Significance of micrometastasis in bone marrow and blood of operable breast cancer patients: research tool or clinical application?

References

• Fisher B, Anderson S, Bryant J et al. Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer. N. Engl. J. Med.347(16), 1233–1241 (2002).
   PubMed Web of Science ®Google Scholar
• Mansi JL, Gogas H, Bliss JM et al. Outcome of primary-breast-cancer patients with micrometastases: a long-term follow-up study. Lancet354(9174), 197–202 (1999).
   PubMed Web of Science ®Google Scholar
• Mirza AN, Mirza NQ, Vlastos G et al. Prognostic factors in node-negative breast cancer: a review of studies with sample size more than 200 and follow-up more than 5 years. Ann. Surg.235(1), 10–26 (2002).
   PubMed Web of Science ®Google Scholar
• Pantel K, Brakenhoff RH. Dissecting the metastatic cascade. Nat. Rev. Cancer4(6), 448–456 (2004).
   PubMed Web of Science ®Google Scholar
• Pantel K, Woelfle U. Micrometastasis in breast cancer and other solid tumors. J. Biol. Regul. Homeost. Agents18(2), 120–125 (2004).
   PubMed Web of Science ®Google Scholar
• Early Breast Cancer Trialists’ Collaborative Group (EBCTCG). Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet365(9472), 1687–1717 (2005).
   PubMed Web of Science ®Google Scholar
• Braun S, Vogl FD, Naume B et al. A pooled analysis of bone marrow micrometastasis in breast cancer. N. Engl. J. Med.353(8), 793–802 (2005).
   PubMed Web of Science ®Google Scholar
• Diel IJ. Bone marrow staging for breast cancer: is it better than axillary node dissection? Semin. Oncol.28(3), 236–244 (2001).
   PubMed Web of Science ®Google Scholar
• Pantel K, Cote RJ, Fodstad O. Detection and clinical importance of micrometastatic disease. J. Natl Cancer Inst.91(13), 1113–1124 (1999).
   PubMedGoogle Scholar
• Osborne MP, Rosen PP. Detection and management of bone marrow micrometastases in breast cancer. Oncology (Williston Park)8(8), 25–31; discussion 35–26, 39–42 (1994).
   PubMedGoogle Scholar
• Gebauer G, Fehm T, Merkle E et al. Epithelial cells in bone marrow of breast cancer patients at time of primary surgery: clinical outcome during long-term follow-up. J. Clin. Oncol.19(16), 3669–3674 (2001).
   PubMed Web of Science ®Google Scholar
• Solomayer EF, Diel IJ, Salanti G et al. Time independence of the prognostic impact of tumor cell detection in the bone marrow of primary breast cancer patients. Clin. Cancer Res.7(12), 4102–4108 (2001).
   PubMed Web of Science ®Google Scholar
• Benoy IH, Salgado R, Elst H et al. Relative microvessel area of the primary tumour, and not lymph node status, predicts the presence of bone marrow micrometastases detected by reverse transcriptase polymerase chain reaction in patients with clinically non-metastatic breast cancer. Breast Cancer Res.7(2), R210–R219 (2005).
   Google Scholar
• Hemsen A, Riethdorf L, Brunner N et al. Comparative evaluation of urokinase-type plasminogen activator receptor expression in primary breast carcinomas and on metastatic tumor cells. Int. J. Cancer107(6), 903–909 (2003).
   PubMed Web of Science ®Google Scholar
• Landys K, Persson S, Kovarik J et al. Prognostic value of bone marrow biopsy in operable breast cancer patients at the time of initial diagnosis: results of a 20-year median follow-up. Breast Cancer Res. Treat.49(1), 27–33 (1998).
   PubMed Web of Science ®Google Scholar
• Braun S, Schlimok G, Heumos I et al. ErbB2 overexpression on occult metastatic cells in bone marrow predicts poor clinical outcome of stage I–III breast cancer patients. Cancer Res.61(5), 1890–1895 (2001).
   PubMed Web of Science ®Google Scholar
• Choesmel V, Pierga JY, Nos C et al. Enrichment methods to detect bone marrow micrometastases in breast carcinoma patients: clinical relevance. Breast Cancer Res.6(5), R556–R570 (2004).
   PubMed Web of Science ®Google Scholar
• Braun S, Pantel K, Muller P et al. Cytokeratin-positive cells in the bone marrow and survival of patients with stage I, II, or III breast cancer. N. Engl. J. Med.342(8), 525–533 (2000).
   PubMed Web of Science ®Google Scholar
• Gerber B, Krause A, Muller H et al. Simultaneous immunohistochemical detection of tumor cells in lymph nodes and bone marrow aspirates in breast cancer and its correlation with other prognostic factors. J. Clin. Oncol.19(4), 960–971 (2001).
   PubMed Web of Science ®Google Scholar
• Braun S, Cevatli BS, Assemi C et al. Comparative analysis of micrometastasis to the bone marrow and lymph nodes of node-negative breast cancer patients receiving no adjuvant therapy. J. Clin. Oncol.19(5), 1468–1475 (2001).
   PubMed Web of Science ®Google Scholar
• Wiedswang G, Borgen E, Karesen R et al. Detection of isolated tumor cells in bone marrow is an independent prognostic factor in breast cancer. J. Clin. Oncol.21(18), 3469–3478 (2003).
   PubMed Web of Science ®Google Scholar
• Braun S, Naume B. Circulating and disseminated tumor cells. J. Clin. Oncol.23(8), 1623–1626 (2005).
   PubMed Web of Science ®Google Scholar
• Racila E, Euhus D, Weiss AJ et al. Detection and characterization of carcinoma cells in the blood. Proc. Natl Acad. Sci. USA95(8), 4589–4594 (1998).
   PubMed Web of Science ®Google Scholar
• Mehes G, Witt A, Kubista E et al. Circulating breast cancer cells are frequently apoptotic. Am. J. Pathol.159(1), 17–20 (2001).
   PubMed Web of Science ®Google Scholar
• Bauer KD, de la Torre-Bueno J, Diel IJ et al. Reliable and sensitive analysis of occult bone marrow metastases using automated cellular imaging. Clin. Cancer Res.6(9), 3552–3559 (2000).
   PubMed Web of Science ®Google Scholar
• 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(9), 3020–3028 (2004).
   PubMed Web of Science ®Google Scholar
• Witzig TE, Bossy B, Kimlinger T et al. Detection of circulating cytokeratin-positive cells in the blood of breast cancer patients using immunomagnetic enrichment and digital microscopy. Clin. Cancer Res.8(5), 1085–1091 (2002).
   PubMed Web of Science ®Google Scholar
• Benoy IH, Elst H, Philips M et al. Real-time RTPCR 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. Cancer94(5), 672–680 (2006).
   PubMed Web of Science ®Google Scholar
• Slade MJ, Singh A, Smith BM et al. Persistence of bone marrow micrometastases in patients receiving adjuvant therapy for breast cancer: results at 4 years. Int. J. Cancer114(1), 94–100 (2005).
   PubMed Web of Science ®Google Scholar
• Masuda TA, Kataoka A, Ohno S et al. Detection of occult cancer cells in peripheral blood and bone marrow by quantitative RTPCR assay for cytokeratin-7 in breast cancer patients. Int. J. Oncol.26(3), 721–730 (2005).
   PubMed Web of Science ®Google Scholar
• Nogi H, Takeyama H, Uchida K et al. Detection of MUC1 and keratin 19 mRNAs in the bone marrow by quantitative RTPCR predicts the risk of distant metastasis in breast cancer patients. Breast Cancer10(1), 74–81 (2003).
   PubMedGoogle Scholar
• Jung YS, Lee KJ, Kim HJ et al. Clinical significance of bone marrow micrometastasis detected by nested rtPCR for keratin-19 in breast cancer patients. Jpn. J. Clin. Oncol.33(4), 167–172 (2003).
   PubMed Web of Science ®Google Scholar
• Kruger W, Krzizanowski C, Holweg M et al. Reverse transcriptase/polymerase chain reaction detection of cytokeratin-19 mRNA in bone marrow and blood of breast cancer patients. J. Cancer Res. Clin. Oncol.122(11), 679–686 (1996).
   PubMed Web of Science ®Google Scholar
• Gerhard M, Juhl H, Kalthoff H et al. Specific detection of carcinoembryonic antigen-expressing tumor cells in bone marrow aspirates by polymerase chain reaction. J. Clin. Oncol.12(4), 725–729 (1994).
   PubMed Web of Science ®Google Scholar
• Schindlbeck C, Jeschke U, Schulze S et al. Characterisation of disseminated tumor cells in the bone marrow of breast cancer patients by the Thomsen-Friedenreich tumor antigen. Histochem. Cell Biol.123(6), 631–637 (2005).
   PubMed Web of Science ®Google Scholar
• Ferrucci PF, Rabascio C, Gigli F et al. A new comprehensive gene expression panel to study tumor micrometastasis in patients with high-risk breast cancer. Int. J. Oncol.30(4), 955–962 (2007).
   PubMed Web of Science ®Google Scholar
• Diel IJ, Kaufmann M, Costa SD et al. Micrometastatic breast cancer cells in bone marrow at primary surgery: prognostic value in comparison with nodal status. J. Natl Cancer Inst.88(22), 1652–1658 (1996).
   PubMed Web of Science ®Google Scholar
• Freire T, Berois N, Sonora C et al. UDP-N-acetyl-d-galactosamine: polypeptide N-acetylgalactosaminyl transferase 6 (ppGalNAc-T6) mRNA as a potential new marker for detection of bone marrow-disseminated breast cancer cells. Int. J. Cancer119(6), 1383–1388 (2006).
   PubMed Web of Science ®Google Scholar
• Berois N, Varangot M, Sonora C et al. Detection of bone marrow-disseminated breast cancer cells using an RTPCR assay of MUC5B mRNA. Int. J. Cancer103(4), 550–555 (2003).
   PubMed Web of Science ®Google Scholar
• Zippelius A, Kufer P, Honold G et al. Limitations of reverse-transcriptase polymerase chain reaction analyses for detection of micrometastatic epithelial cancer cells in bone marrow. J. Clin. Oncol.15(7), 2701–2708 (1997).
   PubMed Web of Science ®Google Scholar
• Cristofanilli M, Budd GT, Ellis MJ et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N. Engl. J. Med.351(8), 781–791 (2004).
   PubMed Web of Science ®Google Scholar
• Budd GT, Cristofanilli M, Ellis MJ et al. Circulating tumor cells versus imaging – predicting overall survival in metastatic breast cancer. Clin. Cancer Res.12(21), 6403–6409 (2006).
   PubMed Web of Science ®Google Scholar
• 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(14 Pt 1), 4218–4224 (2006).
   PubMed Web of Science ®Google Scholar
• Ross AA, Cooper BW, Lazarus HM et al. Detection and viability of tumor cells in peripheral blood stem cell collections from breast cancer patients using immunocytochemical and clonogenic assay techniques. Blood82(9), 2605–2610 (1993).
   PubMed Web of Science ®Google Scholar
• Rosenberg R, Gertler R, Friederichs J et al. Comparison of two density gradient centrifugation systems for the enrichment of disseminated tumor cells in blood. Cytometry49(4), 150–158 (2002).
   PubMedGoogle Scholar
• Ring A, Smith IE, Dowsett M. Circulating tumour cells in breast cancer. Lancet Oncol.5(2), 79–88 (2004).
   PubMed Web of Science ®Google Scholar
• Benoy IH, Elst H, Philips M et al. Prognostic significance of disseminated tumor cells as detected by quantitative real-time reverse-transcriptase polymerase chain reaction in patients with breast cancer. Clin. Breast Cancer7(2), 146–152 (2006).
   PubMed Web of Science ®Google Scholar
• Gebauer G, Fehm T, Merkle E et al. Micrometastases in axillary lymph nodes and bone marrow of lymph node-negative breast cancer patients – prognostic relevance after 10 years. Anticancer Res.23(5B), 4319–4324 (2003).
   PubMed Web of Science ®Google Scholar
• Weinschenker P, Soares HP, Clark O et al. Immunocytochemical detection of epithelial cells in the bone marrow of primary breast cancer patients: a meta-analysis. Breast Cancer Res. Treat.87(3), 215–224 (2004).
   PubMed Web of Science ®Google Scholar
• Wiedswang G, Borgen E, Karesen R et al. Isolated tumor cells in bone marrow three years after diagnosis in disease-free breast cancer patients predict unfavorable clinical outcome. Clin. Cancer Res.10(16), 5342–5348 (2004).
   PubMed Web of Science ®Google Scholar
• Janni W, Rack B, Schindlbeck C et al. The persistence of isolated tumor cells in bone marrow from patients with breast carcinoma predicts an increased risk for recurrence. Cancer103(5), 884–891 (2005).
   PubMed Web of Science ®Google Scholar
• Yie SM, Luo B, Ye NY et al. Detection of Survivin-expressing circulating cancer cells in the peripheral blood of breast cancer patients by a RTPCR ELISA. Clin. Exp. Metastasis23(5–6), 279–289 (2006).
   PubMed Web of Science ®Google Scholar
• Wulfing P, Borchard J, Buerger H et al. HER2-positive circulating tumor cells indicate poor clinical outcome in stage I to III breast cancer patients. Clin. Cancer Res.12(6), 1715–1720 (2006).
   PubMed Web of Science ®Google Scholar
• Zach O, Kasparu H, Wagner H et al. Prognostic value of tumour cell detection in peripheral blood of breast cancer patients. Acta Med. Austriaca Suppl.59, 32–34 (2002).
   PubMedGoogle Scholar
• 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(16), 3404–3412 (2002).
   PubMed Web of Science ®Google Scholar
• Gaforio JJ, Serrano MJ, Sanchez-Rovira P 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. Cancer107(6), 984–990 (2003).
   PubMed Web of Science ®Google Scholar
• Muller V, Stahmann N, Riethdorf S et al. Circulating tumor cells in breast cancer: correlation to bone marrow micrometastases, heterogeneous response to systemic therapy and low proliferative activity. Clin. Cancer Res.11(10), 3678–3685 (2005).
   PubMed Web of Science ®Google Scholar
• Stathopoulos EN, Sanidas E, Kafousi M et al. Detection of CK-19 mRNA-positive cells in the peripheral blood of breast cancer patients with histologically and immunohistochemically negative axillary lymph nodes. Ann. Oncol.16(2), 240–246 (2005).
   PubMedGoogle Scholar
• Pierga JY, Bonneton C, Vincent-Salomon A 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.10(4), 1392–1400 (2004).
   PubMed Web of Science ®Google Scholar
• Wiedswang G, Borgen E, Schirmer C et al. Comparison of the clinical significance of occult tumor cells in blood and bone marrow in breast cancer. Int. J. Cancer118(8), 2013–2019 (2006).
   PubMed Web of Science ®Google Scholar
• Zach O, Lutz D. Tumor cell detection in peripheral blood and bone marrow. Curr. Opin. Oncol.18(1), 48–56 (2006).
   PubMed Web of Science ®Google Scholar
• Gradilone A, Gazzaniga P, Silvestri I et al. Detection of CK19, CK20 and EGFR mRNAs in peripheral blood of carcinoma patients: correlation with clinical stage of disease. Oncol. Rep.10(1), 217–222 (2003).
   PubMed Web of Science ®Google Scholar
• Lobodasch K, Frohlich F, Rengsberger M et al. Quantification of circulating tumour cells for the monitoring of adjuvant therapy in breast cancer: an increase in cell number at completion of therapy is a predictor of early relapse. Breast16(2), 211–218 (2007).
   PubMed Web of Science ®Google Scholar
• Xenidis N, Vlachonikolis I, Mavroudis D et al. Peripheral blood circulating cytokeratin-19 mRNA-positive cells after the completion of adjuvant chemotherapy in patients with operable breast cancer. Ann. Oncol.14(6), 849–855 (2003).
   PubMed Web of Science ®Google Scholar
• Solakoglu O, Maierhofer C, Lahr G et al. Heterogeneous proliferative potential of occult metastatic cells in bone marrow of patients with solid epithelial tumors. Proc. Natl Acad. Sci. USA99(4), 2246–2251 (2002).
   PubMed Web of Science ®Google Scholar
• Klein CA, Blankenstein TJ, Schmidt-Kittler O et al. Genetic heterogeneity of single disseminated tumour cells in minimal residual cancer. Lancet360(9334), 683–689 (2002).
   PubMed Web of Science ®Google Scholar
• Klein CA, Seidl S, Petat-Dutter K et al. Combined transcriptome and genome analysis of single micrometastatic cells. Nat. Biotechnol.20(4), 387–392 (2002).
   PubMed Web of Science ®Google Scholar
• Schmidt-Kittler O, Ragg T, Daskalakis A et al. From latent disseminated cells to overt metastasis: genetic analysis of systemic breast cancer progression. Proc. Natl Acad. Sci. USA100(13), 7737–7742 (2003).
   PubMed Web of Science ®Google Scholar
• Gangnus R, Langer S, Breit E et al. Genomic profiling of viable and proliferative micrometastatic cells from early-stage breast cancer patients. Clin. Cancer Res.10(10), 3457–3464 (2004).
   PubMed Web of Science ®Google Scholar
• Albertson DG, Collins C, McCormick F et al. Chromosome aberrations in solid tumors. Nat. Genet.34(4), 369–376 (2003).
   PubMed Web of Science ®Google Scholar
• Lacroix M. Significance, detection and markers of disseminated breast cancer cells. Endocr. Relat. Cancer13(4), 1033–1067 (2006).
   PubMed Web of Science ®Google Scholar
• Fehm T, Sagalowsky A, Clifford E et al. Cytogenetic evidence that circulating epithelial cells in patients with carcinoma are malignant. Clin. Cancer Res.8(7), 2073–2084 (2002).
   PubMed Web of Science ®Google Scholar
• Meng S, Tripathy D, Frenkel EP et al. Circulating tumor cells in patients with breast cancer dormancy. Clin. Cancer Res.10(24), 8152–8162 (2004).
   PubMed Web of Science ®Google Scholar
• Meng S, Tripathy D, Shete S et al. uPAR and HER-2 gene status in individual breast cancer cells from blood and tissues. Proc. Natl Acad. Sci. USA103(46), 17361–17365 (2006).
   PubMed Web of Science ®Google Scholar
• Meng S, Tripathy D, Shete S et al. HER-2 gene amplification can be acquired as breast cancer progresses. Proc. Natl Acad. Sci. USA101(25), 9393–9398 (2004).
   PubMed Web of Science ®Google Scholar
• Chambers AF, Groom AC, MacDonald IC. Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer2(8), 563–572 (2002).
   PubMed Web of Science ®Google Scholar
• Liotta LA, Stetler-Stevenson WG. Tumor invasion and metastasis: an imbalance of positive and negative regulation. Cancer Res.51(Suppl. 18), S5054–S5059 (1991).
   PubMed Web of Science ®Google Scholar
• Braun S, Pantel K. Biological characteristics of micrometastatic cancer cells in bone marrow. Cancer Metastasis Rev.18(1), 75–90 (1999).
   PubMed Web of Science ®Google Scholar
• Braun S, Kentenich C, Janni W et al. Lack of effect of adjuvant chemotherapy on the elimination of single dormant tumor cells in bone marrow of high-risk breast cancer patients. J. Clin. Oncol.18(1), 80–86 (2000).
   PubMed Web of Science ®Google Scholar
• Loo WT, Fong JH, Zhu L et al. The value of bone marrow aspirates culture for the detection of bone marrow micrometastasis in breast cancer. Biomed. Pharmacother59(Suppl. 2), S384–S386 (2005).
   Google Scholar
• Pierga JY, Bonneton C, Magdelenat H et al. Clinical significance of proliferative potential of occult metastatic cells in bone marrow of patients with breast cancer. Br. J. Cancer89(3), 539–545 (2003).
   PubMed Web of Science ®Google Scholar
• Kraus J, Pantel K, Pinkel D et al. High-resolution genomic profiling of occult micrometastatic tumor cells. Genes Chromosomes Cancer36(2), 159–166 (2003).
   PubMed Web of Science ®Google Scholar
• Putz E, Witter K, Offner S et al. Phenotypic characteristics of cell lines derived from disseminated cancer cells in bone marrow of patients with solid epithelial tumors: establishment of working models for human micrometastases. Cancer Res.59(1), 241–248 (1999).
   PubMed Web of Science ®Google Scholar
• Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc. Natl Acad. Sci. USA100, 3983–3988 (2003).
   PubMed Web of Science ®Google Scholar
• Phillips TM, McBride WH, Pajonk F. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J. Natl Cancer Inst.98(24), 1777–1785 (2006).
   PubMed Web of Science ®Google Scholar
• Shackleton M, Vaillant F, Simpson KJ et al. Generation of a functional mammary gland from a single stem cell. Nature439(7072), 84–88 (2006).
   PubMed Web of Science ®Google Scholar
• Liu S, Dontu G, Wicha MS. Mammary stem cells, self-renewal pathways, and carcinogenesis. Breast Cancer Res.7(3), 86–95 (2005).
   PubMed Web of Science ®Google Scholar
• Li Y, Rosen JM. Stem/progenitor cells in mouse mammary gland development and breast cancer. J. Mammary Gland Biol. Neoplasia10(1), 17–24 (2005).
   PubMed Web of Science ®Google Scholar
• Dalerba P, Cho RW, Clarke MF. Cancer stem cells: models and concepts. Annu. Rev. Med.58, 267–284 (2007).
   PubMed Web of Science ®Google Scholar
• Liu R, Wang X, Chen GY et al. The prognostic role of a gene signature from tumorigenic breast-cancer cells. N. Engl. J. Med.356(3), 217–26 (2007).
   PubMed Web of Science ®Google Scholar
• Balic M, Lin H, Young L et al. Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative breast cancer stem cell phenotype. Clin. Cancer Res.12(19), 5615–5621 (2006).
   PubMed Web of Science ®Google Scholar
• Korah R, Boots M, Wieder R. Integrin α5β1 promotes survival of growth-arrested breast cancer cells: an in vitro paradigm for breast cancer dormancy in bone marrow. Cancer Res.64(13), 4514–4522 (2004).
   PubMed Web of Science ®Google Scholar
• Trocciola S, Hoda, S, Osborne et al. Do bone marrow micrometastases correlate with sentinel lymph node metastases in breast cancer patients? J. Am. Coll. Surg.200(5), 720–725 (2005).
   PubMed Web of Science ®Google Scholar
• Becker S, Becker-Pergola G, Fehm T, Emig R, Wallwiener D, Solomayer E. Image analysis systems for the detection of disseminated breast cancer cells on bone-marrow cytospins. J. Clin. Lab. Anal.19(3), 115–119 (2005).
   PubMed Web of Science ®Google Scholar
• Yu J, Brennan M, Christos P, Osborne M, Hoda S, Simmons R. Bone marrow micrometastases and adjuvant treatment of breast cancer. Breast J.10(3), 181–185 (2004).
   PubMedGoogle Scholar