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Journal of Clinical Oncology, Vol 17, Issue 2 (February), 1999: 460
© 1999 American Society for Clinical Oncology

Clinical Course of Breast Cancer Patients With Complete Pathologic Primary Tumor and Axillary Lymph Node Response to Doxorubicin-Based Neoadjuvant Chemotherapy

Henry M. Kuerer, Lisa A. Newman, Terry L. Smith, Fred C. Ames, Kelly K. Hunt, Kapil Dhingra, Richard L. Theriault, Gurpreet Singh, Susan M. Binkley, Nour Sneige, Thomas A. Buchholz, Merrick I. Ross, Marsha D. McNeese, Aman U. Buzdar, Gabriel N. Hortobagyi, S. Eva Singletary

From the Departments of Surgical Oncology, Biomathematics, Breast Medical Oncology, Pathology, and Radiation Oncology, University of Texas M.D. Anderson Cancer Center, Houston, TX.

Address reprint requests to S. Eva Singletary, MD, Department of Surgical Oncology, Box 106, University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Blvd, Houston, TX 77030; email esinglet{at}notes.mdacc.tmc.edu

PURPOSE: To assess patient and tumor characteristics associated with a complete pathologic response (pCR) in both the breast and axillary lymph node specimens and the outcome of patients found to have a pCR after neoadjuvant chemotherapy for locally advanced breast cancer (LABC).

PATIENTS AND METHODS: Three hundred seventy-two LABC patients received treatment in two prospective neoadjuvant trials using four cycles of doxorubicin-containing chemotherapy. Patients had a total mastectomy with axillary dissection or segmental mastectomy and axillary dissection followed by four or more cycles of additional chemotherapy. Patients then received irradiation treatment of the chest-wall or breast and regional lymphatics. Median follow-up was 58 months (range, 8 to 99 months).

RESULTS: The initial nodal status, age, and stage distribution of patients with a pCR were not significantly different from those of patients with less than a pCR (P > .05). Patients with a pCR had initial tumors that were more likely to be estrogen receptor (ER)–negative (P < .01), and anaplastic (P = .01) but of smaller size (P < .01) than those of patients with less than a pCR. Upon multivariate analysis, the effects of ER status and nuclear grade were independent of initial tumor size. Sixteen percent of the patients in this study (n = 60) had a pathologic complete primary tumor response. Twelve percent of patients (n = 43) had no microscopic evidence of invasive cancer in their breast and axillary specimens. A pathologic complete primary tumor response was predictive of a complete axillary lymph node response (P < .01). The 5-year overall and disease-free survival rates were significantly higher in the group who had a pCR (89% and 87%, respectively) than in the group who had less than a pCR (64% and 58%, respectively; P < .01).

CONCLUSION: Neoadjuvant chemotherapy has the capacity to completely clear the breast and axillary lymph nodes of invasive tumor before surgery. Patients with LABC who have a pCR in the breast and axillary nodes have a significantly improved disease-free survival rate. However, a pCR does not entirely eliminate recurrence. Further efforts should focus on elucidating the molecular mechanisms associated with this response.

Presented at the American Society of Clinical Oncology Annual Meeting, May 19, 1998.

H.M.K. is a recipient of the 1998 American Society of Clinical Oncology Merit Award.


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Neoadjuvant vinorelbine/epirubicin (VE) versus standard adriamycin/cyclophosphamide (AC) in operable breast cancer: analysis of response and tolerability in a randomised phase III trial (TOPIC 2)
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A. M. Gonzalez-Angulo, P. Morandi, and M. Cristofanilli
Inflammatory Breast Cancer and High-Dose Chemotherapy: Back to the Past
J. Clin. Oncol., June 1, 2005; 23(16): 3859 - 3860.
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A. U. Buzdar, N. K. Ibrahim, D. Francis, D. J. Booser, E. S. Thomas, R. L. Theriault, L. Pusztai, M. C. Green, B. K. Arun, S. H. Giordano, et al.
Significantly Higher Pathologic Complete Remission Rate After Neoadjuvant Therapy With Trastuzumab, Paclitaxel, and Epirubicin Chemotherapy: Results of a Randomized Trial in Human Epidermal Growth Factor Receptor 2-Positive Operable Breast Cancer
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S. C. Partridge, J. E. Gibbs, Y. Lu, L. J. Esserman, D. Tripathy, D. S. Wolverton, H. S. Rugo, E. S. Hwang, C. A. Ewing, and N. M. Hylton
MRI Measurements of Breast Tumor Volume Predict Response to Neoadjuvant Chemotherapy and Recurrence-Free Survival
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J. Hannemann, H. M. Oosterkamp, C. A.J. Bosch, A. Velds, L. F.A. Wessels, C. Loo, E. J. Rutgers, S. Rodenhuis, and M. J. van de Vijver
Changes in Gene Expression Associated With Response to Neoadjuvant Chemotherapy in Breast Cancer
J. Clin. Oncol., May 20, 2005; 23(15): 3331 - 3342.
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T.R. J. Evans, A. Yellowlees, E. Foster, H. Earl, D. A. Cameron, A. W. Hutcheon, R. E. Coleman, T. Perren, C. J. Gallagher, M. Quigley, et al.
Phase III Randomized Trial of Doxorubicin and Docetaxel Versus Doxorubicin and Cyclophosphamide As Primary Medical Therapy in Women With Breast Cancer: An Anglo-Celtic Cooperative Oncology Group Study
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G. von Minckwitz, G. Raab, A. Caputo, M. Schutte, J. Hilfrich, J. U. Blohmer, B. Gerber, S. D. Costa, E. Merkle, H. Eidtmann, et al.
Doxorubicin With Cyclophosphamide Followed by Docetaxel Every 21 Days Compared With Doxorubicin and Docetaxel Every 14 Days As Preoperative Treatment in Operable Breast Cancer: The GEPARDUO Study of the German Breast Group
J. Clin. Oncol., April 20, 2005; 23(12): 2676 - 2685.
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M. Panades, I. A. Olivotto, C. H. Speers, T. Shenkier, T. A. Olivotto, L. Weir, S. J. Allan, and P. T. Truong
Evolving Treatment Strategies for Inflammatory Breast Cancer: A Population-Based Survival Analysis
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A. G. Taghian, R. Abi-Raad, S. I. Assaad, A. Casty, M. Ancukiewicz, E. Yeh, P. Molokhia, K. Attia, T. Sullivan, I. Kuter, et al.
Paclitaxel Decreases the Interstitial Fluid Pressure and Improves Oxygenation in Breast Cancers in Patients Treated With Neoadjuvant Chemotherapy: Clinical Implications
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M. Koomen, E. D. Pisano, C. Kuzmiak, D. Pavic, and R. McLelland
Future Directions in Breast Imaging
J. Clin. Oncol., March 10, 2005; 23(8): 1674 - 1677.
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A. Hamilton and G. Hortobagyi
Chemotherapy: What Progress in the Last 5 Years?
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M. Cristofanilli, A. Gonzalez-Angulo, N. Sneige, S.-W. Kau, K. Broglio, R. L. Theriault, V. Valero, A. U. Buzdar, H. Kuerer, T. A. Buccholz, et al.
Invasive Lobular Carcinoma Classic Type: Response to Primary Chemotherapy and Survival Outcomes
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V. Dieras, P. Fumoleau, G. Romieu, M. Tubiana-Hulin, M. Namer, L. Mauriac, J.-P. Guastalla, E. Pujade-Lauraine, P. Kerbrat, P. Maillart, et al.
Randomized Parallel Study of Doxorubicin Plus Paclitaxel and Doxorubicin Plus Cyclophosphamide As Neoadjuvant Treatment of Patients With Breast Cancer
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M. S. Mano and A. Awada
Primary chemotherapy for breast cancer: the evidence and the future
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M. Ayers, W.F. Symmans, J. Stec, A.I. Damokosh, E. Clark, K. Hess, M. Lecocke, J. Metivier, D. Booser, N. Ibrahim, et al.
Gene Expression Profiles Predict Complete Pathologic Response to Neoadjuvant Paclitaxel and Fluorouracil, Doxorubicin, and Cyclophosphamide Chemotherapy in Breast Cancer
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E. Thomas, F. A. Holmes, T. L. Smith, A. U. Buzdar, D. K. Frye, G. Fraschini, S. E. Singletary, R. L. Theriault, M. D. McNeese, F. Ames, et al.
The Use of Alternate, Non-Cross-Resistant Adjuvant Chemotherapy on the Basis of Pathologic Response to a Neoadjuvant Doxorubicin-Based Regimen in Women With Operable Breast Cancer: Long-Term Results From a Prospective Randomized Trial
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A. M. Chen, F. Meric-Bernstam, K. K. Hunt, H. D. Thames, M. J. Oswald, E. D. Outlaw, E. A. Strom, M. D. McNeese, H. M. Kuerer, M. I. Ross, et al.
Breast Conservation After Neoadjuvant Chemotherapy: The M.D. Anderson Cancer Center Experience
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L. G. Estevez and W. J. Gradishar
Evidence-Based Use of Neoadjuvant Taxane in Operable and Inoperable Breast Cancer
Clin. Cancer Res., May 15, 2004; 10(10): 3249 - 3261.
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V. Stearns and N. E. Davidson
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T. Shenkier, L. Weir, M. Levine, I. Olivotto, T. Whelan, and L. Reyno
Clinical practice guidelines for the care and treatment of breast cancer: 15. Treatment for women with stage III or locally advanced breast cancer
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M. Cristofanilli, E. S. Singletary, and G. N. Hortobagyi
Inflammatory Breast Carcinoma: The Sphinx of Breast Cancer Research
J. Clin. Oncol., January 15, 2004; 22(2): 381 - 383.
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S. H. Giordano
Update on Locally Advanced Breast Cancer
Oncologist, December 1, 2003; 8(6): 521 - 530.
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H. D. Bear, S. Anderson, A. Brown, R. Smith, E. P. Mamounas, B. Fisher, R. Margolese, H. Theoret, A. Soran, D. L. Wickerham, et al.
The Effect on Tumor Response of Adding Sequential Preoperative Docetaxel to Preoperative Doxorubicin and Cyclophosphamide: Preliminary Results From National Surgical Adjuvant Breast and Bowel Project Protocol B-27
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International Expert Panel on the Use of Primary (Preoperative) Systemic Treatment of Operable Breast Cancer: Review and Recommendations
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S. C. Formenti, M. Volm, K. A. Skinner, D. Spicer, D. Cohen, E. Perez, A. C. Bettini, S. Groshen, C. Gee, B. Florentine, et al.
Preoperative Twice-Weekly Paclitaxel With Concurrent Radiation Therapy Followed by Surgery and Postoperative Doxorubicin-Based Chemotherapy in Locally Advanced Breast Cancer: A Phase I/II Trial
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E. Baldini, G. Gardin, P. G. Giannessi, G. Evangelista, M. Roncella, T. Prochilo, P. Collecchi, R. Rosso, R. Lionetto, P. Bruzzi, et al.
Accelerated versus standard cyclophosphamide, epirubicin and 5-fluorouracil or cyclophosphamide, methotrexate and 5-fluorouracil: a randomized phase III trial in locally advanced breast cancer
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H. J. Burstein, L. N. Harris, R. Gelman, S. C. Lester, R. A. Nunes, C. M. Kaelin, L. M. Parker, L. W. Ellisen, I. Kuter, M. A. Gadd, et al.
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V. Stearns, B. Singh, T. Tsangaris, J. G. Crawford, A. Novielli, M. J. Ellis, C. Isaacs, M. Pennanen, C. Tibery, A. Farhad, et al.
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P O Chappuis, J Goffin, N Wong, C Perret, P Ghadirian, P N Tonin, and W D Foulkes
A significant response to neoadjuvant chemotherapy in BRCA1/2 related breast cancer
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C. Monnerat, S. Faivre, S. Temam, J. Bourhis, and E. Raymond
End points for new agents in induction chemotherapy for locally advanced head and neck cancers
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G. Bonadonna, M. Zambetti, C. Bumma, M. Donadio, A. Bolognesi, G. Robustelli della Cuna, G. Ambrosini, G. Lelli, M. Mansutti, P. Verderio, et al.
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A. C. Wolff and N. E. Davidson
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Oncologist, June 1, 2002; 7(3): 239 - 245.
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J. G. Schrama, I. F. Faneyte, J. H. Schornagel, J. W. Baars, J. L. Peterse, M. J. van de Vijver, O. Dalesio, H. van Tinteren, E. J. T. Rutgers, D. J. Richel, et al.
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I. C. Smith, S. D. Heys, A. W. Hutcheon, I. D. Miller, S. Payne, F. J. Gilbert, A. K. Ah-See, O. Eremin, L. G. Walker, T. K. Sarkar, et al.
Neoadjuvant Chemotherapy in Breast Cancer: Significantly Enhanced Response With Docetaxel
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National Institutes of Health Consensus Development Conference Statement: Adjuvant Therapy for Breast Cancer, November 1-3, 2000
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J. A. van der Hage, C. J.H. van de Velde, J.-P. Julien, M. Tubiana-Hulin, C. Vandervelden, and L. Duchateau
Preoperative Chemotherapy in Primary Operable Breast Cancer: Results From the European Organization for Research and Treatment of Cancer Trial 10902
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S. Demaria, M. D. Volm, R. L. Shapiro, H. T. Yee, R. Oratz, S. C. Formenti, F. Muggia, and W. F. Symmans
Development of Tumor-infiltrating Lymphocytes in Breast Cancer after Neoadjuvant Paclitaxel Chemotherapy
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