Detection, significance and potential utility of circulating tumor cells in clinical practice in breast cancer (Review)
- Authors:
- Dominika Šmičková Rusnáková
- Ramadan Aziri
- Peter Dubovan
- Miroslav Jurík
- Michal Mego
- Daniel Pinďák
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Affiliations: Department of Surgical Oncology, Faculty of Medicine, Slovak Medical University and National Cancer Institute, 833 10 Bratislava, Slovak Republic, Second Department of Oncology, Faculty of Medicine, Comenius University and National Cancer Institute, 833 10 Bratislava, Slovak Republic - Published online on: October 17, 2024 https://doi.org/10.3892/ol.2024.14756
- Article Number: 10
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Copyright: © Rusnáková et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Ginsburg O, Bray F, Coleman MP, Vanderpuye V, Eniu A, Kotha SR, Sarker M, Huong TT, Allemani C, Dvaladze A, et al: The global burden of women's cancers: A grand challenge in global health. Lancet. 389:847–860. 2017. View Article : Google Scholar | |
GLOBOCAN, . 2020.New global cancer data. https://www.uicc.org/news/globocan-2020-new-global-cancer-dataNovember 24–2021 | |
Siegel RL, Miller KD and Jemal A: Cancer statistics, 2017. CA Cancer J Clin. 67:7–30. 2017. View Article : Google Scholar | |
DeSantis CE, Fedewa SA, Goding Sauer A, Kramer JL, Smith RA and Jemal A: Breast cancer statistics, 2015: Convergence of incidence rates between black and white women. CA Cancer J Clin. 66:31–42. 2016. View Article : Google Scholar | |
Hall CS, Valad L and Lucci A: Circulating tumor cells in breast cancer patients. Crit Rev Oncog. 21:125–139. 2016. View Article : Google Scholar | |
Green M and Hortobagyi GN: Neoadjuvant chemotherapy for operable breast cancer. Oncology (Williston Park). 16:871–884. 889–890. 892–904. 997–998. 2002. | |
Fisher B, Bauer M, Wickerham DL, Redmond CK, Fisher ER, Cruz AB, Foster R, Gardner B, Lerner H, Margolese R, et al: Relation of number of positive axillary nodes to the prognosis of patients with primary breast cancer. An NSABP update. Cancer. 52:1551–1557. 1983. View Article : Google Scholar | |
Gilbey AM, Burnett D, Coleman RE and Holen I: The detection of circulating breast cancer cells in blood. J Clin Pathol. 57:903–911. 2004. View Article : Google Scholar | |
Cueva Bañuelos JF, Rodríguez López C, Cortegoso Mosquera A, Palacios Ozores P and Curiel García T: Clinical relevance and therapeutic application of CTCs in advanced breast cancer. Adv Exp Med Biol. 1220:147–164. 2020. View Article : Google Scholar | |
Cardoso F, Spence D, Mertz S, Corneliussen-James D, Sabelko K, Gralow J, Cardoso MJ, Peccatori F, Paonessa D, Benares A, et al: Global analysis of advanced/metastatic breast cancer: Decade report (2005–2015). Breast. 39:131–138. 2018. View Article : Google Scholar | |
Weiss L: Metastasis of cancer: A conceptual history from antiquity to the 1990s. Cancer Metastasis Rev. 19:193–383. 2000. View Article : Google Scholar | |
Wittekind C and Neid M: Cancer invasion and metastasis. Oncology. 69 (Suppl 1):S14–S16. 2005. View Article : Google Scholar | |
Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Matera J, Miller MC, Reuben JM, Doyle GV, Allard WJ, Terstappen LW and Hayes DF: Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med. 351:781–791. 2004. View Article : Google Scholar | |
Giuliano M, Giordano A, Jackson S, De Giorgi U, Mego M, Cohen EN, Gao H, Anfossi S, Handy BC, Ueno NT, et al: Circulating tumor cells as early predictors of metastatic spread in breast cancer patients with limited metastatic dissemination. Breast Cancer Res. 16:4402014. View Article : Google Scholar | |
Ignatiadis M, Kallergi G, Ntoulia M, Perraki M, Apostolaki S, Kafousi M, Chlouverakis G, Stathopoulos E, Lianidou E, Georgoulias V and Mavroudis D: 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. View Article : Google Scholar | |
Lucci A, Hall CS, Lodhi AK, Bhattacharyya A, Anderson AE, Xiao L, Bedrosian I, Kuerer HM and Krishnamurthy S: Circulating tumour cells in non-metastatic breast cancer: A prospective study. Lancet Oncol. 13:688–695. 2012. View Article : Google Scholar | |
Zhang L, Riethdorf S, Wu G, Wang T, Yang K, Peng G, Liu J and Pantel K: Meta-analysis of the prognostic value of circulating tumor cells in breast cancer. Clin Cancer Res. 18:5701–5710. 2012. View Article : Google Scholar | |
Enderling H, Hlatky L and Hahnfeldt P: Migration rules: Tumours are conglomerates of self-metastases. Br J Cancer. 100:1917–1925. 2009. View Article : Google Scholar | |
Kim MY, Oskarsson T, Acharyya S, Nguyen DX, Zhang XH, Norton L and Massagué J: Tumor self-seeding by circulating cancer cells. Cell. 139:1315–1326. 2009. View Article : Google Scholar | |
Pantel K and Speicher MR: The biology of circulating tumor cells. Oncogene. 35:1216–1224. 2016. View Article : Google Scholar | |
Gerlinger M, Rowan AJ, Horswell S, Math M, Larkin J, Endesfelder D, Gronroos E, Martinez P, Matthews N, Stewart A, et al: Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 366:883–889. 2012. View Article : Google Scholar | |
Bae SY, Kamalanathan KJ, Galeano-Garces C, Konety BR, Antonarakis ES, Parthasarathy J, Hong J and Drake JM: Dissemination of circulating tumor cells in breast and prostate cancer: Implications for early detection. Endocrinology. 165:bqae0222024. View Article : Google Scholar | |
Alix-Panabières C and Pantel K: Challenges in circulating tumour cell research. Nat Rev Cancer. 14:623–631. 2014. View Article : Google Scholar | |
Coumans FAW, Ligthart ST, Uhr JW and Terstappen LWMM: Challenges in the enumeration and phenotyping of CTC. Clin Cancer Res. 18:5711–5718. 2012. View Article : Google Scholar | |
Mego M and Reuben JM: Prognostic and predictive role of circulating tumor cells in breast cancer. Curr Breast Cancer Rep. 6:251–259. 2014. View Article : Google Scholar | |
Kanwar N and Done SJ: Molecular profiling and significance of circulating tumor cell based genetic signatures. Adv Exp Med Biol. 994:143–167. 2017. View Article : Google Scholar | |
Mego M, Mani SA and Cristofanilli M: Molecular mechanisms of metastasis in breast cancer-clinical applications. Nat Rev Clin Oncol. 7:693–701. 2010. View Article : Google Scholar | |
Feng Z, Wu J, Lu Y, Chan YT, Zhang C, Wang D, Luo D, Huang Y, Feng Y and Wang N: Circulating tumor cells in the early detection of human cancers. Int J Biol Sci. 18:3251–3265. 2022. View Article : Google Scholar | |
Ju S, Chen C, Zhang J, Xu L, Zhang X, Li Z, Chen Y, Zhou J, Ji F and Wang L: Detection of circulating tumor cells: Opportunities and challenges. Biomark Res. 10:582022. View Article : Google Scholar | |
Cristofanilli M: Circulating tumor cells, disease progression, and survival in metastatic breast cancer. Semin Oncol. 33 (3 Suppl 9):S9–S14. 2006. View Article : Google Scholar | |
Cristofanilli M, Hayes DF, Budd GT, Ellis MJ, Stopeck A, Reuben JM, Doyle GV, Matera J, Allard WJ, Miller MC, et al: Circulating tumor cells: A novel prognostic factor for newly diagnosed metastatic breast cancer. J Clin oncol. 23:1420–1430. 2005. View Article : Google Scholar | |
Alix-Panabières C and Pantel K: Clinical applications of circulating tumor cells and circulating tumor DNA as liquid biopsy. Cancer Discov. 6:479–491. 2016. View Article : Google Scholar | |
Lianidou ES and Markou A: Circulating tumor cells in breast cancer: Detection systems, molecular characterization, and future challenges. Clin Chem. 57:1242–1255. 2011. View Article : Google Scholar | |
Andree KC, van Dalum G and Terstappen LWMM: Challenges in circulating tumor cell detection by the CellSearch system. Mol Oncol. 10:395–407. 2016. View Article : Google Scholar | |
Müller V, Riethdorf S, Rack B, Janni W, Fasching PA, Solomayer E, Aktas B, Kasimir-Bauer S, Pantel K and Fehm T; DETECT study group, : Prognostic impact of circulating tumor cells assessed with the CellSearch system™ and AdnaTest breast™ in metastatic breast cancer patients: The DETECT study. Breast Cancer Res. 14:R1182012. View Article : Google Scholar | |
Aktas B, Tewes M, Fehm T, Hauch S, Kimmig R and Kasimir-Bauer S: Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res. 11:R462009. View Article : Google Scholar | |
Danila DC, Samoila A, Patel C, Schreiber N, Herkal A, Anand A, Bastos D, Heller G, Fleisher M and Scher HI: Clinical validity of detecting circulating tumor cells by AdnaTest assay compared with direct detection of tumor mrna in stabilized whole blood, as a biomarker predicting overall survival for metastatic castration-resistant prostate cancer patients. Cancer J. 22:315–320. 2016. View Article : Google Scholar | |
Gorges TM, Stein A, Quidde J, Hauch S, Röck K, Riethdorf S, Joosse SA and Pantel K: Improved detection of circulating tumor cells in metastatic colorectal cancer by the combination of the CellSearch® system and the AdnaTest®. PLoS One. 11:e01551262016. View Article : Google Scholar | |
Talasaz AH, Powell AA, Huber DE, Berbee JG, Roh KH, Yu W, Xiao W, Davis MM, Pease RF, Mindrinos MN, et al: Isolating highly enriched populations of circulating epithelial cells and other rare cells from blood using a magnetic sweeper device. Proc Natl Acad Sci USA. 106:3970–3975. 2009. View Article : Google Scholar | |
Harb W, Fan A, Tran T, Danila DC, Keys D, Schwartz M and Ionescu-Zanetti C: Mutational analysis of circulating tumor cells using a novel microfluidic collection device and qPCR assay. Transl Oncol. 6:528–538. 2013. View Article : Google Scholar | |
Cho H, Kim J, Jeon CW and Han KH: A disposable microfluidic device with a reusable magnetophoretic functional substrate for isolation of circulating tumor cells. Lab Chip. 17:4113–4123. 2017. View Article : Google Scholar | |
Liu Z, Fusi A, Klopocki E, Schmittel A, Tinhofer I, Nonnenmacher A and Keilholz U: Negative enrichment by immunomagnetic nanobeads for unbiased characterization of circulating tumor cells from peripheral blood of cancer patients. J Transl Med. 9:702011. View Article : Google Scholar | |
Naume B, Borgen E, Tøssvik S, Pavlak N, Oates D and Nesland JM: Detection of isolated tumor cells in peripheral blood and in BM: Evaluation of a new enrichment method. Cytotherapy. 6:244–252. 2004. View Article : Google Scholar | |
Habli Z, AlChamaa W, Saab R, Kadara H and Khraiche ML: Circulating tumor cell detection technologies and clinical utility: Challenges and opportunities. Cancers (Basel). 12:19302020. View Article : Google Scholar | |
Tong B, Xu Y, Zhao J, Chen M, Xing J, Zhong W and Wang M: Prognostic significance of circulating tumor cells in non-small cell lung cancer patients undergoing chemotherapy. Oncotarget. 8:86615–86624. 2017. View Article : Google Scholar | |
Drucker A, Teh EM, Kostyleva R, Rayson D, Douglas S and Pinto DM: Comparative performance of different methods for circulating tumor cell enrichment in metastatic breast cancer patients. PLoS One. 15:e02373082020. View Article : Google Scholar | |
Mego M, Mani SA, Lee BN, Li C, Evans KW, Cohen EN, Gao H, Jackson SA, Giordano A, Hortobagyi GN, et al: Expression of epithelial-mesenchymal transition-inducing transcription factors in primary breast cancer: The effect of neoadjuvant therapy. Int J Cancer. 130:808–816. 2012. View Article : Google Scholar | |
Vona G, Sabile A, Louha M, Sitruk V, Romana S, Schütze K, Capron F, Franco D, Pazzagli M, Vekemans M, et al: Isolation by size of epithelial tumor cells: A new method for the immunomorphological and molecular characterization of circulatingtumor cells. Am J Pathol. 156:57–63. 2000. View Article : Google Scholar | |
Dolfus C, Piton N, Toure E and Sabourin JC: Circulating tumor cell isolation: The assets of filtration methods with polycarbonate track-etched filters. Chin J Cancer Res. 27:479–487. 2015. | |
Hou HW, Warkiani ME, Khoo BL, Li ZR, Soo RA, Tan DS, Lim WT, Han J, Bhagat AA and Lim CT: Isolation and retrieval of circulating tumor cells using centrifugal forces. Sci Rep. 3:12592013. View Article : Google Scholar | |
Tamminga M, Andree KC, Hiltermann TJN, Jayat M, Schuuring E, van den Bos H, Spierings DCJ, Lansdorp PM, Timens W, Terstappen LWMM and Groen HJM: Detection of circulating tumor cells in the diagnostic leukapheresis product of non-small-cell lung cancer patients comparing CellSearch® and ISET. Cancers (Basel). 12:8962020. View Article : Google Scholar | |
Miller MC, Robinson PS, Wagner C and O'Shannessy DJ: The parsortix™ cell separation system-A versatile liquid biopsy platform. Cytometry A. 93:1234–1239. 2018. View Article : Google Scholar | |
Xu L, Mao X, Imrali A, Syed F, Mutsvangwa K, Berney D, Cathcart P, Hines J, Shamash J and Lu YJ: Optimization and evaluation of a novel size based circulating tumor cell isolation system. PLoS One. 10:e01380322015. View Article : Google Scholar | |
Bankó P, Lee SY, Nagygyörgy V, Zrínyi M, Chae CH, Cho DH and Telekes A: Technologies for circulating tumor cell separation from whole blood. J Hematol Oncol. 12:482019. View Article : Google Scholar | |
Rosenberg R, Gertler R, Friederichs J, Fuehrer K, Dahm M, Phelps R, Thorban S, Nekarda H and Siewert JR: Comparison of two density gradient centrifugation systems for the enrichment of disseminated tumor cells in blood. Cytometry. 49:150–158. 2002. View Article : Google Scholar | |
Lagoudianakis EE, Kataki A, Manouras A, Memos N, Papadima A, Derventzi A, Zografos G, Papadopoulos S, Katergiannakis V and Konstadoulakis MM: Detection of epithelial cells by RT-PCR targeting CEA, CK20, and TEM-8 in colorectal carcinoma patients using OncoQuick density gradient centrifugation system. J Surg Res. 155:183–190. 2009. View Article : Google Scholar | |
Gupta V, Jafferji I, Garza M, Melnikova VO, Hasegawa DK, Pethig R and Davis DW: ApoStream(™), a new dielectrophoretic device for antibody independent isolation and recovery of viable cancer cells from blood. Biomicrofluidics. 6:241332012. View Article : Google Scholar | |
O'Shannessy DJ, Davis DW, Anderes K and Somers EB: Isolation of circulating tumor cells from multiple epithelial cancers with ApoStream(®) for detecting (or monitoring) the expression of Folate receptor alpha. Biomark Insights. 11:7–18. 2016. View Article : Google Scholar | |
Le Du F, Fujii T, Kida K, Davis DW, Park M, Liu DD, Wu W, Chavez-MacGregor M, Barcenas CH, Valero V, et al: EpCAM-independent isolation of circulating tumor cells with epithelial-to-mesenchymal transition and cancer stem cell phenotypes using ApoStream® in patients with breast cancer treated with primary systemic therapy. PLoS One. 15:e02299032020. View Article : Google Scholar | |
Wu S, Gu L, Qin J, Zhang L, Sun F, Liu Z, Wang Y and Shi D: Rapid label-free isolation of circulating tumor cells from patients' peripheral blood using electrically charged Fe3O4 nanoparticles. ACS Appl Mater Interfaces. 12:4193–4203. 2020. View Article : Google Scholar | |
Pavlova NN and Thompson CB: The emerging hallmarks of cancer metabolism. Cell Metab. 23:27–47. 2016. View Article : Google Scholar | |
Luc R, Tortorella SM, Ververis K and Karagiannis TC: Lactate as an insidious metabolite due to the Warburg effect. Mol Biol Rep. 42:835–840. 2015. View Article : Google Scholar | |
Zhu Z and Zhang YHP: In vitro metabolic engineering of bioelectricity generation by the complete oxidation of glucose. Metab Eng. 39:110–116. 2017. View Article : Google Scholar | |
Nasiri R, Shamloo A, Ahadian S, Amirifar L, Akbari J, Goudie MJ, Lee K, Ashammakhi N, Dokmeci MR, Di Carlo D and Khademhosseini A: Microfluidic-based approaches in targeted cell/particle separation based on physical properties: Fundamentalsand applications. Small. 16:e20001712020. View Article : Google Scholar | |
Burinaru TA, Avram M, Avram A, Mărculescu C, Ţîncu B, Ţucureanu V, Matei A and Militaru M: Detection of circulating tumor cells using microfluidics. ACS Comb Sci. 20:107–126. 2018. View Article : Google Scholar | |
Nagrath S, Sequist LV, Maheswaran S, Bell DW, Irimia D, Ulkus L, Smith MR, Kwak EL, Digumarthy S, Muzikansky A, et al: Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature. 450:1235–1239. 2007. View Article : Google Scholar | |
Park MH, Reátegui E, Li W, Tessier SN, Wong KH, Jensen AE, Thapar V, Ting D, Toner M, Stott SL and Hammond PT: Enhanced isolation and release of circulating tumor cells using nanoparticle binding and ligand exchange in a microfluidic chip. J Am Chem Soc. 139:2741–2749. 2017. View Article : Google Scholar | |
Zhang X, Zhu Z, Xiang N, Long F and Ni Z: Automated microfluidic instrument for label-free and high-throughput cell separation. Anal Chem. 90:4212–4220. 2018. View Article : Google Scholar | |
Wang J, Li Y, Wang R, Han C, Xu S, You T, Li Y, Xia J, Xu X, Wang D, et al: A fully automated and integrated microfluidic system for efficient CTC detection and its application in hepatocellular carcinoma screening and prognosis. ACS Appl Mater Interfaces. 13:30174–30186. 2021. View Article : Google Scholar | |
Lee J and Kwak B: Simultaneous on-chip isolation and characterization of circulating tumor cell sub-populations. Biosens Bioelectron. 168:1125642020. View Article : Google Scholar | |
Lee AC, Svedlund J, Darai E, Lee Y, Lee D, Lee HB, Kim SM, Kim O, Bae HJ, Choi A, et al: OPENchip: An on-chip in situ molecular profiling platform for gene expression analysis and oncogenic mutation detection in single circulating tumour cells. Lab Chip. 20:912–922. 2020. View Article : Google Scholar | |
Zhang Y, Li M, Gao X, Chen Y and Liu T: Nanotechnology in cancer diagnosis: Progress, challenges and opportunities. J Hematol Oncol. 12:1372019. View Article : Google Scholar | |
Huang Q, Yin W, Chen X, Wang Y, Li Z, Du S, Wang L and Shi C: Nanotechnology-based strategies for early cancer diagnosis using circulating tumor cells as a liquid biopsy. Nanotheranostics. 2:21–41. 2018. View Article : Google Scholar | |
Muthu MS and Feng SS: Theranostic liposomes for cancer diagnosis and treatment: Current development and pre-clinical success. Expert Opin Drug Deliv. 10:151–155. 2013. View Article : Google Scholar | |
Lin D, Shen L, Luo M, Zhang K, Li J, Yang Q, Zhu F, Zhou D, Zheng S, Chen Y and Zhou J: Circulating tumor cells: Biology and clinical significance. Sig Transduct Target Ther. 6:4042021. View Article : Google Scholar | |
Hüsemann Y, Geigl JB, Schubert F, Musiani P, Meyer M, Burghart E, Forni G, Eils R, Fehm T, Riethmüller G and Klein CA: Systemic spread is an early step in breast cancer. Cancer Cell. 13:58–68. 2008. View Article : Google Scholar | |
Hosseini H, Obradović MMS, Hoffmann M, Harper KL, Sosa MS, Werner-Klein M, Nanduri LK, Werno C, Ehrl C, Maneck M, et al: Early dissemination seeds metastasis in breast cancer. Nature. 540:552–558. 2016. View Article : Google Scholar | |
Rhim AD, Thege FI, Santana SM, Lannin TB, Saha TN, Tsai S, Maggs LR, Kochman ML, Ginsberg GG, Lieb JG, et al: Detection of circulating pancreas epithelial cells in patients with pancreatic cystic lesions. Gastroenterology. 146:647–651. 2014. View Article : Google Scholar | |
Yamaguchi J, Kokuryo T, Yokoyama Y, Ebata T, Ochiai Y and Nagino M: Premalignant pancreatic cells seed stealth metastasis in distant organs in mice. Oncogene. 40:2273–2284. 2021. View Article : Google Scholar | |
Banys M, Hahn M, Gruber I, Krawczyk N, Wallwiener M, Hartkopf A, Taran FA, Röhm C, Kurth R, Becker S, et al: Detection and clinical relevance of hematogenous tumor cell dissemination in patients with ductal carcinoma in situ. Breast Cancer Res Treat. 144:531–538. 2014. View Article : Google Scholar | |
Shao X, Jin X, Chen Z, Zhang Z, Chen W, Jiang J, Wang Z, Cui Y, Fan WH, Wang K, et al: A comprehensive comparison of circulating tumor cells and breast imaging modalities as screening tools for breast cancer in Chinese women. Front Oncol. 12:8902482022. View Article : Google Scholar | |
Ignatiadis M, Rothé F, Chaboteaux C, Durbecq V, Rouas G, Criscitiello C, Metallo J, Kheddoumi N, Singhal SK, Michiels S, et al: HER2-positive circulating tumor cells in breast cancer. PLoS One. 6:e156242011. View Article : Google Scholar | |
Thery L, Meddis A, Cabel L, Proudhon C, Latouche A, Pierga JY and Bidard FC: Circulating tumor cells in early breast cancer. JNCI Cancer Spectr. 3:pkz0262019. View Article : Google Scholar | |
Bidard FC, Michiels S, Riethdorf S, Mueller V, Esserman LJ, Lucci A, Naume B, Horiguchi J, Gisbert-Criado R, Sleijfer S, et al: Circulating tumor cells in breast cancer patients treated by neoadjuvant chemotherapy: A meta-analysis. J Natl Cancer Inst. 110:560–567. 2018. View Article : Google Scholar | |
Rack B, Schindlbeck C, Jückstock J, Andergassen U, Hepp P, Zwingers T, Friedl TW, Lorenz R, Tesch H, Fasching PA, et al: Circulating tumor cells predict survival in early average-to-high risk breast cancer patients. J Natl Cancer Inst. 106:dju0662014. View Article : Google Scholar | |
Janni WJ, Rack B, Terstappen LWMM, Pierga JY, Taran FA, Fehm T, Hall C, de Groot MR, Bidard FC, Friedl TW, et al: Pooled analysis of the prognostic relevance of circulating tumor cells in primary breast cancer. Clin Cancer Res. 22:2583–2593. 2016. View Article : Google Scholar | |
Pierga JY, Bidard FC, Mathiot C, Brain E, Delaloge S, Giachetti S, de Cremoux P, Salmon R, Vincent-Salomon A and Marty M: Circulating tumor cell detection predicts early metastatic relapse after neoadjuvant chemotherapy in large operable and locally advanced breast cancer in a phase II randomized trial. Clin Cancer Res. 14:7004–7010. 2008. View Article : Google Scholar | |
Hall C, Karhade M, Laubacher B, Anderson A, Kuerer H, DeSynder S and Lucci A: Circulating tumor cells after neoadjuvant chemotherapy in stage I–III triple-negative breast cancer. Ann Surg Oncol. 22 (Suppl 3):S552–S558. 2015. View Article : Google Scholar | |
Hwang SB, Bae JW, Lee HY and Kim HY: Circulating tumor cells detected by RT-PCR for CK-20 before surgery indicate worse prognostic impact in triple-negative and HER2 subtype breast cancer. J Breast Cancer. 15:34–42. 2012. View Article : Google Scholar | |
Azim HA Jr, Rothé F, Aura CM, Bavington M, Maetens M, Rouas G, Gebhart G, Gamez C, Eidtmann H, Baselga J, et al: Circulating tumor cells and response to neoadjuvant paclitaxel and HER2-targeted therapy: A sub-study from the NeoALTTO phase III trial. Breast. 22:1060–1065. 2013. View Article : Google Scholar | |
Onstenk W, Kraan J, Mostert B, Timmermans MM, Charehbili A, Smit VT, Kroep JR, Nortier JW, van de Ven S, Heijns JB, et al: Improved circulating tumor cell detection by a combined EpCAM and MCAM cellsearch enrichment approach in patients with breast cancer undergoing neoadjuvant chemotherapy. Mol Cancer Ther. 14:821–827. 2015. View Article : Google Scholar | |
Kasimir-Bauer S, Bittner AK, König L, Reiter K, Keller T, Kimmig R and Hoffmann O: Does primary neoadjuvant systemic therapy eradicate minimal residual disease? Analysis of disseminated and circulating tumor cells before and after therapy. Breast Cancer Res. 18:202016. View Article : Google Scholar | |
Pierga JY, Bidard FC, Autret A, Petit T, Andre F, Dalenc F, Levy C, Ferrero JM, Romieu G, Bonneterre J, et al: Circulating tumour cells and pathological complete response: Independent prognostic factors in inflammatory breast cancer in a pooled analysis of two multicentre phase II trials (BEVERLY-1 and −2) of neoadjuvant chemotherapy combined with bevacizumab. Ann Oncol. 28:103–109. 2017. View Article : Google Scholar | |
Riethdorf S, Müller V, Loibl S, Nekljudova V, Weber K, Huober J, Fehm T, Schrader I, Hilfrich J, Holms F, et al: Prognostic impact of circulating tumor cells for breast cancer patients treated in the neoadjuvant ‘Geparquattro’ trial. Clin Cancer Res. 23:5384–5393. 2017. View Article : Google Scholar | |
Bidard FC, Mathiot C, Delaloge S, Brain E, Giachetti S, de Cremoux P, Marty M and Pierga JY: Single circulating tumor cell detection and overall survival in nonmetastatic breast cancer. Ann Oncol. 21:729–733. 2009. View Article : Google Scholar | |
Bidard FC, Belin L, Delaloge S, Lerebours F, Ngo C, Reyal F, Alran S, Giacchetti S, Marty M, Lebofsky R and Pierga JY: Time-dependent prognostic impact of circulating tumor cells detection in non-metastatic breast cancer: 70-Month analysis of the REMAGUS02 study. Int J Breast Cancer. 2013:1304702013. View Article : Google Scholar | |
Riethdorf S, Müller V, Zhang L, Rau T, Loibl S, Komor M, Roller M, Huober J, Fehm T, Schrader I, et al: Detection and HER2 expression of circulating tumor cells: Prospective monitoring in breast cancer patients treated in the neoadjuvant GeparQuattro trial. Clin Cancer Res. 16:2634–2645. 2010. View Article : Google Scholar | |
Sparano J, O'Neill A, Alpaugh K, Wolff AC, Northfelt DW, Dang CT, Sledge GW and Miller KD: Association of circulating tumor cells with late recurrence of estrogen receptor-positive breast cancer: A secondary analysis of a randomized clinical trial. JAMA Oncol. 4:1700–1706. 2018. View Article : Google Scholar | |
Janni W, Rack BK, Fasching PA, Haeberle L, Tesch H, Lorenz R, Schochter F, Tzschaschel M, De Gregorio A, Fehm TN, et al: Persistence of circulating tumor cells in high risk early breast cancer patients five years after adjuvant chemotherapy and late recurrence: Results from the adjuvant SUCCESS A trial. J Clin Oncol. 36 (Suppl):S5152018. View Article : Google Scholar | |
Trapp E, Janni W, Schindlbeck C, Jückstock J, Andergassen U, de Gregorio A, Alunni-Fabbroni M, Tzschaschel M, Polasik A, Koch JG, et al: Presence of circulating tumor cells in high-risk early breast cancer during follow-up and prognosis. J Natl Cancer Inst. 111:380–387. 2019. View Article : Google Scholar | |
Bidard FC, Fehm T, Ignatiadis M, Smerage JB, Alix-Panabières C, Janni W, Messina C, Paoletti C, Müller V, Hayes DF, et al: Clinical application of circulating tumor cells in breast cancer: Overview of the current interventional trials. Cancer Metastasis Rev. 32:179–188. 2013. View Article : Google Scholar | |
Hall CS, Karhade MG, Bowman Bauldry JB, Valad LM, Kuerer HM, DeSnyder SM and Lucci A: Prognostic value of circulating tumor cells identified before surgical resection in nonmetastatic breast cancer patients. J Am Coll Surg. 223:20–29. 2016. View Article : Google Scholar | |
Cortazar P, Zhang L, Untch M, Mehta K, Costantino JP, Wolmark N, Bonnefoi H, Cameron D, Gianni L, Valagussa P, et al: Pathological complete response and long-term clinical benefit in breast cancer: The CTNeoBC pooled analysis. Lancet. 384:164–172. 2014. View Article : Google Scholar | |
Walter VP, Taran FA, Wallwiener M, Hahn M, Brucker SY and Hartkopf AD: Simultaneous detection of circulating and disseminated tumor cells in primary breast cancer patients following neoadjuvant chemotherapy. Arch Gynecol Obstet. 297:785–790. 2018. View Article : Google Scholar | |
Peeters DJE, van Dam PJ, Van den Eynden GGM, Rutten A, Wuyts H, Pouillon L, Peeters M, Pauwels P, Van Laere SJ, van Dam PA, et al: Detection and prognostic significance of circulating tumour cells in patients with metastatic breast cancer according to immunohistochemical subtypes. Br J Cancer. 110:375–383. 2014. View Article : Google Scholar | |
Giordano A, Giuliano M, Hsu L, Handy BC, Ueno NT, Andreopoulou E, Alvarez RH, Valero V, Hortobagyi GN and Cristofanilli M: Prognostic value of circulating tumor cells (CTC) in metastatic breast cancer (MBC): Correlation with immunohistochemically defined molecular subtypes and metastatic disease sites. J Clin Oncol. 28 (Suppl):S10002010. View Article : Google Scholar | |
Budd GT, Cristofanilli M, Ellis MJ, Stopeck A, Borden E, Miller MC, Matera J, Repollet M, Doyle GV, Terstappen LW and Hayes DF: Circulating tumor cells versus imaging-predicting overall survival in metastatic breast cancer. Clin Cancer Res. 12:6403–6409. 2006. View Article : Google Scholar | |
Giuliano M, Giordano A, Jackson S, Hess KR, De Giorgi U, Mego M, Handy BC, Ueno NT, Alvarez RH, De Laurentiis M, et al: Circulating tumor cells as prognostic and predictive markers in metastatic breast cancer patients receiving first-line systemic treatment. Breast Cancer Res. 13:R672011. View Article : Google Scholar | |
Giordano A, Giuliano M, De Laurentiis M, Arpino G, Jackson S, Handy BC, Ueno NT, Andreopoulou E, Alvarez RH, Valero V, 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. 23:1144–1150. 2012. View Article : Google Scholar | |
Bidard FC, Peeters DJ, Fehm T, Nolé F, Gisbert-Criado R, Mavroudis D, Grisanti S, Generali D, Garcia-Saenz JA, Stebbing J, et al: Clinical validity of circulating tumour cells in patients with metastatic breast cancer: A pooled analysis of individual patient data. Lancet Oncol. 15:406–414. 2014. View Article : Google Scholar | |
Lv Q, Gong L, Zhang T, Ye J, Chai L, Ni C and Mao Y: Prognostic value of circulating tumor cells in metastatic breast cancer: A systemic review and meta-analysis. Clin Transl Oncol. 18:322–330. 2016. View Article : Google Scholar | |
Hayes DF, Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Miller MC, Matera J, Allard WJ, Doyle GV and Terstappen LW: 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. View Article : Google Scholar | |
Cristofanilli M, Broglio KR, Guarneri V, Jackson S, Fritsche HA, Islam R, Dawood S, Reuben JM, Kau SW, Lara JM, et al: Circulating tumor cells in metastatic breast cancer: Biologic staging beyond tumor burden. Clin Breast Cancer. 7:471–479. 2007. View Article : Google Scholar | |
Bidard FC, Vincent-Salomon A, Sigal-Zafrani B, Diéras V, Mathiot C, Mignot L, Thiery JP, Sastre-Garau X and Pierga JY: Prognosis of women with stage IV breast cancer depends on detection of circulating tumor cells rather than disseminated tumor cells. Ann Oncol. 19:496–500. 2008. View Article : Google Scholar | |
Yagata H, Nakamura S, Toi M, Bando H, Ohno S and Kataoka A: Evaluation of circulating tumor cells in patients with breast cancer: Multi-institutional clinical trial in Japan. Int J Clin Oncol. 13:252–256. 2008. View Article : Google Scholar | |
De Giorgi U, Valero V, Rohren E, Dawood S, Ueno NT, Miller MC, Doyle GV, Jackson S, Andreopoulou E, Handy BC, et al: Circulating tumor cells and [18F]fluorodeoxyglucose positron emission tomography/computed tomography for outcome prediction in metastatic breast cancer. J Clin Oncol. 27:3303–3311. 2009. View Article : Google Scholar | |
Liu MC, Shields PG, Warren RD, Cohen P, Wilkinson M, Ottaviano YL, Rao SB, Eng-Wong J, Seillier-Moiseiwitsch F, Noone AM and Isaacs C: Circulating tumor cells: A useful predictor of treatment efficacy in metastatic breast cancer. J Clin Oncol. 27:5153–5159. 2009. View Article : Google Scholar | |
Mego M, De Giorgi U, Hsu L, Ueno NT, Valero V, Jackson S, Andreopoulou E, Kau SW, Reuben JM and Cristofanilli M: Circulating tumor cells in metastatic inflammatory breast cancer. Annals Oncol. 20:1824–1828. 2009. View Article : Google Scholar | |
De Giorgi U, Valero V, Rohren E, Mego M, Doyle GV, Miller MC, Ueno NT, Handy BC, Reuben JM, Macapinlac HA, et al: Circulating tumor cells and bone metastases as detected by FDG-PET/CT in patients with metastatic breast cancer. Annals Oncol. 21:33–39. 2010. View Article : Google Scholar | |
Consoli F, Grisanti S, Amoroso V, Almici C, Verardi R, Marini M and Simoncini E: Circulating tumor cells as predictors of prognosis in metastatic breast cancer: Clinical application outside a clinical trial. Tumori. 97:737–742. 2011. View Article : Google Scholar | |
Hartkopf AD, Wagner P, Wallwiener D, Fehm T and Rothmund R: Changing levels of circulating tumor cells in monitoring chemotherapy response in patients with metastatic breast cancer. Anticancer Res. 31:979–984. 2011. | |
Tokudome N, Ito Y, Takahashi S, Kobayashi K, Taira S, Tsutsumi C, Oto M, Oba M, Inoue K, Kuwayama A, et al: Detection of circulating tumor cells in peripheral blood of heavily treated metastatic breast cancer patients. Breast Cancer. 18:195–202. 2011. View Article : Google Scholar | |
De Giorgi U, Mego M, Scarpi E, Giuliano M, Giordano A, Reuben JM, Valero V, Ueno NT, Hortobagyi GN and Cristofanilli M: Relationship between lymphocytopenia and circulating tumor cells as prognostic factors for overall survival in metastatic breast cancer. Clin Breast Cancer. 12:264–269. 2012. View Article : Google Scholar | |
Hayashi N, Nakamura S, Tokuda Y, Shimoda Y, Yagata H, Yoshida A, Ota H, Hortobagyi GN, Cristofanilli M and Ueno NT: Prognostic value of HER2-positive circulating tumor cells in patients with metastatic breast cancer. Int J Clin Oncol. 17:96–104. 2012. View Article : Google Scholar | |
Pierga JY, Hajage D, Bachelot T, Delaloge S, Brain E, Campone M, Diéras V, Rolland E, Mignot L, Mathiot C and Bidard FC: 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. Annals Oncol. 23:618–624. 2012. View Article : Google Scholar | |
Weissenstein U, Schumann A, Reif M, Link S, Toffol-Schmidt UD and Heusser P: Detection of circulating tumor cells in blood of metastatic breast cancer patients using a combination of cytokeratin and EpCAM antibodies. BMC Cancer. 12:2062012. View Article : Google Scholar | |
Jiang ZF, Cristofanilli M, Shao ZM, Tong ZS, Song EW, Wang XJ, Liao N, Hu XC, Liu Y, Wang Y, et al: Circulating tumor cells predict progression-free and overall survival in Chinese patients with metastatic breast cancer, HER2-positive or triple-negative (CBCSG004): A multicenter, double-blind, prospective trial. Annals Oncol. 24:2766–2772. 2013. View Article : Google Scholar | |
Liu Y, Liu Q, Wang T, Bian L, Zhang S, Hu H, Li S, Hu Z, Wu S, Liu B and Jiang Z: Circulating tumor cells in HER2-positive metastatic breast cancer patients: A valuable prognostic and predictive biomarker. BMC Cancer. 13:2022013. View Article : Google Scholar | |
Tarhan MO, Gonel A, Kucukzeybek Y, Erten C, Cuhadar S, Yigit SC, Atay A, Somali I, Dirican A, Demir L and Koseoglu M: Prognostic significance of circulating tumor cells and serum CA15-3 levels in metastatic breast cancer, single center experience, preliminary results. Asian Pac J Cancer Prev. 14:1725–1729. 2013. View Article : Google Scholar | |
Turker I, Uyeturk U, Sonmez OU, Oksuzoglu B, Helvaci K, Arslan UY, Budakoglu B, Alkis N, Aksoy S and Zengin N: Detection of circulating tumor cells in breast cancer patients: Prognostic predictive role. Asian Pac J Cancer Prev. 14:1601–1607. 2013. View Article : Google Scholar | |
Wallwiener M, Hartkopf AD, Baccelli I, Riethdorf S, Schott S, Pantel K, Marmé F, Sohn C, Trumpp A, Rack B, et al: The prognostic impact of circulating tumor cells in subtypes of metastatic breast cancer. Breast Cancer Res Treat. 137:503–510. 2013. View Article : Google Scholar | |
Cristofanilli M, Pierga JY, Reuben J, Rademaker A, Davis AA, Peeters DJ, Fehm T, Nolé F, Gisbert-Criado R, Mavroudis D, et al: The clinical use of circulating tumor cells (CTCs) enumeration for staging of metastatic breast cancer (MBC): International expert consensus paper. Crit Rev Oncol Hematol. 134:39–45. 2019. View Article : Google Scholar | |
Magbanua MJM, Hendrix LH, Hyslop T, Barry WT, Winer EP, Hudis C, Toppmeyer D, Carey LA, Partridge AH, Pierga JY, et al: Serial analysis of circulating tumor cells in metastatic breast cancer receiving first-line chemotherapy. J Natl Cancer Inst. 113:443–452. 2021. View Article : Google Scholar | |
Sundling KE and Lowe AC: Circulating tumor cells: Overview and opportunities in cytology. Adv Anat Pathol. 26:56–63. 2019. View Article : Google Scholar | |
Larsson AM, Jansson S, Bendahl PO, Levin Tykjaer Jörgensen C, Loman N, Graffman C, Lundgren L, Aaltonen K and Rydén L: Longitudinal enumeration and cluster evaluation of circulating tumor cells improve prognostication for patients with newly diagnosed metastatic breast cancer in a prospective observational trial. Breast Cancer Res. 20:482018. View Article : Google Scholar | |
Jauch SF, Riethdorf S, Sprick MR, Schütz F, Schönfisch B, Brucker SY, Deutsch TM, Nees J, Saini M, Becker LM, et al: Sustained prognostic impact of circulating tumor cell status and kinetics upon further progression of metastatic breast cancer. Breast Cancer Res. Treat. 173:155–165. 2019. | |
Cabel L, Berger F, Cottu P, Loirat D, Rampanou A, Brain E, Cyrille S, Bourgeois H, Kiavue N, Deluche E, et al: Clinical utility of circulating tumour cell-based monitoring of late-line chemotherapy for metastatic breast cancer: The randomised CirCe01 trial. Br J Cancer. 124:1207–1213. 2021. View Article : Google Scholar | |
Smerage JB, Barlow WE, Hortobagyi GN, Winer EP, Leyland-Jones B, Srkalovic G, Tejwani S, Schott AF, O'Rourke MA, Lew DL, et al: Circulating tumor cells and response to chemotherapy in metastatic breast cancer: SWOG S0500. J Clin oncol. 32:3483–3489. 2014. View Article : Google Scholar | |
Bidard FC, Jacot W, Kiavue N, Dureau S, Kadi A, Brain E, Bachelot T, Bourgeois H, Gonçalves A, Ladoire S, et al: Efficacy of circulating tumor cell count-driven vs clinician-driven first-line therapy choice in hormone receptor-positive, ERBB2-negative metastatic breast cancer: The STIC CTC randomized clinical trial. JAMA Oncol. 7:34–41. 2021. View Article : Google Scholar | |
Jacot W, Cottu P, Berger F, Dubot C, Venat-Bouvet L, Lortholary A, Bourgeois H, Bollet M, Servent V, Luporsi E, et al: Actionability of HER2-amplified circulating tumor cells in HER2-negative metastatic breast cancer: The CirCe T-DM1 trial. Breast Cancer Res. 21:1212019. View Article : Google Scholar | |
Fehm T, Müller V, Banys-Paluchowski M, Fasching PA, Friedl TWP, Hartkopf AD, Huober J, Loehberg C, Rack B, Riethdorf S, et al: Abstract PD3-12: Efficacy of the tyrosine kinase inhibitor lapatinib in the treatment of patients with HER2-negative metastatic breast cancer and HER2-positive circulating tumor cells-results from the randomized phase III DETECT III trial. Cancer Res. 81 (4 Suppl):PD3–12. 2021. View Article : Google Scholar | |
Amir E, Miller N, Geddie W, Freedman O, Kassam F, Simmons C, Oldfield M, Dranitsaris G, Tomlinson G, Laupacis A, et al: Prospective study evaluating the impact of tissue confirmation of metastatic disease in patients with breast cancer. J Clin Oncol. 30:587–592. 2012. View Article : Google Scholar | |
Simmons C, Miller N, Geddie W, Gianfelice D, Oldfield M, Dranitsaris G and Clemons MJ: Does confirmatory tumor biopsy alter the management of breast cancer patients with distant metastases? Ann Oncol. 20:1499–1504. 2009. View Article : Google Scholar | |
Thompson AM, Jordan LB, Quinlan P, Anderson E, Skene A, Dewar JA and Purdie CA; Breast Recurrence in Tissues Study Group, : Prospective comparison of switches in biomarker status between primary and recurrent breast cancer: The breast recurrence in tissues study (BRITS). Breast Cancer Res. 12:R922010. View Article : Google Scholar | |
Curigliano G, Bagnardi V, Viale G, Fumagalli L, Rotmensz N, Aurilio G, Locatelli M, Pruneri G, Giudici S, Bellomi M, et al: Should liver metastases of breast cancer be biopsied to improve treatment choice? Ann Oncol. 22:2227–2233. 2011. View Article : Google Scholar | |
Xiao C, Gong Y, Han EY, Gonzalez-Angulo AM and Sneige N: Stability of HER2-positive status in breast carcinoma: A comparison between primary and paired metastatic tumors with regard to the possible impact of intervening trastuzumab treatment. Ann Oncol. 22:1547–1553. 2011. View Article : Google Scholar | |
Sari E, Guler G, Hayran M, Gullu I, Altundag K and Ozisik Y: Comparative study of the immunohistochemical detection of hormone receptor status and HER-2 expression in primary and paired recurrent/metastatic lesions of patients with breast cancer. Med Oncol. 28:57–63. 2011. View Article : Google Scholar | |
Amir E, Clemons M, Purdie CA, Miller N, Quinlan P, Geddie W, Coleman RE, Freedman OC, Jordan LB and Thompson AM: Tissue confirmation of disease recurrence in breast cancer patients: Pooled analysis of multi-centre, multi-disciplinary prospective studies. Cancer Treat Rev. 38:708–714. 2012. View Article : Google Scholar | |
Chang HJ, Han SW, Oh DY, Im SA, Jeon YK, Park IA, Han W, Noh DY, Bang YJ and Kim TY: Discordant human epidermal growth factor receptor 2 and hormone receptor status in primary and metastatic breast cancer and response to trastuzumab. Jpn J Clin Oncol. 41:593–599. 2011. View Article : Google Scholar | |
Dieci MV, Barbieri E, Piacentini F, Ficarra G, Bettelli S, Dominici M, Conte PF and Guarneri V: Discordance in receptor status between primary and recurrent breast cancer has a prognostic impact: A single-institution analysis. Ann Oncol. 24:101–108. 2013. View Article : Google Scholar | |
Lindström LS, Karlsson E, Wilking UM, Johansson U, Hartman J, Lidbrink EK, Hatschek T, Skoog L and Bergh J: Clinically used breast cancer markers such as estrogen receptor, progesterone receptor, and human epidermal growth factor receptor 2 are unstable throughout tumor progression. J Clin Oncol. 30:2601–2608. 2012. View Article : Google Scholar | |
Alix-Panabières C and Pantel K: Circulating tumor cells: Liquid biopsy of cancer. Clin Chem. 59:110–118. 2013. View Article : Google Scholar | |
Schochter F, Friedl TWP, deGregorio A, Krause S, Huober J, Rack B and Janni W: Are circulating tumor cells (CTCs) ready for clinical use in breast cancer? An overview of completed and ongoing trials using CTCs for clinical treatment decisions. Cells. 8:14122019. View Article : Google Scholar | |
Müller V, Banys-Paluchowski M, Friedl TWP, Fasching PA, Schneeweiss A, Hartkopf A, Wallwiener D, Rack B, Meier-Stiegen F, Huober J, et al: Prognostic relevance of the HER2 status of circulating tumor cells in metastatic breast cancer patients screened for participation in the DETECT study program. ESMO Open. 6:1002992021. View Article : Google Scholar | |
Paoletti C, Regan MM, Liu MC, Marcom PK, Hart LL, Smith JW, Tedesco KL, Amir E, Krop IE, DeMichele AM, et al: Abstract P1-01-01: Circulating tumor cell number and CTC-endocrine therapy index predict clinical outcomes in ER positive metastatic breast cancer patients: Results of the COMETI phase 2 trial. Cancer Res. 77 (4 Suppl):P1-01-01. 2017. View Article : Google Scholar | |
Salu P and Reindl KM: Advancements in circulating tumor cell research: Bridging biology and clinical applications. Cancers (Basel). 16:12132024. View Article : Google Scholar | |
Smit DJ, Schneegans S and Pantel K: Clinical applications of circulating tumor cells in patients with solid tumors. Clin Exp Metastasis. 41:403–411. 2024. View Article : Google Scholar | |
Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL and Trotti A: AJCC cancer staging manual (7th ed). New York, NY: Springer; 2010 | |
Cabel L, Proudhon C, Gortais H, Loirat D, Coussy F, Pierga JY and Bidard FC: Circulating tumor cells: Clinical validity and utility. Int J Clin Oncol. 22:421–430. 2017. View Article : Google Scholar |