Meta-analysis of the prognostic value of circulating tumor cells in breast cancer

Clinical Cancer Research

Volumn 18, Issue 20, 2012, Pages 5701-5710

  Zhang, Liling ^a   Riethdorf, Sabine ^b   Wu, Gang ^a   Wang, Tao ^a   Yang, Kunyu ^a   Peng, Gang ^a   Liu, Junli ^a   Pantel, Klaus ^b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BLOOD SAMPLING; BREAST CANCER; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; CIRCULATING TUMOR CELL; DISEASE FREE SURVIVAL; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; SENSITIVITY ANALYSIS; SYSTEMATIC REVIEW;

BREAST NEOPLASMS; DISEASE-FREE SURVIVAL; FEMALE; HUMANS; NEOPLASM METASTASIS; NEOPLASM STAGING; NEOPLASTIC CELLS, CIRCULATING; PROGNOSIS;

EID: 84867556074     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-12-1587     Document Type: Article

References (59)

1. Braun S, Vogl FD, Naume B, Janni W, Osborne MP, Coombes RC, et al. A pooled analysis of bone marrow micrometastasis in breast cancer.N Engl J Med 2005;353:793-802. (Pubitemid 41215488)
2. Ashworth TA. A case of cancer in which cells similar to those in the tumors were seen in the blood after death. Aust Med J 1869;14:146-9.
3. Harris L, Fritsche H, Mennel R, Norton L, Ravdin P, Taube S, et al. American Society of Clinical Oncology 2007 update of recommendations for the use of tumor markers in breast cancer. J Clin Oncol 2007;25:5287-312. (Pubitemid 350232263)
4. Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Matera J, Miller MC, et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med 2004;351:781-91. (Pubitemid 39095313)
5. Cristofanilli M, Hayes DF, Budd GT, Ellis MJ, Stopeck A, Reuben JM, et al. Circulating tumor cells: a novel prognostic factor for newly diagnosed metastatic breast cancer. J Clin Oncol 2005;23:1420-30.
6. Hayes DF, Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Miller MC, et al. Circulating tumor cells at each follow-up time point during therapy of metastatic breast cancer patients predict progression-free and overall survival. Clin Cancer Res 2006;12:4218-24.
7. Budd GT, Cristofanilli M, Ellis MJ, Stopeck A, Borden E, Miller MC, et al. Circulating tumor cells versus imaging - Predicting overall survival in metastatic breast cancer. Clin Cancer Res 2006;12:6403-9. (Pubitemid 44799711)
8. Bidard FC, Vincent-Salomon A, Sigal-Zafrani B, Dieras V, Mathiot C, Mignot L, et al. Prognosis of women with stage IV breast cancer depends on detection of circulating tumor cells rather than disseminated tumor cells. Ann Oncol 2008;19:496-500. (Pubitemid 351325670)
9. Yagata H, Nakamura S, Toi M, Bando H, Ohno S, Kataoka A. Evaluation of circulating tumor cells in patients with breast cancer: multi-institutional clinical trial in Japan. Int J Clin Oncol 2008;13:252-6. (Pubitemid 351871893)
10. Botteri E, Sandri MT, Bagnardi V, Munzone E, Zorzino L, Rotmensz N, et al. Modeling the relationship between circulating tumour cells number and prognosis of metastatic breast cancer. Breast Cancer Res Treat 2010;122:211-7.
11. Wulfing P, Borchard J, Buerger H, Heidl S, Zanker KS, Kiesel L, et al. HER2-positive circulating tumor cells indicate poor clinical outcome in stage I to III breast cancer patients. Clin Cancer Res 2006;12:1715-20.
12. Xenidis N, Perraki M, Kafousi M, Apostolaki S, Bolonaki I, Stathopoulou A, et al. Predictive and prognostic value of peripheral blood cytokeratin-19 mRNA-positive cells detected by real-time polymerase chain reaction in node-negative breast cancer patients. J Clin Oncol 2006;24:3756-62. (Pubitemid 46622314)
13. Xenidis N, Ignatiadis M, Apostolaki S, Perraki M, Kalbakis K, Agelaki S, et al. Cytokeratin-19 mRNA-positive circulating tumor cells after adjuvant chemotherapy in patients with early breast cancer. J Clin Oncol 2009;27:2177-84.
14. Pierga JY, Bonneton C, Vincent-Salomon A, de Cremoux P,Nos C, Blin N, et al. Clinical significance of immunocytochemical detection of tumor cells using digital microscopy in peripheral blood and bone marrow of breast cancer patients. Clin Cancer Res 2004;10:1392-400. (Pubitemid 38365234)
15. Benoy IH, Elst H, Philips M, Wuyts H, Van Dam P, Scharpe S, et al. Real-time RT-PCR detection of disseminated tumour cells in bone marrow has superior prognostic significance in comparison with circulating tumour cells in patients with breast cancer. Br J Cancer 2006;94:672-80. (Pubitemid 43361898)
16. Serrano MJ, Sanchez-Rovira P, Delgado-Rodriguez M, Gaforio JJ. Detection of circulating tumor cells in the context of treatment Prognostic value in breast cancer. Cancer Biol Ther 2009;8:671-5.
17. Marques AR, Teixeira E, Diamond J, Correia H, Santos S, Neto L, et al. Detection of human mammaglobin mRNA in serial peripheral blood samples from patients with non-metastatic breast cancer is not predictive of disease recurrence. Breast Cancer Res Treat 2009;114:223-32.
18. Ntoulia M, Stathopoulou A, Ignatiadis M, Malamos N, Mavroudis D, Georgoulias V, et al. Detection of Mammaglobin A-mRNA-positive circulating tumor cells in peripheral blood of patients with operable breast cancer with nested RT-PCR. Clin Biochem 2006;39:879-87. (Pubitemid 44363084)
19. Chen Y, Zou TN, Wu ZP, Zhou YC, Gu YL, Liu X, et al. Detection of cytokeratin 19, human mammaglobin, and carcinoembryonic antigen-positive circulating tumor cells by three-marker reverse transcription-PCRassay and its relation to clinical outcome in early breast cancer. Int J Biol Markers 2010;25:59-68.
20. Gradilone A, Naso G, Raimondi C, Cortesi E, Gandini O, Vincenzi B, et al. Circulating tumor cells (CTCs) in metastatic breast cancer (MBC): prognosis, drug resistance and phenotypic characterization. Ann Oncol 2011;22:86-92.
21. Mego M, De Giorgi U, Dawood S, Wang X, Valero V, Andreopoulou E, et al. Characterization of metastatic breast cancer patients with non-detectable circulating tumor cells. Int J Cancer 2011;129:417-23.
22. Parmar MK, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival end-points. Stat Med 1998;17:2815-34. (Pubitemid 28562978)
23. Apostolaki S, Perraki M, Pallis A, Bozionelou V, Agelaki S, Kanellou P, et al. Circulating HER2 mRNA-positive cells in the peripheral blood of patients with stage I and II breast cancer after the administration of adjuvant chemotherapy: evaluation of their clinical relevance. Ann Oncol 2007;18:851-8. (Pubitemid 47054081)
24. Apostolaki S, Perraki M, Kallergi G, Kafousi M, Papadopoulos S, Kotsakis A, et al. Detection of occult HER2 mRNA-positive tumor cells in the peripheral blood of patients with operable breast cancer: evaluation of their prognostic relevance. Breast Cancer Res Treat 2009;117:525-34.
25. Stathopoulou A, Vlachonikolis I, Mavroudis D, Perraki M, Kouroussis C, Apostolaki S, et al. Molecular detection of cytokeratin-19-positive cells in the peripheral blood of patients with operable breast cancer: evaluation of their prognostic significance. J Clin Oncol 2002;20:3404-12.
26. Gaforio JJ, Serrano MJ, Sanchez-Rovira P, Sirvent A, Delgado-Rodriguez M, Campos M, et al. Detection of breast cancer cells in the peripheral blood is positively correlated with estrogen-receptor status and predicts for poor prognosis. Int J Cancer 2003;107:984-90. (Pubitemid 37429841)
27. Weigelt B, Bosma AJ, Hart AA, Rodenhuis S, van't Veer LJ. Marker genes for circulating tumour cells predict survival in metastasized breast cancer patients. Br J Cancer 2003;88:1091-4. (Pubitemid 36560781)
28. Xenidis N, Vlachonikolis I, Mavroudis D, Perraki M, Stathopoulou A, Malamos N, et al. Peripheral blood circulating cytokeratin-19 mRNA-positive cells after the completion of adjuvant chemotherapy in patients with operable breast cancer. Ann Oncol 2003;14:849-55. (Pubitemid 36827199)
29. Giatromanolaki A, Koukourakis MI, Kakolyris S, Mavroudis D, Kouroussis C, Mavroudi C, et al. Assessment of highly angiogenic and disseminated in the peripheral blood disease in breast cancer patients predicts for resistance to adjuvant chemotherapy and early relapse. Int J Cancer 2004;108:620-7. (Pubitemid 38036666)
30. Masuda TA, Kataoka A, Ohno S, Murakami S, Mimori K, Utsunomiya T, et al. Detection of occult cancer cells in peripheral blood and bone marrow by quantitative RT-PCR assay for cytokeratin-7 in breast cancer patients. Int J Oncol 2005;26:721-30.
31. Wiedswang G, Borgen E, Schirmer C, Karesen R, Kvalheim G, Nesland JM, et al. Comparison of the clinical significance of occult tumor cells in blood and bone marrow in breast cancer. Int J Cancer 2006;118:2013-9.
32. Wong NS, Kahn HJ, Zhang L, Oldfield S, Yang LY, Marks A, et al. Prognostic significance of circulating tumour cells enumerated after filtration enrichment in early and metastatic breast cancer patients. Breast Cancer Res Treat 2006;99:63-9. (Pubitemid 44168604)
33. Cristofanilli M, Broglio KR, Guarneri V, Jackson S, Fritsche HA, Islam R, et al. Circulating tumor cells in metastatic breast cancer: biologic staging beyond tumor burden. Clin Breast Cancer 2007;7:471-9. (Pubitemid 46424284)
34. Ignatiadis M, Perraki M, Apostolaki S, Politaki E, Xenidis N, Kafousi M, et al. Molecular detection and prognostic value of circulating cytokeratin-19 messenger RNA-positive and HER2 messenger RNA-positive cells in the peripheral blood of women with early-stage breast cancer. Clin Breast Cancer 2007;7:883-9.
35. Xenidis N, Markos V, Apostolaki S, Perraki M, Pallis A, Sfakiotaki G, et al. Clinical relevance of circulating CK-19 mRNA-positive cells detected during the adjuvant tamoxifen treatment in patients with early breast cancer. Ann Oncol 2007;18:1623-31. (Pubitemid 47506248)
36. Dawood S, Broglio K, Valero V, Reuben J, Handy B, Islam R, et al. Circulating tumor cells in metastatic breast cancer from prognostic stratification to modification of the staging system? Cancer 2008;113:2422-30.
37. Ignatiadis M, Kallergi G, Ntoulia M, Perraki M, Apostolaki S, Kafousi 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 2008;14:2593-600.
38. Tkaczuk KH, Goloubeva O, Tait NS, Feldman F, Tan M, Lum ZP, et al. The significance of circulating epithelial cells in Breast Cancer patients by a novel negative selection method. Breast Cancer Res Treat 2008;111:355-64.
39. Daskalaki A, Agelaki S, Perraki M, Apostolaki S, Xenidis N, Stathopoulos E, et al. Detection of cytokeratin-19 mRNA-positive cells in the peripheral blood and bone marrow of patients with operable breast cancer. Brit J Cancer 2009;101:589-97.
40. De Giorgi U, Valero V, Rohren E, Dawood S, Ueno NT, Miller MC, et al. Circulating tumor cells and [18F]fluorodeoxyglucose positron emission tomography/computed tomography for outcome prediction in metastatic breast cancer. J Clin Oncol 2009;27:3303-11.
41. Liu MC, Shields PG, Warren RD, Dawood S, Ueno NT, Miller MC, et al. Circulating tumor cells: a useful predictor of treatment efficacy in metastatic breast cancer. J Clin Oncol 2009;27:5153-9.
42. Tewes M, Aktas B, Welt A, Mueller S, Hauch S, Kimmig R, et al. Molecular profiling and predictive value of circulating tumor cells in patients with metastatic breast cancer: an option for monitoring response to breast cancer related therapies. Breast Cancer Res Treat 2009;115:581-90.
43. Bidard FC, Mathiot C, Delaloge S, Brain E, Giachetti S, de Cremoux P, et al. Single circulating tumor cell detection and overall survival in nonmetastatic breast cancer. Ann Oncol 2010;21:729-33.
44. Bidard FC, Mathiot C, Degeorges A, Etienne-Grimaldi MC, Delva R, Pivot X, et al. Clinical value of circulating endothelial cells and circulating tumor cells in metastatic breast cancer patients treated first line with bevacizumab and chemotherapy. Ann Oncol 2010;21:1765-71.
45. De Giorgi U, Valero V, Rohren E, Mego M, Doyle GV, Miller MC, et al. Circulating tumor cells and bone metastases as detected by FDG-PET/CT in patients with metastatic breast cancer. Ann Oncol 2010;21:33-9.
46. Hu Y, Fan L, Zheng J, Cui R, Liu W, He Y, et al. Detection of circulating tumor cells in breast cancer patients utilizing multiparameter flow cytometry and assessment of the prognosis of patients in different CTCs levels. Cytometry A 2010;77:213-9.
47. Nakamura S, Yagata H, Ohno S, Yamaguchi H, Iwata H, Tsunoda N, et al. Multi-center study evaluating circulating tumor cells as a surrogate for response to treatment and overall survival in metastatic breast cancer. Breast Cancer 2010;17:199-204.
48. Consoli F, Grisanti S, Amoroso V, Almici C, Verardi R, Marini M, et al. Circulating tumor cells as predictors of prognosis in metastatic breast cancer: clinical application outside a clinical trial. Tumori 2011;97:737-42.
49. Giordano A, Giuliano M, De Laurentiis M, Arpino G, Jackson S, Handy BC, et al. Circulating tumor cells in immunohistochemical subtypes of metastatic breast cancer: lack of prediction in HER2-positive disease treated with targeted therapy. Ann Oncol 2012;23:1144-50.
50. Hayashi N, Nakamura S, Tokuda Y, Shimoda Y, Yagata H, Yoshida A, et al. Prognostic value of HER2-positive circulating tumor cells in patients with metastatic breast cancer. Int J Clin Oncol 2012;17:96-104.
51. Molloy TJ, Devriese LA, Helgason HH, Bosma AJ, Hauptmann M, Voest EE, et al. A multimarker QPCR-based platform for the detection of circulating tumour cells in patients with early-stage breast cancer. Br J Cancer 2011;104:1913-9.
52. Muller V, Riethdorf S, Rack B, Janni W, Fasching PA, Solomayer E, et al. Prospective evaluation of serum tissue inhibitor of metalloproteinase 1 and carbonic anhydrase IX in correlation to circulating tumor cells in patients with metastatic breast cancer. Breast Cancer Res 2011;13:R71.
53. Pierga JY, Hajage D, Bachelot T, Delaloge S, Brain E, Campone M, et al. High independent prognostic and predictive value of circulating tumor cells compared with serum tumor markers in a large prospective trial in first-line chemotherapy for metastatic breast cancer patients. Ann Oncol 2012;23:618-24.
54. Reinholz MM, Kitzmann KA, Tenner K, Hillman D, Dueck AC, Hobday TJ, et al. Cytokeratin-19 and mammaglobin gene expression in circulating tumor cells from metastatic breast cancer patients enrolled in North Central Cancer Treatment Group trials, N0234/336/436/437. Clin Cancer Res 2011;17:7183-93.
55. Serrano MJ, Lorente JA, Delgado Rodriguez M, Fernandez A, Fernandez M, de la Torre C, et al. Circulating tumour cells in peripheral blood: potential impact on breast cancer outcome. Clin Transl Oncol 2011;13:204-8.
56. Zhao S, Liu Y, Zhang Q, Li H, Zhang M, Ma W, et al. The prognostic role of circulating tumor cells (CTCs) detected by RT-PCR in breast cancer: a meta-analysis of published literature. Breast Cancer Res Treat 2011;130:809-16.
57. Zhang L, Wu G, Pantel K. Detection of circulating tumor cells by RT-PCR significantly associated with poor prognosis in breast cancer. Breast Cancer Res Treat 2011;130:359-64.
58. Ring AE, Zabaglo L, Ormerod MG, Smith IE, Dowsett M. Detection of circulating epithelial cells in the blood of patients with breast cancer: comparison of three techniques. Br J Cancer 2005;92:906-12. (Pubitemid 40462638)
59. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM. Reporting recommendations for tumor markers prognostic studies. J Clin Oncol 2005;23:9067-72.