Triple-Negative Breast Cancer: What the Radiologist Needs to Know

Seminars in Roentgenology

Volumn 46, Issue 1, 2011, Pages 26-39

  Whitman, Gary J ^a   Albarracin, Constance T ^a   Gonzalez Angulo, Ana Maria ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS INHIBITOR; ANTHRACYCLINE DERIVATIVE; BRCA1 PROTEIN; CAPECITABINE; CYCLOPHOSPHAMIDE; DOXORUBICIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIRUBICIN; EPOTHILONE DERIVATIVE; ESTROGEN RECEPTOR; FLUORODEOXYGLUCOSE F 18; FLUOROURACIL; IXABEPILONE; KI 67 ANTIGEN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PACLITAXEL; PLATINUM COMPLEX; PROGESTERONE RECEPTOR; PROTEIN P53; TAXANE DERIVATIVE; ZOLEDRONIC ACID;

ARTICLE; BREAST ADENOCARCINOMA; BREAST BIOPSY; BREAST CALCIFICATION; BREAST CANCER; CANCER HORMONE THERAPY; CANCER INVASION; CANCER RISK; CANCER SCREENING; CANCER STAGING; CHROMOSOME 17; CONTRAST ENHANCEMENT; DISTANT METASTASIS; ECHOMAMMOGRAPHY; GENE AMPLIFICATION; GENE EXPRESSION; HUMAN; INTRADUCTAL CARCINOMA; LYMPH NODE DISSECTION; MAMMOGRAPHY; MASTECTOMY; MULTIPLE CYCLE TREATMENT; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITRON EMISSION TOMOGRAPHY; PREVALENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CLASSIFICATION; TUMOR VOLUME;

BREAST NEOPLASMS; DIAGNOSTIC IMAGING; FEMALE; GENES, BRCA1; GENES, P53; HUMANS; MUTATION; RECEPTOR, ERBB-2; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE; RISK FACTORS; TUMOR MARKERS, BIOLOGICAL;

EID: 78649839311     PISSN: 0037198X     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.ro.2010.09.004     Document Type: Article

References (89)

1. Perou C.M., Sorlie T., Eisen M.B., et al. Molecular portraits of human breast tumours. Nature 2000, 406:747-752.
2. Sorlie T. Molecular portraits of breast cancer: tumour subtypes as distinct disease entities. Eur J Cancer 2004, 40:2667-2675.
3. Sorlie T., Perou C.M., Tibshirani R., et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 2001, 98:10869-10874.
4. Brenton J.D., Carey L.A., Ahmed A.A., et al. Molecular classification and molecular forecasting of breast cancer: ready for clinical application?. J Clin Oncol 2005, 23:7350-7360.
5. Dent R., Trudeau M., Pritchard K.I., et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res 2007, 13:4429-4434.
6. Rakha E.A., Elsheikh S.E., Aleskandarany M.A., et al. Triple-negative breast cancer: distinguishing between basal and nonbasal subtypes. Clin Cancer Res 2009, 15:2302-2310.
7. Livasy C.A., Karaca G., Nanda R., et al. Phenotypic evaluation of the basal-like subtype of invasive breast carcinoma. Mod Pathol 2006, 19:264-271.
8. Bertucci F., Finetti P., Cervera N., et al. How basal are triple-negative breast cancers?. Int J Cancer 2008, 123:236-240.
9. Nielsen T.O., Hsu F.D., Jensen K., et al. Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res 2004, 10:5367-5374.
10. Carey L.A., Perou C.M., Livasy C.A., et al. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 2006, 295:2492-2502.
11. Cheang M.C., Voduc D., Bajdik C., et al. Basal-like breast cancer defined by five biomarkers has superior prognostic value than triple-negative phenotype. Clin Cancer Res 2008, 14:1368-1376.
12. Tischkowitz M., Brunet J.S., Begin L.R., et al. Use of immunohistochemical markers can refine prognosis in triple negative breast cancer. BMC Cancer 2007, 7:134.
13. Gusterson B.A., Warburton M.J., Mitchell D., et al. Distribution of myoepithelial cells and basement membrane proteins in the normal and in benign and malignant breast diseases. Cancer Res 1982, 42:4763-4770.
14. Moll R., Franke W.W., Schiller D.L., et al. The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells. Cell 1982, 31:11-24.
15. Allred D.C., Bustamante M.A., Daniel C.O., et al. Immunocytochemical analysis of estrogen receptors in human breast carcinomas. Evaluation of 130 cases and review of the literature regarding concordance with biochemical assay and clinical relevance. Arch Surg 1990, 125:107-113.
16. Goldhirsch A., Glick J.H., Gelber R.D., et al. Meeting highlights: International Consensus Panel on the Treatment of Primary Breast Cancer. Seventh International Conference on Adjuvant Therapy of Primary Breast Cancer. J Clin Oncol 2001, 19:3817-3827.
17. Osborne C.K., Yochmowitz M.G., Knight W.A., et al. The value of estrogen and progesterone receptors in the treatment of breast cancer. Cancer 1980, 46:2884-2888.
18. Harvey J.M., Clark G.M., Osborne C.K., et al. Estrogen receptor status by immunohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer. J Clin Oncol 1999, 17:1474-1481.
19. Love R.R., Duc N.B., Allred D.C., et al. Oophorectomy and tamoxifen adjuvant therapy in premenopausal Vietnamese and Chinese women with operable breast cancer. J Clin Oncol 2002, 20:2559-2566.
20. Mohsin S.K., Weiss H., Havighurst T., et al. Progesterone receptor by immunohistochemistry and clinical outcome in breast cancer: a validation study. Mod Pathol 2004, 17:1545-1554.
21. Layfield L.J., Goldstein N., Perkinson K.R., et al. Interlaboratory variation in results from immunohistochemical assessment of estrogen receptor status. Breast J 2003, 9:257-259.
22. Rhodes A., Jasani B., Balaton A.J., et al. Study of interlaboratory reliability and reproducibility of estrogen and progesterone receptor assays in Europe. Documentation of poor reliability and identification of insufficient microwave antigen retrieval time as a major contributory element of unreliable assays. Am J Clin Pathol 2001, 115:44-58.
23. Bevitt D.J., Milton I.D., Piggot N., et al. New monoclonal antibodies to oestrogen and progesterone receptors effective for paraffin section immunohistochemistry. J Pathol 1997, 183:228-232.
24. Elledge R.M., Green S., Pugh R., et al. Estrogen receptor (ER) and progesterone receptor (Pgr), by ligand-binding assay compared with ER, PgR and pS2, by immuno-histochemistry in predicting response to tamoxifen in metastatic breast cancer: a Southwest Oncology Group Study. Int J Cancer 2000, 89:111-117.
25. Cheang M.C., Treaba D.O., Speers C.H., et al. Immunohistochemical detection using the new rabbit monoclonal antibody SP1 of estrogen receptor in breast cancer is superior to mouse monoclonal antibody 1D5 in predicting survival. J Clin Oncol 2006, 24:5637-5644.
26. Gown A.M. Current issues in ER and HER2 testing by IHC in breast cancer. Mod Pathol 2008, 21(suppl 2):S8-S15.
27. Allred D.C., Harvey J.M., Berardo M., et al. Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol 1998, 11:155-168.
28. Barnes D.M., Harris W.H., Smith P., et al. Immunohistochemical determination of oestrogen receptor: comparison of different methods of assessment of staining and correlation with clinical outcome of breast cancer patients. Br J Cancer 1996, 74:1445-1451.
29. Lee H., Douglas-Jones A.G., Morgan J.M., et al. The effect of fixation and processing on the sensitivity of oestrogen receptor assay by immunohistochemistry in breast carcinoma. J Clin Pathol 2002, 55:236-238.
30. Fitzgibbons P.L., Page D.L., Weaver D., et al. Prognostic factors in breast cancer. College of American Pathologists consensus statement 1999. Arch Pathol Lab Med 2000, 124:966-978.
31. McCann J. Better assays needed for hormone receptor status, experts say. J Natl Cancer Inst 2001, 93:579-580.
32. Slamon D.J., Clark G.M., Wong S.G., et al. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987, 235:177-182.
33. Wolf A.C., Hammond M.E., Schwartz J.N., et al. American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor 2 testing in breast cancer. J Clin Oncol 2007, 25:118-145.
34. Gutman S. Regulatory issues in tumor marker development. Semin Oncol 2002, 29:294-300.
35. Paik S., Bryant J., Tan-Chiu E., et al. Real-world performance of HER2 testing-National Surgical Adjuvant Breast and Bowel Project experience. J Natl Cancer Inst 2002, 94:852-854.
36. Roche P.C., Suman V.J., Jenkins R.B., et al. Concordance between local and central laboratory HER2 testing in the breast intergroup trial N9831. J Natl Cancer Inst 2002, 94:855-857.
37. Moeder C.B., Giltnane J.M., Harigopal M., et al. Quantitative justification of the change from 10% to 30% for human epidermal growth factor receptor 2 scoring in the American Society of Clinical Oncology/College of American Pathologists guidelines: tumor heterogeneity in breast cancer and its implications for tissue microarray based assessment of outcome. J Clin Oncol 2007, 25:5418-5425.
38. Jimenez R.E., Wallis T., Tabasczka P., et al. Determination of Her-2/neu status in breast carcinoma: comparative analysis of immunohistochemistry and fluorescent in situ hybridization. Mod Pathol 2000, 13:37-45.
39. Pauletti G., Dandekar S., Rong H., et al. Assessment of methods for tissue-based detection of the HER-2/neu alteration in human breast cancer: a direct comparison of fluorescence in situ hybridization and immunohistochemistry. J Clin Oncol 2000, 18:3651-3664.
40. Press M.F., Hung G., Godolphin W., et al. Sensitivity of HER-2/neu antibodies in archival tissue samples: potential source of error in immunohistochemical studies of oncogene expression. Cancer Res 1994, 54:2771-2777.
41. Cobleigh M.A., Vogel C.L., Tripathy D., et al. Multinational study of the efficacy and safety of humanized anti-HER2 monoclonal antibody in women who have HER2-overexpressing metastatic breast cancer that has progressed after chemotherapy for metastatic disease. J Clin Oncol 1999, 17:2639-2648.
42. Konecny G.E., Thomssen C., Luck H.J., et al. Her-2/neu gene amplification and response to paclitaxel in patients with metastatic breast cancer. J Natl Cancer Inst 2004, 96:1141-1151.
43. Hoff K., Jorgensen J.T., Muller S., et al. Visualization of FISH probes by dual-color chromogenic in situ hybridization. Am J Clin Pathol 2010, 133:205-211.
44. Gokhale S., Rosen D., Sneige N., et al. Assessment of two automated imaging systems in evaluating estrogen receptor status in breast carcinoma. Appl Immunohistochem Mol Morphol 2007, 15:451-455.
45. Perez E.A., Suman V.J., Davidson N.E., et al. HER2 testing by local, central, and reference laboratories in specimens from the North Central Cancer Treatment Group N9831 intergroup adjuvant trial. J Clin Oncol 2006, 24:3032-3038.
46. Sneige N. Utility of cytologic specimens in the evaluation of prognostic and predictive factors of breast cancer: current issues and future directions. Diagn Cytopathol 2004, 30:158-165.
47. Lofgren L., Skoog L., von Schoultz E., et al. Hormone receptor status in breast cancer-a comparison between surgical specimens and fine needle aspiration biopsies. Cytopathology 2003, 14:136-142.
48. Masood S. Estrogen and progesterone receptors in cytology: a comprehensive review. Diagn Cytopathol 1992, 8:475-491.
49. Hodi Z., Chakrabarti J., Lee A.H., et al. The reliability of assessment of oestrogen receptor expression on needle core biopsy specimens of invasive carcinomas of the breast. J Clin Pathol 2007, 60:299-302.
50. Arber D.A. Effect of prolonged formalin fixation on the immunohistochemical reactivity of breast markers. Appl Immunohistochem Mol Morphol 2002, 10:183-186.
51. Olopade OI, Ikpatt JJ, Dignam A, et al: Intrinsic gene expression subtypes correlated with grade and morphometric parameters reveal a high proportion of aggressive basal-like tumors among black women of African ancestry. Paper presented at: ASCO Annual Meeting Proceedings, Vol 22, No 14S, 2004, 9509.
52. Stead L.A., Lash T.L., Sobieraj J.E., et al. Triple-negative breast cancers are increased in black women regardless of age or body mass index. Breast Cancer Res 2009, 11:R18.
53. Millikan R.C., Newman B., Tse C.K., et al. Epidemiology of basal-like breast cancer. Breast Cancer Res Treat 2008, 109:123-139.
54. Anders C., Carey L.A. Understanding and treating triple-negative breast cancer. Oncology 2008, 22:1233-1239.
55. Smid M., Wang Y., Zhang Y., et al. Subtypes of breast cancer show preferential site of relapse. Cancer Res 2008, 68:3108-3114.
56. Freedman G.M., Anderson P.R., Li T., et al. Locoregional recurrence of triple-negative breast cancer after breast-conserving surgery and radiation. Cancer 2009, 115:946-951.
57. Nguyen P.L., Taghian A.G., Katz M.S., et al. Breast cancer subtype approximated by estrogen receptor, progesterone receptor, and HER-2 is associated with local and distant recurrence after breast-conserving therapy. J Clin Oncol 2008, 26:2373-2378.
58. Kassam F., Enright K., Dent R., et al. Survival outcomes for patients with metastatic triple-negative breast cancer: implications for clinical practice and trial design. Clin Breast Cancer 2009, 9:29-33.
59. Pestalozzi B.C., Zahrieh D., Price K.N., et al. Identifying breast cancer patients at risk for central nervous system (CNS) metastases in trials of the International Breast Cancer Study Group (IBCSG). Ann Oncol 2006, 17:935-944.
60. Tham Y.L., Sexton K., Kramer R., et al. Primary breast cancer phenotypes associated with propensity for central nervous system metastases. Cancer 2006, 107:696-704.
61. Dawood S., Broglio K., Esteva F.J., et al. Survival among women with triple receptor-negative breast cancer and brain metastases. Ann Oncol 2009, 20:621-627.
62. Bocker W., Bier B., Freytag G., et al. An immunohistochemical study of the breast using antibodies to basal and luminal keratins, alpha-smooth muscle actin, vimentin, collagen IV and laminin. Part I: Normal breast and benign proliferative lesions. Virchows Arch A Pathol Anat Histopathol 1992, 421:315-322.
63. Putti T.C., El-Rehim D.M., Rakha E.A., et al. Estrogen receptor-negative breast carcinomas: a review of morphology and immunophenotypical analysis. Mod Pathol 2005, 18:26-35.
64. Goffin J.R., Straume O., Chappuis P.O., et al. Glomeruloid microvascular proliferation is associated with p53 expression, germline BRCA1 mutations and an adverse outcome following breast cancer. Br J Cancer 2003, 89:1031-1034.
65. +) phenotype of BRCA1-related breast cancer. Cancer Res 2004, 64:830-835.
66. Kennedy R.D., Quinn J.E., Mullan P.B., et al. The role of BRCA1 in cellular response to chemotherapy. J Natl Cancer Inst 2004, 96:1659-1668.
67. Turner N.C., Reis-Filho J.S., Russell A.M., et al. BRCA1 dysfunction in sporadic basal-like breast cancer. Oncogene 2007, 26:2126-2132.
68. Sorlie T., Tibshirani R., Parker J., et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A 2003, 100:8418-8423.
69. Foulkes W.D., Stefansson I.M., Chappuis P.O., et al. Germline BRCA1 mutations and a basal epithelial phenotype in breast cancer. J Natl Cancer Inst 2003, 95:1482-1485.
70. Elledge R.M., Allred D.C. Prognostic and predictive value of p53 and p21 in breast cancer. Breast Cancer Res Treat 1998, 52:79-98.
71. Rudolph P., Olsson H., Bonatz G., et al. Correlation between p53, c-erbB-2, and topoisomerase II alpha expression, DNA ploidy, hormonal receptor status and proliferation in 356 node-negative breast carcinomas: prognostic implications. J Pathol 1999, 187:207-216.
72. Yang W.T., Dryden M., Broglio K., et al. Mammographic features of triple receptor-negative primary breast cancers in young premenopausal women. Breast Cancer Res Treat 2008, 111:405-410.
73. Dogan B.E., Gonzalez-Angulo A.M., Gilcrease M., et al. Multimodality imaging of triple receptor-negative tumors with mammography, ultrasound, and MRI. AJR Am J Roentgenol 2010, 194:1160-1166.
74. Ko E.S., Lee B.H., Kim H.A., et al. Triple-negative breast cancer: correlation between imaging and pathological findings. Eur Radiol 2010, 20:1111-1117.
75. Ma H., Luo J., Press M.F., et al. Is there a difference in the association between percent mammographic density and subtypes of breast cancer?. Luminal A and triple-negative breast cancer. Cancer Epidemiol Biomarkers Prev 2009, 18:479-485.
76. Whitman G.J., Strom E.A. Workup and staging of locally advanced breast cancer. Semin Radiat Oncol 2009, 19:211-221.
77. Zhang Y.J., Oh J.L., Whitman G.J., et al. Clinically apparent internal mammary nodal metastasis in patients with advanced breast cancer: incidence and local control. Int J Radiat Oncol Biol Phys 2010, 77:1113-1119.
78. Khan A., Sabel M.S., Nees A., et al. Comprehensive axillary evaluation in neoadjuvant chemotherapy patients with ultrasonography and sentinel lymph node biopsy. Ann Surg Oncol 2005, 12:697-704.
79. Swinson C., Ravichandran D., Nayagam M., et al. Ultrasound and fine needle aspiration cytology of the axilla in the pre-operative identification of axillary nodal involvement in breast cancer. Eur J Surg Oncol 2009, 35:1152-1157.
80. Krishnamurthy S. Current applications and future prospects of fine-needle aspiration biopsy of locoregional lymph nodes in the management of breast cancer. Cancer Cytopathol 2009, 117:451-462.
81. ACR BI-RADS. ACR Breast Imaging Reporting and Data System, Breast Imaging Atlas 2003, American College of Radiology (ACR), American College of Radiology, Reston, VA. (ed 4).
82. Chen J.H., Agrawal G., Feig B., et al. Triple-negative breast cancer: MRI features in 29 patients. Ann Oncol 2007, 18:2042-2043.
83. Uematsu T., Kasami M., Yuen S. Triple-negative breast cancer: correlation between MR imaging and pathologic findings. Radiology 2009, 250:638-647.
84. Chen J.H., Mehta R.S., Carpenter P.M., et al. Magnetic resonance imaging in predicting pathological response of triple negative breast cancer following neoadjuvant chemotherapy. J Clin Oncol 2007, 25:5667-5669.
85. Basu S., Chen W., Tchou J., et al. Comparison of triple-negative and estrogen receptor-positive/progesterone receptor-positive/HER2-negative breast carcinoma using quantitative fluorine-18 fluorodeoxyglucose/positron emission tomography imaging parameters. A potentially useful method for disease characterization. Cancer 2008, 112:995-1000.
86. Tchou J., Sonnad S.S., Bergey M.R., et al. Degree of tumor FDG uptake correlates with proliferation index in triple negative breast cancer. Mol Imaging Biol 2009 December 12, (Epub ahead of print).
87. Hama Y., Nakagawa K. Early distant relapse in early stage triple-negative breast cancer: usefulness of FDG-PET for diagnosis of distant metastases. Breast Cancer 2010 January 16, (Epub ahead of print).
88. Rouzier R., Perou C.M., Symmans W.F., et al. Breast cancer molecular subtypes respond differently to preoperative chemotherapy. Clin Cancer Res 2005, 11:5678-5685.
89. Liedtke C., Mazouni C., Hess K.R., et al. Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer. J Clin Oncol 2008, 26:1275-1281.