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Estrogen Receptor Status by Immunohistochemistry Is Superior to the Ligand-Binding Assay for Predicting Response to Adjuvant Endocrine Therapy in Breast Cancer

From the Department of Pathology, University of Western Australia, Nedlands, Western Australia, Australia; and Division of Medical Oncology and Department of Pathology, University of Texas Health Science Center at San Antonio, San Antonio, TX.

Address reprint requests to D. Craig Allred, MD, University of Texas Health Science Center at San Antonio, Department of Pathology, San Antonio, TX 78284-7750; email allred{at}uthscsa.edu

PURPOSE: Immunohistochemistry (IHC) is a newer technique for assessing the estrogen receptor (ER) status of breast cancers, with the potential to overcome many of the shortcomings associated with the traditional ligand-binding assay (LBA). The purpose of this study was to evaluate the ability of ER status determination by IHC, compared with LBA, to predict clinical outcome—especially response to adjuvant endocrine therapy—in a large number of patients with long-term clinical follow-up.

PATIENTS AND METHODS: ER status was evaluated in 1,982 primary breast cancers by IHC on formalin-fixed paraffin-embedded tissue sections, using antibody 6F11 and standard methodology. Slides were scored on a scale representing the estimated proportion and intensity of positive-staining tumor cells (range, 0 to 8). Results were compared with ER values obtained by the LBA in the same tumors and to clinical outcome.

RESULTS: An IHC score of greater than 2 (corresponding to as few as 1% to 10% weakly positive cells) was used to define ER positivity on the basis of a univariate cut-point analysis of all possible scores and disease-free survival (DFS) in patients receiving any adjuvant endocrine therapy. Using this definition, 71% of all tumors were determined to be ER-positive by IHC, and the level of agreement with the LBA was 86%. In multivariate analyses of patients receiving adjuvant endocrine therapy alone, ER status determined by IHC was better than that determined by the LBA at predicting improved DFS (hazard ratios/P = 0.474/.0008 and 0.707/.3214, respectively) and equivalent at predicting overall survival (0.379/.0001 and 0.381/.0003, respectively).

CONCLUSION: IHC is superior to the LBA for assessing ER status in primary breast cancer because it is easier, safer, and less expensive, and has an equivalent or better ability to predict response to adjuvant endocrine therapy.

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				M. Dowsett, J. Cuzick, C. Wale, T. Howell, J. Houghton, and M. Baum Retrospective Analysis of Time to Recurrence in the ATAC Trial According to Hormone Receptor Status: An Hypothesis-Generating Study J. Clin. Oncol., October 20, 2005; 23(30): 7512 - 7517. [Abstract] [Full Text] [PDF]

				X. Cui, R. Schiff, G. Arpino, C. K. Osborne, and A. V. Lee Biology of Progesterone Receptor Loss in Breast Cancer and Its Implications for Endocrine Therapy J. Clin. Oncol., October 20, 2005; 23(30): 7721 - 7735. [Abstract] [Full Text] [PDF]

				I. Poola, S. A.W. Fuqua, R. L. De Witty, J. Abraham, J. J. Marshallack, and A. Liu Estrogen Receptor {alpha}-Negative Breast Cancer Tissues Express Significant Levels of Estrogen-Independent Transcription Factors, ER{beta}1 and ER{beta}5: Potential Molecular Targets for Chemoprevention Clin. Cancer Res., October 15, 2005; 11(20): 7579 - 7585. [Abstract] [Full Text] [PDF]

				J. I. Neves, M. D. Begnami, V. Arias, and G. C. Santos Antigen Retrieval Methods and Estrogen Receptor Immunoexpression Using 1D5 Antibody: A Comparative Study International Journal of Surgical Pathology, October 1, 2005; 13(4): 353 - 357. [Abstract] [PDF]

				A. Goldhirsch, J. H. Glick, R. D. Gelber, A. S. Coates, B. Thurlimann, H.-J. Senn, and and Panel Members Meeting Highlights: International Expert Consensus on the Primary Therapy of Early Breast Cancer 2005 Ann. Onc., October 1, 2005; 16(10): 1569 - 1583. [Abstract] [Full Text] [PDF]

				G. B. Mann, V. D. Fahey, F. Feleppa, and M. R. Buchanan Reliance on Hormone Receptor Assays of Surgical Specimens May Compromise Outcome in Patients With Breast Cancer J. Clin. Oncol., August 1, 2005; 23(22): 5148 - 5154. [Abstract] [Full Text] [PDF]

				S. B. Wedam and S. M. Swain Contralateral Breast Cancer: Where Does It All Begin? J. Clin. Oncol., July 20, 2005; 23(21): 4585 - 4587. [Full Text] [PDF]

				H. Kawai, A. Ishii, K. Washiya, T. Konno, H. Kon, C. Yamaya, I. Ono, Y. Minamiya, and J. Ogawa Estrogen Receptor {alpha} and {beta} are Prognostic Factors in Non-Small Cell Lung Cancer Clin. Cancer Res., July 15, 2005; 11(14): 5084 - 5089. [Abstract] [Full Text] [PDF]

				A. K. Witkiewicz, S. Varambally, R. Shen, R. Mehra, M. S. Sabel, D. Ghosh, A. M. Chinnaiyan, M. A. Rubin, and C. G. Kleer {alpha}-Methylacyl-CoA Racemase Protein Expression Is Associated with the Degree of Differentiation in Breast Cancer Using Quantitative Image Analysis Cancer Epidemiol. Biomarkers Prev., June 1, 2005; 14(6): 1418 - 1423. [Abstract] [Full Text] [PDF]

				M. Colleoni, S. Li, R. D. Gelber, A. S. Coates, M. Castiglione-Gertsch, K. N. Price, J. Lindtner, C.-M. Rudenstam, D. Crivellari, J. Collins, et al. Timing of CMF chemotherapy in combination with tamoxifen in postmenopausal women with breast cancer: role of endocrine responsiveness of the tumor Ann. Onc., May 1, 2005; 16(5): 716 - 725. [Abstract] [Full Text] [PDF]

				F. J. Esteva, A. A. Sahin, M. Cristofanilli, K. Coombes, S.-J. Lee, J. Baker, M. Cronin, M. Walker, D. Watson, S. Shak, et al. Prognostic Role of a Multigene Reverse Transcriptase-PCR Assay in Patients with Node-Negative Breast Cancer Not Receiving Adjuvant Systemic Therapy Clin. Cancer Res., May 1, 2005; 11(9): 3315 - 3319. [Abstract] [Full Text] [PDF]

				E. Myers, A. D.K. Hill, G. Kelly, E. W. McDermott, N. J. O'Higgins, Y. Buggy, and L. S. Young Associations and Interactions between Ets-1 and Ets-2 and Coregulatory Proteins, SRC-1, AIB1, and NCoR in Breast Cancer Clin. Cancer Res., March 15, 2005; 11(6): 2111 - 2122. [Abstract] [Full Text] [PDF]

				S. Dellapasqua, M. Colleoni, R. D. Gelber, and A. Goldhirsch Adjuvant Endocrine Therapy for Premenopausal Women With Early Breast Cancer J. Clin. Oncol., March 10, 2005; 23(8): 1736 - 1750. [Full Text] [PDF]

				M. J. Duffy Predictive Markers in Breast and Other Cancers: A Review Clin. Chem., March 1, 2005; 51(3): 494 - 503. [Abstract] [Full Text] [PDF]

				S. A.W. Fuqua, Y. Cui, A. V. Lee, C. K. Osborne, and K. B. Horwitz Insights Into the Role of Progesterone Receptors in Breast Cancer J. Clin. Oncol., February 1, 2005; 23(4): 931 - 932. [Full Text] [PDF]

				P. F. Lebowitz, J. Eng-Wong, B. C. Widemann, F. M. Balis, N. Jayaprakash, C. Chow, G. Clark, S. B. Gantz, D. Venzon, and J. Zujewski A Phase I Trial and Pharmacokinetic Study of Tipifarnib, a Farnesyltransferase Inhibitor, and Tamoxifen in Metastatic Breast Cancer Clin. Cancer Res., February 1, 2005; 11(3): 1247 - 1252. [Abstract] [Full Text] [PDF]

				H. B. Nichols, A. Trentham-Dietz, R. R. Love, J. M. Hampton, P. T. Hoang Anh, D. C. Allred, S. K. Mohsin, and P. A. Newcomb Differences in Breast Cancer Risk Factors by Tumor Marker Subtypes among Premenopausal Vietnamese and Chinese Women Cancer Epidemiol. Biomarkers Prev., January 1, 2005; 14(1): 41 - 47. [Abstract] [Full Text] [PDF]

				Z. Zhang, H. Yamashita, T. Toyama, H. Sugiura, Y. Ando, K. Mita, M. Hamaguchi, M. Kawaguchi, Y. Miura, and H. Iwase ATBF1-A Messenger RNA Expression Is Correlated with Better Prognosis in Breast Cancer Clin. Cancer Res., January 1, 2005; 11(1): 193 - 198. [Abstract] [Full Text] [PDF]

				M. H. Herynk and S. A. W. Fuqua Estrogen Receptor Mutations in Human Disease Endocr. Rev., December 1, 2004; 25(6): 869 - 898. [Abstract] [Full Text] [PDF]

				T. A. Hopp, H. L. Weiss, I. S. Parra, Y. Cui, C. K. Osborne, and S. A. W. Fuqua Low Levels of Estrogen Receptor {beta} Protein Predict Resistance to Tamoxifen Therapy in Breast Cancer Clin. Cancer Res., November 15, 2004; 10(22): 7490 - 7499. [Abstract] [Full Text] [PDF]

				M. Colleoni, N. Rotmensz, G. Peruzzotti, P. Maisonneuve, G. Viale, G. Renne, C. Casadio, P. Veronesi, M. Intra, R. Torrisi, et al. Minimal and small size invasive breast cancer with no axillary lymph node involvement: the need for tailored adjuvant therapies Ann. Onc., November 1, 2004; 15(11): 1633 - 1639. [Abstract] [Full Text] [PDF]

				O. O. Oduwole, Y. Li, V. V. Isomaa, A. Mantyniemi, A. E. Pulkka, Y. Soini, and P. T. Vihko 17{beta}-Hydroxysteroid Dehydrogenase Type 1 Is an Independent Prognostic Marker in Breast Cancer Cancer Res., October 15, 2004; 64(20): 7604 - 7609. [Abstract] [Full Text] [PDF]

				Z. Zhang, H. Yamashita, T. Toyama, H. Sugiura, Y. Omoto, Y. Ando, K. Mita, M. Hamaguchi, S.-i. Hayashi, and H. Iwase HDAC6 Expression Is Correlated with Better Survival in Breast Cancer Clin. Cancer Res., October 15, 2004; 10(20): 6962 - 6968. [Abstract] [Full Text] [PDF]

				F J Fleming, E Myers, G Kelly, T B Crotty, E W McDermott, N J O'Higgins, A D K Hill, and L S Young Expression of SRC-1, AIB1, and PEA3 in HER2 mediated endocrine resistant breast cancer; a predictive role for SRC-1 J. Clin. Pathol., October 1, 2004; 57(10): 1069 - 1074. [Abstract] [Full Text] [PDF]

				O. Modlich, H.-B. Prisack, M. Munnes, W. Audretsch, and H. Bojar Immediate Gene Expression Changes After the First Course of Neoadjuvant Chemotherapy in Patients with Primary Breast Cancer Disease Clin. Cancer Res., October 1, 2004; 10(19): 6418 - 6431. [Abstract] [Full Text] [PDF]