Clinical outcome with correlation to disseminated tumor cell (DTC) status after DTC-guided secondary adjuvant treatment with docetaxel in early breast cancer

Journal of Clinical Oncology

Volumn 32, Issue 34, 2014, Pages 3848-3857

  Naume, Bjørn ^a,b   Synnestvedt, Marit ^a   Falk, Ragnhild Sørum ^a   Wiedswang, Gro ^a   Weyde, Kjetil ^c   Risberg, Terje ^d   Kersten, Christian ^e   Mjaaland, Ingvil ^f   Vindi, Lise ^g   Sommer, Hilde H ^a   Sætersdal, Anna Barbro ^a   Rypdal, Maria Christine ^a   Schirmer, Cecilie Bendigtsen ^a   Wist, Erik Andreas ^a,b   Borgen, Elin ^a,b  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c Sykehuset Innlandet   (Norway)

^d UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

^e Center for Cancer Treatment   (Norway)

^f STAVANGER UNIVERSITY HOSPITAL   (Norway)

^g A lesund Hospital   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHOSPHAMIDE; DOCETAXEL; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIRUBICIN; FLUOROURACIL; TAMOXIFEN; TRASTUZUMAB; ANTINEOPLASTIC AGENT; KERATIN; KI 67 ANTIGEN; TAXOID;

ADULT; ARTICLE; AXILLARY LYMPH NODE; BONE MARROW BIOPSY; BONE MARROW METASTASIS; BREAST CANCER; CANCER ADJUVANT THERAPY; CANCER COMBINATION CHEMOTHERAPY; CANCER RECURRENCE; DISEASE FREE INTERVAL; FEMALE; FOLLOW UP; HUMAN; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; MAJOR CLINICAL STUDY; MULTICENTER STUDY; MULTIPLE CYCLE TREATMENT; PROSPECTIVE STUDY; TREATMENT OUTCOME; ADJUVANT CHEMOTHERAPY; BONE MARROW CELL; BREAST NEOPLASMS; CHEMISTRY; CHI SQUARE DISTRIBUTION; CLINICAL TRIAL; DISEASE FREE SURVIVAL; DRUG ADMINISTRATION; DRUG EFFECTS; IMMUNOHISTOCHEMISTRY; INTRAVENOUS DRUG ADMINISTRATION; KAPLAN MEIER METHOD; MIDDLE AGED; MORTALITY; NORWAY; PATHOLOGY; PREDICTIVE VALUE; PROPORTIONAL HAZARDS MODEL; RETREATMENT; RISK FACTOR; TIME; TREATMENT FAILURE; TUMOR EMBOLISM;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BONE MARROW CELLS; BREAST NEOPLASMS; CHEMOTHERAPY, ADJUVANT; CHI-SQUARE DISTRIBUTION; CYCLOPHOSPHAMIDE; DISEASE-FREE SURVIVAL; DRUG ADMINISTRATION SCHEDULE; EPIRUBICIN; FEMALE; FLUOROURACIL; HUMANS; IMMUNOHISTOCHEMISTRY; INFUSIONS, INTRAVENOUS; KAPLAN-MEIER ESTIMATE; KERATINS; KI-67 ANTIGEN; MIDDLE AGED; NEOPLASTIC CELLS, CIRCULATING; NORWAY; PREDICTIVE VALUE OF TESTS; PROPORTIONAL HAZARDS MODELS; PROSPECTIVE STUDIES; RETREATMENT; RISK FACTORS; TAXOIDS; TIME FACTORS; TREATMENT FAILURE;

EID: 84913596780     PISSN: 0732183X     EISSN: 15277755     Source Type: Journal    
DOI: 10.1200/JCO.2014.56.9327     Document Type: Article

References (81)

1. 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. Lancet 365:1687-1717, 2005
2. Early Breast Cancer Trialists' Collaborative Group (EBCTCG), Peto R, Davies C, et al: Comparisons between different polychemotherapy regimens for early breast cancer: Meta-analyses of long-term outcome among 100,000 women in 123 randomised trials. Lancet 379:432-444, 2012
3. Jacquin JP, Jones S, Magné N, et al: Docetaxel-containing adjuvant chemotherapy in patients with early stage breast cancer: Consistency of effect independent of nodal and biomarker status - A meta-analysis of 14 randomized clinical trials. Breast Cancer Res Treat 134: 903-913, 2012
4. Nabholtz JM, Reese DM, Lindsay MA, et al: Docetaxel in the treatment of breast cancer: An update on recent studies. Semin Oncol 29:28-34, 2002 (suppl 12)
5. Nabholtz JM, Pienkowski T, Mackey J, et al: Phase III trial comparing TAC (docetaxel, doxorubicin, cyclophosphamide) with FAC (5-fluorouracil, doxorubicin, cyclophosphamide) in the adjuvant treatment of node positive breast cancer (BC) patients: Interim analysis of the BCIRG 001 study. Proc Am Soc Clin Oncol 21:141, 2002 (abstr 141)
6. Sotiriou C, Pusztai L: Gene-expression signatures in breast cancer. N Engl J Med 360:790-800, 2009
7. Cancer Genome Atlas Network: Comprehensive molecular portraits of human breast tumours. Nature 490:61-70, 2012
8. Parker JS, Mullins M, Cheang MC, et al: Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 27:1160-1167, 2009
9. Perou CM, Sørlie T, Eisen MB, et al: Molecular portraits of human breast tumours. Nature 406: 747-752, 2000
10. Curtis C, Shah SP, Chin SF, et al: The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 486:346-352, 2012
11. Ellis MJ, Perou CM: The genomic landscape of breast cancer as a therapeutic roadmap. Cancer Discov 3:27-34, 2013
12. Paik S, Shak S, Tang G, et al: A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med 351: 2817-2826, 2004
13. Goldhirsch A, Winer EP, Coates AS, et al: Personalizing the treatment of women with early breast cancer: Highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013. Ann Oncol 24:2206-2223, 2013
14. Shiozawa Y, Havens AM, Pienta KJ, et al: The bone marrow niche: Habitat to hematopoietic and mesenchymal stem cells, and unwitting host to molecular parasites. Leukemia 22:941-950, 2008
15. Wan L, Pantel K, Kang Y: Tumor metastasis: Moving new biological insights into the clinic. Nat Med 19:1450-1464, 2013
16. Bragado P, Estrada Y, Parikh F, et al: TGF-β2 dictates disseminated tumour cell fate in target organs through TGF-β-RIII and p38α/β signalling. Nat Cell Biol 15:1351-1361, 2013
17. Kim RS, Avivar-Valderas A, Estrada Y, et al: Dormancy signatures and metastasis in estrogen receptor positive and negative breast cancer. PLoS One 7:e35569, 2012
18. Koebel CM, Vermi W, Swann JB, et al: Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450:903-907, 2007
19. Aguirre-Ghiso JA: Models, mechanisms and clinical evidence for cancer dormancy. Nat Rev Cancer 7:834-846, 2007
20. Meng S, Tripathy D, Frenkel EP, et al: Circulating tumor cells in patients with breast cancer dormancy. Clin Cancer Res 10:8152-8162, 2004
21. Braun S, Vogl FD, Naume B, et al: A pooled analysis of bone marrow micrometastasis in breast cancer. N Engl J Med 353:793-802, 2005
22. Drageset V, Nesland JM, Erikstein B, et al: Monitoring of disseminated tumor cells in bone marrow in high-risk breast cancer patients treated with high-dose chemotherapy. Int J Cancer 118: 2877-2881, 2006
23. Braun S, Schindlbeck C, Hepp F, et al: Occult tumor cells in bone marrow of patients with locoregionally restricted ovarian cancer predict early distant metastatic relapse. J Clin Oncol 19:368-375, 2001
24. Janni W, Vogl FD, Wiedswang G, et al: Persistence of disseminated tumor cells in the bone marrow of breast cancer patients predicts increased risk for relapse: A European pooled analysis. Clin Cancer Res 17:2967-2976, 2011
25. Hall C, Krishnamurthy S, Lodhi A, et al: Disseminated tumor cells predict survival after neoadjuvant therapy in primary breast cancer. Cancer 118:342-348, 2012
26. Mathiesen RR, Borgen E, Renolen A, et al: Persistence of disseminated tumor cells after neoadjuvant treatment for locally advanced breast cancer predicts poor survival. Breast Cancer Res 14: R117, 2012
27. Sjöström J, Blomqvist C, Mouridsen H, et al: Docetaxel compared with sequential methotrexate and 5-fluorouracil in patients with advanced breast cancer after anthracycline failure: A randomised phase III study with crossover on progression by the Scandinavian Breast Group. Eur J Cancer 35:1194-1201, 1999
28. Nabholtz JM, Senn HJ, Bezwoda WR, et al: Prospective randomized trial of docetaxel versus mitomycin plus vinblastine in patients with metastatic breast cancer progressing despite previous anthracycline-containing chemotherapy: 304 Study Group. J Clin Oncol 17:1413-1424, 1999
29. Chan S, Friedrichs K, Noel D, et al: Prospective randomized trial of docetaxel versus doxorubicin in patients with metastatic breast cancer. J Clin Oncol 17:2341-2354, 1999
30. Borgen E, Naume B, Nesland JM, et al: Standardization of the immunocytochemical detection of cancer cells in BM and blood: I. Establishment of objective criteria for the evaluation of immunostained cells. Cytotherapy 1:377-388, 1999
31. Fehm T, Braun S, Muller V, et al: A concept for the standardized detection of disseminated tumor cells in bone marrow from patients with primary breast cancer and its clinical implementation. Cancer 107:885-892, 2006
32. McShane LM, Altman DG, Sauerbrei W, et al: REporting recommendations for tumor MARKer prognostic studies (REMARK). Breast Cancer Res Treat 100:229-235, 2006
33. Synnestvedt M, Borgen E, Wist E, et al: Disseminated tumor cells as selection marker and monitoring tool for secondary adjuvant treatment in early breast cancer: Descriptive results from an intervention study. BMC Cancer 12:616, 2012
34. Wiedswang G, Borgen E, Ka˚resen R, et al: Detection of isolated tumor cells in bone marrow is an independent prognostic factor in breast cancer. J Clin Oncol 21:3469-3478, 2003
35. Elston CW, Ellis IO: Pathological prognostic factors in breast cancer: I. The value of histological grade in breast cancer - Experience from a large study with long-term follow-up. Histopathology 19: 403-410, 1991
36. SPSS: PASW Statistics for Windows, Version 18.0. http://www-01.ibm.com/support/docview.wss?uid=swg21476197
37. StataCorp: Stata Statistical Software: Release 11. http://www.stata.com/support/faqs/resources/citing-software-documentation-faqs/
38. De Mattos-Arruda L, Cortes J, Santarpia L, et al: Circulating tumour cells and cell-free DNA as tools for managing breast cancer. Nat Rev Clin Oncol 10:377-389, 2013
39. Bednarz-Knoll N, Alix-Panabieres C, Pantel K: Clinical relevance and biology of circulating tumor cells. Breast Cancer Res 13:228, 2011
40. Crowley E, Di Nicolantonio F, Loupakis F, et al: Liquid biopsy: Monitoring cancer-genetics in the blood. Nat Rev Clin Oncol 10:472-484, 2013
41. Pantel K, Brakenhoff RH: Dissecting the metastatic cascade. Nat Rev Cancer 4:448-456, 2004
42. Müller 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 11:3678-3685, 2005
43. Cristofanilli M, Gonzalez-Angulo A, Sneige N, et al: Invasive lobular carcinoma classic type: Response to primary chemotherapy and survival outcomes. J Clin Oncol 23:41-48, 2005
44. Katz A, Saad ED, Porter P, Pusztai L: Primary systemic chemotherapy of invasive lobular carcinoma of the breast. Lancet Oncol 8:55-62, 2007
45. Tubiana-Hulin M, Stevens D, Lasry S, et al: Response to neoadjuvant chemotherapy in lobular and ductal breast carcinomas: A retrospective study on 860 patients from one institution. Ann Oncol 17:1228-1233, 2006
46. Valachis A, Polyzos NP, Coleman RE, et al: Adjuvant therapy with zoledronic acid in patients with breast cancer: A systematic review and meta-analysis. Oncologist 18:353-361, 2013
47. Gnant M, Mlineritsch B, Stoeger H, et al: Adjuvant endocrine therapy plus zoledronic acid in premenopausal women with early-stage breast cancer: 62-month follow-up from the ABCSG-12 randomised trial. Lancet Oncol 12:631-641, 2011
48. Hugh J, Hanson J, Cheang MC, et al: Breast cancer subtypes and response to docetaxel in node-positive breast cancer: Use of an immunohistochemical definition in the BCIRG 001 trial. J Clin Oncol 27:1168-1176, 2009
49. Penault-Llorca F, André F, Sagan C, et al: Ki67 expression and docetaxel efficacy in patients with estrogen receptor-positive breast cancer. J Clin Oncol 27:2809-2815, 2009
50. Baselga J, Campone M, Piccart M, et al: Everolimus in postmenopausal hormone-receptorpositive advanced breast cancer. N Engl J Med 366:520-529, 2012
51. Bachelot T, Bourgier C, Cropet C, et al: Randomized phase II trial of everolimus in combination with tamoxifen in patients with hormone receptor-positive, human epidermal growth factor receptor 2-negative metastatic breast cancer with prior exposure to aromatase inhibitors: A GINECO study. J Clin Oncol 30:2718-2724, 2012
52. Solomayer EF, Gebauer G, Hirnle P, et al: Influence of zoledronic acid on disseminated tumor cells in primary breast cancer patients. Ann Oncol 23:2271-2277, 2012
53. Rack B, Jückstock J, Günthner-Biller M, et al: Trastuzumab clears HER2/neu-positive isolated tumor cells from bone marrow in primary breast cancer patients. Arch Gynecol Obstet 285:485-492, 2012
54. Naume B, Borgen E, Nesland JM, et al: Increased sensitivity for detection of micrometastases in bone-marrow/peripheral-blood stem-cell products from breast-cancer patients by negative immunomagnetic separation. Int J Cancer 78:556-560, 1998
55. Pantel K, Brakenhoff RH, Brandt B: Detection, clinical relevance and specific biological properties of disseminating tumour cells. Nat Rev Cancer 8:329-340, 2008
56. 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. Br J Cancer 101:589-597, 2009
57. Becker S, Becker-Pergola G, Banys M, et al: Evaluation of a RT-PCR based routine screening tool for the detection of disseminated epithelial cells in the bone marrow of breast cancer patients. Breast Cancer Res Treat 117:227-233, 2009
58. 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 Cancer 7:146-152, 2006
59. Gilje B, Nordga˚rd O, Tjensvoll K, et al: Comparison of molecular and immunocytochemical methods for detection of disseminated tumor cells in bone marrow from early breast cancer patients. BMC Cancer 14:514, 2014
60. Wiedswang G, Borgen E, Karesen R, et al: Detection of isolated tumor cells in BM from breastcancer patients: Significance of anterior and posterior iliac crest aspirations and the number of mononuclear cells analyzed. Cytotherapy 5:40-45, 2003
61. Czyz ZT, Hoffmann M, Schlimok G, et al: Reliable single cell array CGH for clinical samples. PLoS One 9:e85907, 2014
62. Fuhrmann C, Schmidt-Kittler O, Stoecklein NH, et al: High-resolution array comparative genomic hybridization of single micrometastatic tumor cells. Nucleic Acids Res 36:e39, 2008
63. Mathiesen RR, Fjelldal R, Liestøl K, et al: High-resolution analyses of copy number changes in disseminated tumor cells of patients with breast cancer. Int J Cancer 131:E405-E415, 2012
64. Yu M, Bardia A, Wittner BS, et al: Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 339: 580-584, 2013
65. Siddappa CM, Watson MA, Pillai SG, et al: Detection of disseminated tumor cells in the bone marrow of breast cancer patients using multiplex gene expression measurements identifies new therapeutic targets in patients at high risk for the development of metastatic disease. Breast Cancer Res Treat 137:45-56, 2013
66. Payne RE, Wang F, Su N, et al: Viable circulating tumour cell detection using multiplex RNA in situ hybridisation predicts progression-free survival in metastatic breast cancer patients. Br J Cancer 106:1790-1797, 2012
67. Balic M, Rapp N, Stanzer S, et al: Novel immunofluorescence protocol for multimarker assessment of putative disseminating breast cancer stem cells. Appl Immunohistochem Mol Morphol 19:33-40, 2011
68. Moller EK, Kumar P, Voet T, et al: Nextgeneration sequencing of disseminated tumor cells. Front Oncol 3:320, 2013
69. Heitzer E, Auer M, Gasch C, et al: Complex tumor genomes inferred from single circulating tumor cells by array-CGH and next-generation sequencing. Cancer Res 73:2965-2975, 2013
70. Navin N, Kendall J, Troge J, et al: Tumour evolution inferred by single-cell sequencing. Nature 472:90-94, 2011
71. Dawson SJ, Tsui DW, Murtaza M, et al: Analysis of circulating tumor DNA to monitor metastatic breast cancer. N Engl J Med 368:1199-1209, 2013
72. Bettegowda C, Sausen M, Leary RJ, et al: Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med 19: 224ra24, 2014
73. Xenidis N, Perraki M, Kafousi M, et al: Predictive and prognostic value of peripheral blood cytokeratin-19 mRNA-positive cells detected by realtime polymerase chain reaction in node-negative breast cancer patients. J Clin Oncol 24:3756-3762, 2006
74. Xenidis N, Ignatiadis M, Apostolaki S, et al: Cytokeratin-19 mRNA-positive circulating tumor cells after adjuvant chemotherapy in patients with early breast cancer. J Clin Oncol 27:2177-2184, 2009
75. Molloy TJ, Bosma AJ, Baumbusch LO, et al: The prognostic significance of tumour cell detection in the peripheral blood versus the bone marrow in 733 early-stage breast cancer patients. Breast Cancer Res 13:R61, 2011
76. Rack BK, Schindlbeck C, Andergassen U, et al: Use of circulating tumor cells (CTC) in peripheral blood of breast cancer patients before and after adjuvant chemotherapy to predict risk for relapse: The SUCCESS trial. J Clin Oncol 28, 2010 (suppl 15s; abstr 1003)
77. Franken B, de Groot MR, Mastboom WJ, et al: Circulating tumor cells, disease recurrence and survival in newly diagnosed breast cancer. Breast Cancer Res 14:R133, 2012
78. Benoy IH, Elst H, Philips M, 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 94:672-680, 2006
79. 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 10:1392-1400, 2004
80. 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 Cancer 118:2013-2019, 2006
81. Bednarz-Knoll N, Alix-Panabières C, Pantel K: Plasticity of disseminating cancer cells in patients with epithelial malignancies. Cancer Metastasis Rev 31:673-687, 2012