Prognostic Value of Circulating Tumor Cells for Non-metastatic Breast Cancer: A Meta-Analysis_Chinese Journal of Evidence-Based Medicine

Authors：

 DUXing , Adilijiang·Maimaitiming ,  Dilimulati·Aisimutula

Department of Breast Surgery, First Affiliated Hospital of Xinjiang Medical University, Urumqi 830054, China;

Corresponding author：

Dilimulati·Aisimutula, Email: 2499156828@qq.com

Keywords：

Non-metastatic breast cancer; Circulating tumour cell; Prognosis; Meta-analysis; Cohort study

DOI：

10.7507/1672-2531.20140122

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Objective To systematically review the prognostic value of circulating tumour cells (CTCs) in non-metastatic breast cancer patients. Methods We electronically searched PubMed, EMbase, WanFang Data, CNKI and CBM for collecting cohort studies about the prognostic relevance of CTCs in the peripheral blood of stage I to Ⅲ breast cancer patients from inception to March 20^th, 2014. Two reviewers independently screened studies according to the inclusion and exclusion criteria, extracted data and assessed methodological quality. Meta-analysis was conducted using RevMan 5.2 software. Results A total of 7 studies involving 1 780 patients were eligible for final analyses. The results of meta-analysis showed that, the presence of CTCs was associated with both poor DFS (RR=2.24, 95%CI 1.92 to 2.61, P < 0.000 01) and OS (RR=2.55, 95%CI 1.99 to 3.28, P < 0.000 01). The results of subgroup analysis by detection time of CTCs showed that CTCs detected before and after adjuvant chemotherapy was a statistically significant prognostic factor (P≤0.000 4). Conclusion CTCs is an adverse prognostic factor in non-metastatic breast cancer patients, which is not significantly influenced by adjuvant chemotherapy.

Citation： DUXing, Adilijiang·Maimaitiming, Dilimulati·Aisimutula. Prognostic Value of Circulating Tumor Cells for Non-metastatic Breast Cancer: A Meta-Analysis. Chinese Journal of Evidence-Based Medicine, 2014, 14(6): 721-728. doi: 10.7507/1672-2531.20140122 Copy

1.	Siegel R, Naishadham D, Jemal A. Cancer statistics:2013. CA Cancer J Clin, 2013, 63:11-30.
2.	Gangopadhyay S, Nandy A, Hor P, et al. Breast cancer stem cells:a novel therapeutic target. Clin Breast Cancer, 2013, 13(1):7-15.
3.	Braun S, VogI FD, Naume B, et al. A pooled analysis of bone marrow micrometastasis in breast cancer. N Engl J Med, 2005, 353: 793-802.
4.	Zhe X, Cher ML, Bonfil RD. Circulating tumor cells:Finding the needle in the haystack. Am J Cancer Res, 2011, 1(6):740-751.
5.	Ashwoah TR. A case of cancer in which cells similar to those in the tumors were seen in the blood after death. Aust Med J, 1869, 14:146-149.
6.	Joosse SA, Pantel K. Biologic challenges in the detection of circulating tumor cells. Cancer Res, 2013, 73(1):8-11.
7.	Serrano MJ, Rovira PS, Lorente JA, et al. Dynamics of circulating tumor cells in early breast cancer under neoadjuvant therapy. Exp Ther Med, 2012, 4(1):43-48.
8.	Strati A, Kasimir-Bauer S, Markou A, et al. Comparison of three molecular assays for the detection and molecular characterization of circulating tumor cells in breast cancer. Breast Cancer Res, 2013, 15(2):R20.
9.	Ekaterina I, Galanzha, Vladimir P, et al. Circulating Tumor Cell Detection and Capture by Photoacoustic Flow Cytometry in Vivo and ex Vivo. Cancers(Basel), 2013, 5(4):1691-1738.
10.	Yusa A, Toneri M, Masuda T, et al. Development of a New Rapid Isolation Device for Circulating Tumor Cells (CTCs) Using 3D Palladium Filter and Its Application for Genetic Analysis. PLoS One, 2014, 9(2):e88821.
11.	Riahi R, Gogoi P, Sepehri S, et al. A novel microchannel-based device to capture and analyze circulating tumor cells (CTCs) of breast cancer. Int J Oncol, 2014, Mar 21. doi:10.3892/ijo.2014.2353.
12.	Qin J, Alt JR, Hunsley BA, et al. Stabilization of circulating tumor cells in blood using a collection device with a preservative reagent. Cancer Cell Int, 2014, 14(1):23.
13.	Alix-Panabières C, Pantel K. Technologies for detection of circulating tumor cells:facts and vision. Lab Chip, 2014, 14(1):57-62.
14.	Bidard FC, Peeters DJ, Fehm T, et al. Clinical validity of circulating tumor cells in patients with metastatic breast cancer:a pooled analysis of individual patient data. Lancet Oncol, 2014, 15(4):406-414.
15.	Martin M, Custodio S, de Las Casas ML, et al. Circulating tumor cells following first chemotherapy cycle:an early and strong predictor of outcome in patients with metastatic breast cancer. Oncologist, 2013, 18, 917-923.
16.	Giordano A, Giuliano M, De Laurentiis M, 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, 23:1144-1150.
17.	Ramirez JM, Fehm T, Orsini M, et al. Prognostic relevance of viable circulating tumor cells detected by EPISPOT in metastatic breast cancer patients. Clin Chem, 2014, 60(1):214-221.
18.	Liu Y, Liu Q, Wang T, et al. Circulating tumor cells in HER2 positive metastatic breast cancer patients:a valuable prognostic and predictive biomarker. BMC Cancer, 2013, 13:202.
19.	Saloustros E, Mavroudis D. CTCs in primary breast cancer (Ⅱ). Recent Results Cancer Res, 2012, 195:187-192.
20.	Lucci A, Hall CS, Lodhi AK, et al. Circulating tumor cells in nonmetastatic breast cancer:a prospective study. Lancet Oncol, 2012, 13(7):688-695.
21.	Xenidis N, Ignatiadis M, Apostolaki S, et al. Cytokeratin-19 mRNApositive circulating tumor cells after adjuvant chemotherapy in patients with early breast cancer. J Clin Oncol, 2009, 27:2177-2184.
22.	Marques AR, Teixeira E, Diamond J, 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, 114:223-232.
23.	Ntoulia M, Stathopoulou A, Ignatiadis M, 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, 39:879-887.
24.	Chen Y, Zou TN, Wu ZP, et al. Detection of cytokeratin 19, human mammaglobin and carcinoembryonic antigenpositive circulating tumor cells by three-marker reverse transcription-PCR assay and its relation to clinical outcome in early breast cancer. Int J Biol Markers, 2010, 25:59-68.
25.	Wells G, Shea B, O'Connell D, et al. New Castle-Ottawa Quality Assessment Scale--Cohort Studies. Available at:http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Assessed on June 15, 2012.
26.	Xenidis N, Markos V, Apostolaki S, 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, 18:1623-1631.
27.	Apostolaki S, Perraki M, Pallis A, et al. Circulating HER2 mRNApositive 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, 18:851-858.
28.	Ignatiadis M, Perraki M, Apostolaki S, et al. Molecular detection and prognostic value of circulating cytokeratin-19 messenger RNApositive and HER2 messenger RNA-positive cells in the peripheral blood of women with early-stage breast cancer. Clin Breast Cancer, 2007, 7:883-889.
29.	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, 2007, 25:5194-5202.
30.	Daskalaki A, Agelaki S, Perraki M, 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, 101:589-597.
31.	Xenidis N, Ignatiadis M, Apostolaki S, et al. Cytokeratin-19 mRNApositive circulating tumor cells after adjuvant chemotherapy in patients with early breast cancer. J Clin Oncol, 2009, 27:2177-2184.
32.	Apostolaki S, Perraki M, Kallergi G, 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, 117:525-534.
33.	Zhao S, Liu Y, Zhang Q, et al. The prognostic role of circulating tumor cells (CTCs) detected by RT-PCR in breast cancer:a metaanalysis of published literature. Breast Cancer Res Treat, 2011, 130: 809-816.
34.	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, 130:359-364.
35.	Zhang L, Riethdorf S, Wu G, et al. Meta-analysis of the prognostic of circulating tumor cells in breast caner. Clin Cancer Res, 2012, 18: 5701-5710.

1. Siegel R, Naishadham D, Jemal A. Cancer statistics:2013. CA Cancer J Clin, 2013, 63:11-30.
2. Gangopadhyay S, Nandy A, Hor P, et al. Breast cancer stem cells:a novel therapeutic target. Clin Breast Cancer, 2013, 13(1):7-15.
3. Braun S, VogI FD, Naume B, et al. A pooled analysis of bone marrow micrometastasis in breast cancer. N Engl J Med, 2005, 353: 793-802.
4. Zhe X, Cher ML, Bonfil RD. Circulating tumor cells:Finding the needle in the haystack. Am J Cancer Res, 2011, 1(6):740-751.
5. Ashwoah TR. A case of cancer in which cells similar to those in the tumors were seen in the blood after death. Aust Med J, 1869, 14:146-149.
6. Joosse SA, Pantel K. Biologic challenges in the detection of circulating tumor cells. Cancer Res, 2013, 73(1):8-11.
7. Serrano MJ, Rovira PS, Lorente JA, et al. Dynamics of circulating tumor cells in early breast cancer under neoadjuvant therapy. Exp Ther Med, 2012, 4(1):43-48.
8. Strati A, Kasimir-Bauer S, Markou A, et al. Comparison of three molecular assays for the detection and molecular characterization of circulating tumor cells in breast cancer. Breast Cancer Res, 2013, 15(2):R20.
9. Ekaterina I, Galanzha, Vladimir P, et al. Circulating Tumor Cell Detection and Capture by Photoacoustic Flow Cytometry in Vivo and ex Vivo. Cancers(Basel), 2013, 5(4):1691-1738.
10. Yusa A, Toneri M, Masuda T, et al. Development of a New Rapid Isolation Device for Circulating Tumor Cells (CTCs) Using 3D Palladium Filter and Its Application for Genetic Analysis. PLoS One, 2014, 9(2):e88821.
11. Riahi R, Gogoi P, Sepehri S, et al. A novel microchannel-based device to capture and analyze circulating tumor cells (CTCs) of breast cancer. Int J Oncol, 2014, Mar 21. doi:10.3892/ijo.2014.2353.
12. Qin J, Alt JR, Hunsley BA, et al. Stabilization of circulating tumor cells in blood using a collection device with a preservative reagent. Cancer Cell Int, 2014, 14(1):23.
13. Alix-Panabières C, Pantel K. Technologies for detection of circulating tumor cells:facts and vision. Lab Chip, 2014, 14(1):57-62.
14. Bidard FC, Peeters DJ, Fehm T, et al. Clinical validity of circulating tumor cells in patients with metastatic breast cancer:a pooled analysis of individual patient data. Lancet Oncol, 2014, 15(4):406-414.
15. Martin M, Custodio S, de Las Casas ML, et al. Circulating tumor cells following first chemotherapy cycle:an early and strong predictor of outcome in patients with metastatic breast cancer. Oncologist, 2013, 18, 917-923.
16. Giordano A, Giuliano M, De Laurentiis M, 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, 23:1144-1150.
17. Ramirez JM, Fehm T, Orsini M, et al. Prognostic relevance of viable circulating tumor cells detected by EPISPOT in metastatic breast cancer patients. Clin Chem, 2014, 60(1):214-221.
18. Liu Y, Liu Q, Wang T, et al. Circulating tumor cells in HER2 positive metastatic breast cancer patients:a valuable prognostic and predictive biomarker. BMC Cancer, 2013, 13:202.
19. Saloustros E, Mavroudis D. CTCs in primary breast cancer (Ⅱ). Recent Results Cancer Res, 2012, 195:187-192.
20. Lucci A, Hall CS, Lodhi AK, et al. Circulating tumor cells in nonmetastatic breast cancer:a prospective study. Lancet Oncol, 2012, 13(7):688-695.
21. Xenidis N, Ignatiadis M, Apostolaki S, et al. Cytokeratin-19 mRNApositive circulating tumor cells after adjuvant chemotherapy in patients with early breast cancer. J Clin Oncol, 2009, 27:2177-2184.
22. Marques AR, Teixeira E, Diamond J, 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, 114:223-232.
23. Ntoulia M, Stathopoulou A, Ignatiadis M, 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, 39:879-887.
24. Chen Y, Zou TN, Wu ZP, et al. Detection of cytokeratin 19, human mammaglobin and carcinoembryonic antigenpositive circulating tumor cells by three-marker reverse transcription-PCR assay and its relation to clinical outcome in early breast cancer. Int J Biol Markers, 2010, 25:59-68.
25. Wells G, Shea B, O'Connell D, et al. New Castle-Ottawa Quality Assessment Scale--Cohort Studies. Available at:http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Assessed on June 15, 2012.
26. Xenidis N, Markos V, Apostolaki S, 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, 18:1623-1631.
27. Apostolaki S, Perraki M, Pallis A, et al. Circulating HER2 mRNApositive 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, 18:851-858.
28. Ignatiadis M, Perraki M, Apostolaki S, et al. Molecular detection and prognostic value of circulating cytokeratin-19 messenger RNApositive and HER2 messenger RNA-positive cells in the peripheral blood of women with early-stage breast cancer. Clin Breast Cancer, 2007, 7:883-889.
29. 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, 2007, 25:5194-5202.
30. Daskalaki A, Agelaki S, Perraki M, 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, 101:589-597.
31. Xenidis N, Ignatiadis M, Apostolaki S, et al. Cytokeratin-19 mRNApositive circulating tumor cells after adjuvant chemotherapy in patients with early breast cancer. J Clin Oncol, 2009, 27:2177-2184.
32. Apostolaki S, Perraki M, Kallergi G, 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, 117:525-534.
33. Zhao S, Liu Y, Zhang Q, et al. The prognostic role of circulating tumor cells (CTCs) detected by RT-PCR in breast cancer:a metaanalysis of published literature. Breast Cancer Res Treat, 2011, 130: 809-816.
34. 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, 130:359-364.
35. Zhang L, Riethdorf S, Wu G, et al. Meta-analysis of the prognostic of circulating tumor cells in breast caner. Clin Cancer Res, 2012, 18: 5701-5710.

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Prognostic Value of Circulating Tumor Cells for Non-metastatic Breast Cancer: A Meta-Analysis

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