, Terstappen LW. Significance of circulating tumor cells detected by the CellSearchTM system in patients with metastatic breast colorectal and prostate cancer. J. Oncol. 2010, 617421 (2010
35. Kraan J, Sleijfer S, Strijbos MH et al. External quality assurance of circulating tumor cell enumeration using the CEllSearchTM system: a feasibility study. Cytometry B. Clin. Cytom. 80(2), 112-118 (2010
36. Mostert B, Kraan J, Bolt-de-Vries J et al. Detection of circulating tumour cells in breast cancer may improve through enrichment with anti-CD146. Breast Cancer Res. Treat. 127(1), 33-41 (2010
37. Obermayr E, Sanchez-Cabo F, Tea MK et al. Assessment of a six-gene panel for the molecular detection of circulating tumor cells in the blood of female cancer patients. BMC Cancer 10, 666 (2010
38. Simpson SJ, Vachula M, Kennedy MJ et al. Detection of tumor cells in the bone marrow, peripheral blood and apheresis products of breast cancer patients using flow cytometry. Exp. Hematol. 23, 1062-1068 (1995
39. Basiji DA, Ortyn WE, Liang L, Venkatachalam V, Morrissey P. Cellular Image analysis and imaging by flow cytometry. Clin. Lab. Med. 27, 653-669 (2007
40. Will B, Steidl U. Multiparameter fluorescence-activated cell sorting and analysis of stem and progenitor cells in myeloid malignancies. Best Pract. Res. Clin. Hematol. 23, 391-401 (2010
41. Cruz I, Ciudad J, Cruz J et al. Evaluation of multiparameter flow cytometry for the detection of breast cancer tumor cells in blood samples. Am. J. Clin. Pathol. 123, 66-74 (2005
42. Allan AL, Vantyghem SA, Tuck AB, Chambers AP, Chin-Yee IH, Kenney M. Detection and quantification of circulating tumor cells in mouse models of human breast cancer using immunomagnetic enrichment and multiparameter flow cytometry. Cytometry A 65, 4-14 (2005
43. Wang L, Wang Y, Liu Y, Chang M, Wu X, Wie H. Flow cytometric analysis of CK19 expression in the peripheral blood of breast carcinoma patients. Relevance for circulating tumor cell detection. J. Exp. Clin. Cancer Res. 28, 28-57 (2009
44. Hu Y, Fan L, Zheng J et al. Detection of circulating tumor cells in breast cancer patients utilizing multiparameter flow cytometry and assessment of the prognosis of patients in different CTC levels. Cytometry A 77, 213-219 (2010
45. Wu LY, Liu T, Grimm AL, Davis WC, Berkman CE. Flow cytometric detection of prostate tumor cells using chemoaffinity labels. Prostate 71, 52-61 (2011
46. Takao M, Takeda K. Enumeration, characterization and collection of intact circulating tumor cells by cross contamination-free flow cytometry. Cytometry A 79, 107-117 (2011
47. Kraeft SK, Ladanyi A, Galiger K et al. Reliable and sensitive identification of occult tumor cells using the improved rare event imaging system. Clin. Cancer Res. 10, 3020-3028 (2004
48. Pachmann K, Clement JH, Schneider CP et al. Standardized quantification of circulating peripheral tumor cells from lung and breast cancer. Clin. Chem. Lab. Med. 43, 617-627 (2005
49. Scholtens TM, Schreuder F, Ligthart ST et al. CellTracks TDI: an image cytometer for cell characterization. Cytometry A DOI: 10.1002/cyto.a.21024 (2011) (Epub ahead of print
50. Smith B, Selby P, Southgate J, Pittman K, Bradley C, Blair GE. Detection of melanoma cells in peripheral blood by means of reverse-transcriptase and polymerase chain reaction. Lancet 338, 1227-1229 (1991
51. Sergeant G, Penninckx F, Topal B. Quantitative RT-PCR detection of colorectal tumor cells in peripheral blood: a systematic review. J. Surg. Res. 150, 144-152 (2008
52. 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. 25, 5194-5202 (2007
53. 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. 27, 2177-2184 (2009
54. Ignatiadis M, Kallergi G, Ntoulia M et al. Prognostic value of the molecular detection of circulating tumor cells using a multimarker reverse transcription-PCR assay for cytokeratin 19, mammaglobin A, and HER2 in early breast cancer. Clin. Cancer Res. 14, 2593-2600 (2008
55. Lambrechts AC, Bosma AJ, Klaver SG et al. Comparison of immunocytochemistry, reverse trascriptase polymerase chain reaction, and nucleic acid sequence-based amplification for the detection of circulating breast cancer cells. Breast Cancer Res. Treat. 56, 219-231 (1999
56. Panteleakou Z, Lembessis P, Sourla A et al. Detection of circulating tumor cells in prostate cancer patients: methodological pitfalls and clinical relevance. Mol. Med. 15, 101-114 (2009
57. Ross JS, Slodkowska EA. Circulating and disseminated tumor cells in the management of breast cancer. Am. J. Clin. Pathol. 132, 237-245 (2009
58. Alix-Panabieres C, Riethdorf S, Pantel K. Circulating tumor cells and bone marrow micrometastases. Clin. Cancer Res. 14, 5013-5021 (2008
59. Pantel K, Alix-Panabieres C. The clinical significance of circulating tumor cells. Nat. Clin. Pract. Oncol. 4, 62-63 (2007
60. Hauch S, Zimmermann S, Lankiewicz S, Zieglschmid V, Bocher O, Winfried HA. The clinical significance of circulating tumor cells in breast cancer and colorectal cancer patients. Anticancer Res. 27, 1337-1341 (2007
61. Kojima T, Hashimoto Y, Watanabe Y et al. A simple biological imaging system for detecting viable human circulating tumor cells. J. Clin. Invest. 119, 3172-3181 (2009
62. Nagrath S, Sequist LV, Maheswaran S et al. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 450, 1235-1239 (2007
63. Maheswaran S, Sequist LV, Nagrath S et al. Detection of mutations in EGFR in circulating lung-cancer cells. N. Engl. J. Med. 359, 366-377 (2008
64. Sequist LV, Nagrath S, Toner M, Haber DA, Lynch TJ. The CTC-chip: an exciting new tool to detect circulating tumor cells in lung cancer patients. J. Thorac. Oncol. 4, 281-283 (2009
65. Stott SL, Lee JR, Nagrath S et al. Isolation and characterization of circulating tumour cells from patients with localized and metastatic prostate cancer. Sci. Transl. Med. 2(25), 25ra23 (2010
66. Chatzileontiadou S, Defanti S, Manzoni M et al. Circulating tumour cells in cancer patients: methodological contributions to their detection and immunomagnetic separation. Cytometry 77A, 194-195 (2010
67. Stott SL, Hsu CH, Tsukrov DI et al. Isolation of circulating tumour cells using a microvortex-generating herringbone-chip. PNAS 107, 18392-18397 (2010
68. Jin D, Piper JA, Leif RC et al. Time-gated flow cytometry: an ultra high selectivity method to recover ultra-rare-event μ-targets in high-background biosamples. J. Biomed. Opt. 14, 24-28 (2009
69. Liu G, Mao X, Phillips JA, Xu H, Tan W, Zeng L. Aptamer-nanoparticle strip biosensor for sensitive detection of cancer cells. Anal. Chem. 81, 10013-10018 (2009
70. Deng T, Li J, Zhang LL et al. A sensitive fluorescence anisotropy method for the direct detection of cancer cells in whole blood based on aptamer-conjugated near-infrared fluorescent nanoparticles. Biosens. Bioelectron. 25, 1587-1591 (2010
71. Eifler RL, Lid J, Falkenhagen D, Weber W, Fischer MB, Zeillinger R. Enrichment of circulating tumor cells from a large blood volume using leukapheresis and elutriation: proof of concept. Cytometry B Clin. Cytom. 80(2), 100-111 (2010
72. Zimmerlin L, Donnenberg VS, Donnenberg AD. Rare event detection and analysis in flow cytometry: bone marrow mesenchymal stem cells, breast cancer stem/progenitor cells in malignant effusions, and pericytes in disaggregate adipose tissue. Methods Mol. Biol. 699, 251-273 (2011
73. Wang X, Qiang X, Beitler JJ et al. Detection of circulating tumor cells in human peripheral blood using surface-enhanced raman scattering nanoparticles. Cancer Res. 71(5), 1526-1532 (2011
74. Hsieh YH, Liu SJ, Chen HW, Lin YK, Liang KS, Lai LJ. Highly sensitive rare cell detection based on quantum dot probe fluorescence analysis. Anal. Bioanal. Chem. 396, 1135-1141 (2010
75. Bao N, Le TT, Cheng JX, Lu C. Microfluidic electroporation of tumor and blood cells: observation of nucleus expansion and implications on selective analysis and purging of circulating tumor cells. Integr. Biol. 2, 113-120 (2010
76. Hosokawa M, Hayata T, Fukuda Y et al. Size-selective microcavity array for rapid and efficient detection of circulating tumor cells. Anal. Chem. 82, 6629-6635 (2010
77. Breton F, Bennettau B, Liderau R et al. A mesofluidic multiplex immunosensor for detection of circulating cytokeratin-positive cells in the blood of breast cancer patients. Biomed. Microdevices 13(1), 1-9 (2010
78. Lin HK, Zheng S, Williams AJ et al. Portable filter-based microdevice for detection and characterization of circulating tumor cells. Clin. Cancer Res. 16, 5011-5018 (2010
79. Chung YK, Reboud J, Lee KC et al. An electrical biosensor for the detection of circulating tumor cells. Biosens. Bioelectron. 26(5), 2520-2526 (2010
80. Moon HS, Kwon K, Kim SI et al. Continuous separation of breast cancer cells from blood samples using multi-orifice flow fractionation (MOFF) and dielectrophoresis (DEPLab. Chip 11(6), 1118-1125 (2011
81. Dharmasiri U, Njoroge SK, Witek MA et al. High-throughput selection, enumeration, electrokinetic manipulation, and molecular profiling of low-abundance circulating tumor cells using a microfluidic system. Anal. Chem. 83(6), 2301-2309 (2011
82. Galanzha EI, Shashkov EV, Kelly T, Kim JW, Yang L, Zharov VP. In vivo magnetic enrichment and multiplex photoacoustic detection of circulating tumor cells. Nat. Nanotechnol. 4, 855-860 (2009
83. Zemp RJ. Nanomedicine: detecting rare cancer cells. Nat. Nanotechnol. 4, 798-799 (2009
84. 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. 20, 3404-3412 (2002
85. 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. 24, 3756-3762 (2006
86. Chen Y, Zou TN, Wu ZP et al. Detection of cytokeratin 19, human mammaglobin and carcinoembryonic antigen-positive circulating tumor cells by three-marker reverse transcription-PCR assay and its relation to clinical outcome in early breast cancer. Int. J. Biol. Markers 25, 59-68 (2010
87. Hayes DF, Smerage JR. Is there a role for circulating tumor cells in the management of breast cancer? Clin. Cancer Res. 14, 57-70 (2008).
88. Krishnamurthy S, Cristofanilli M, Singh B et al. Detection of minimal residual disease in blood and bone marrow in early stage breast cancer. Cancer 116, 3330-3333 (2010
89. Zhao S, Liu Y, Zhang Q et al. The prognostic role of circulating tumor cells (CTC) detected by RT-PCR in breast cancer: a meta-analysis of published literature. Breast Cancer Res. Treat. DOI: 10.1007/s10549-011-1379-4 (2011) (Epub ahead of print
90. Allen-Mersh TG, McCullough TK, Patel H et al. Role of circulating tumour cells in predicting recurrence after excision of primary colorectal carcinoma. Br. J. Surg. 94, 96-105 (2007
91. Rahbari NN, Aigner M, Thorlund K et al. Meta-analysis shows that detection of circulating tumor cells indicates poor prognosis in patients with colorectal cancer. Gastroenterology 138, 1714-1726 (2010
92. Allen JE, El-Deiry W. Circulating tumor cells and colorectal cancer. Curr. Colorectal Cancer Rep. 6, 212-220 (2010
93. Garrigos N, Gallego J, Guillen-Ponce C et al. Circulating tumor cell analysis as an early marker for relapse in stage II and III colorectal cancer patients: a pilot study. Clin. Transl. Oncol. 12, 142-147 (2010
94. Thorsteinsson M, Jess P. The clinical significance of circulating tumor cells in non metastatic colorectal cancer - a review. Eur. J. Cancer Surg. DOI:10.1016/j.ejso.2011.01.025 (2011) (Epub ahead of print
95. Helo P, Cronin AM, Danila DC et al. Circulating prostate tumor cells detected by reverse transcription-PCR in men with localized or castration-refractory prostate cancer: concordance with CellSearch assay and association with bone metastases and with survival. Clin. Chem. 55, 765-773 (2009
96. Graves H, Czerniecki BJ. Circulating tumor cells in breast cancer patients: an evolving role in patient prognosis and disease progression. Patholog. Res. Int. 2011, 621090 (2011
97. Harris L, Fritsche H, Mennel R et al. American Society of Clinical Oncology 2007 update of recommendations for the use of tumor markers in breast cancer. J. Clin. Oncol. 25, 5287-5312 (2007
98. Armakolas A, Panteleakou Z, Nazos A et al. Detection of the circulating tumor cells in cancer patients. Future Oncol. 6, 1849-1856 (2010
99. Cristofanilli M, Hayes DF, Budd GT et al. Circulating tumor cells: a novel prognostic factor for newly diagnosed metastatic breast cancer. J. Clin. Oncol. 23, 1420-1430 (2005
100. De Bono JS, Scher HI, Montgomery RB et al. Circulating tumor cells predict survival benefit for treatment in metastatic castration resistant prostate cancer. Clin. Cancer Res. 14, 6302-6309 (2008
101. Cohen SJ, Punt CJ, Iannotti N et al. Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer. J. Clin. Oncol. 26, 3213-3221 (2008
102. 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. 12, 4218-4224 (2006
103. Budd GT, Cristofanilli M, Ellis MJ et al. Circulating tumor cells versus imaging in predicting overall survival in metastatic breast cancer. Clin. Cancer Res. 12, 6403-6409 (2006
104. Fehm T, Becker S, Duerr-Stoerzer S et al. Determination of HER2 status using both serum HER2 levels and circulating tumor cells in patients with recurrent breast cancer whose primary tumor was HER2 negative or of unknown HER2 status. Breast Cancer Res. 9, R74 (2007
105. Ignatiadis M, Rothè F, Chaboteaux C et al. HER2-positive circulating tumor cells in breast cancer. PLoS One 6, 1-6 (2011
106. Dawood S, Broglio K, Valero V et al. Circulating tumor cells in metastatic breast cancer: from prognostic stratification to modification of the staging system? Cancer 113, 2422-2430 (2008
107. 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. 10, 233-239 (2009
108. Cohen SJ, Punt CJ, Iannotti N et al. Prognostic significance of circulating tumor cells in patients with metastatic colorectal cancer. Ann. Oncol. 20, 1223-1229 (2009
109. Attard G, de Bono JS. Utilizing circulating tumor cells: challenges and pitfalls. Curr. Opin. Genet. Dev. 21, 50-58 (2011).