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Originally published as JCO Early Release 10.1200/JCO.2003.09.081 on February 13 2003

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Journal of Clinical Oncology, Vol 21, Issue 8 (April), 2003: 1431-1439
© 2003 American Society for Clinical Oncology

Randomized Trial of Dose-Dense Versus Conventionally Scheduled and Sequential Versus Concurrent Combination Chemotherapy as Postoperative Adjuvant Treatment of Node-Positive Primary Breast Cancer: First Report of Intergroup Trial C9741/Cancer and Leukemia Group B Trial 9741

Marc L. Citron, Donald A. Berry, Constance Cirrincione, Clifford Hudis, Eric P. Winer, William J. Gradishar, Nancy E. Davidson, Silvana Martino, Robert Livingston, James N. Ingle, Edith A. Perez, John Carpenter, David Hurd, James F. Holland, Barbara L. Smith, Carolyn I. Sartor, Eleanor H. Leung, Jeffrey Abrams, Richard L. Schilsky, Hyman B. Muss, Larry Norton

From the ProHEALTH Care Associates, LLP, Lake Success; and Memorial Sloan-Kettering Cancer Center and Mt Sinai School of Medicine, New York, NY; University of Texas M.D. Anderson Cancer Center, Houston, TX; Cancer and Leukemia Group B Statistical Office and Data Operations, Durham; Comprehensive Cancer Center of Wake Forest University, Winston-Salem; and University of North Carolina School of Medicine, Chapel Hill, NC; Dana-Farber Cancer Institute, Brigham and Women’s Hospital, and Massachusetts General Hospital, Boston, MA; Northwestern University and Cancer and Leukemia Group B Central Office, Chicago, IL; Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins, Baltimore, and National Cancer Institute, Bethesda, MD; John Wayne Cancer Institute, Santa Monica, CA; University of Washington, Seattle, WA; Mayo Clinic, Rochester, MN; Mayo Clinic, Jacksonville, FL; University of Alabama at Birmingham, Birmingham, AL; and University of Vermont, Burlington, VT.

Address reprint requests to Marc L. Citron, MD, ProHEALTH Care Associates, LLP, 2800 Marcus Ave, Lake Success, NY 11042; email: mcitron{at}prohealthcare.com.

Purpose: Using a 2 x 2 factorial design, we studied the adjuvant chemotherapy of women with axillary node–positive breast cancer to compare sequential doxorubicin (A), paclitaxel (T), and cyclophosphamide (C) with concurrent doxorubicin and cyclophosphamide (AC) followed by paclitaxel (T) for disease-free (DFS) and overall survival (OS); to determine whether the dose density of the agents improves DFS and OS; and to compare toxicities.

Patients and Methods: A total of 2,005 female patients were randomly assigned to receive one of the following regimens: (I) sequential A x 4 (doses) -> T x 4 -> C x 4 with doses every 3 weeks, (II) sequential A x 4 -> T x 4 -> C x 4 every 2 weeks with filgrastim, (III) concurrent AC x 4 -> T x 4 every 3 weeks, or (IV) concurrent AC x 4 -> T x 4 every 2 weeks with filgrastim.

Results: A protocol-specified analysis was performed at a median follow-up of 36 months: 315 patients had experienced relapse or died, compared with 515 expected treatment failures. Dose-dense treatment improved the primary end point, DFS (risk ratio [RR] = 0.74; P = .010), and OS (RR = 0.69; P = .013). Four-year DFS was 82% for the dose-dense regimens and 75% for the others. There was no difference in either DFS or OS between the concurrent and sequential schedules. There was no interaction between density and sequence. Severe neutropenia was less frequent in patients who received the dose-dense regimens.

Conclusion: Dose density improves clinical outcomes significantly, despite the lower than expected number of events at this time. Sequential chemotherapy is as effective as concurrent chemotherapy.


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Related Correspondence

  • Improved Outcome With Dose-Dense Chemotherapy
    Bruce Keith, Rob Hall, and Aaron Scholnik
    JCO 2004 22: 749 [Full Text]
  • Dose-Dense Chemotherapy As Adjuvant Treatment for Breast Cancer
    Carl D. Atkins
    JCO 2004 22: 749-780 [Full Text]
  • Dose Density by Any Other Name
    William Hryniuk, Joseph Ragaz, and William Peters
    JCO 2004 22: 750-751 [Full Text]

Related Reply

  • In Reply:
    Marc L. Citron, Donald A. Berry, Constance Cirrincione, Clifford Hudis, Larry Norton, Eric P. Winer, William J. Gradishar, Nancy E. Davidson, Silvana Martino, Robert Livingston, James N. Ingle, John Carpenter, David Hurd, James F. Holland, Barbara Smith, Carolyn I. Sartor, Eleanor H. Leung, Jeffrey Abrams, Richard L Schilsky, and Hyman B. Muss
    JCO 2004 22: 751-753 [Full Text]


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D. Hershman, A. I. Neugut, J. S. Jacobson, J. Wang, W.-Y. Tsai, R. McBride, C. L. Bennett, and V. R. Grann
Acute Myeloid Leukemia or Myelodysplastic Syndrome Following Use of Granulocyte Colony-Stimulating Factors During Breast Cancer Adjuvant Chemotherapy
J Natl Cancer Inst, February 7, 2007; 99(3): 196 - 205.
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I. J. Lewis, M. A. Nooij, J. Whelan, M. R. Sydes, R. Grimer, P. C. W. Hogendoorn, M. A. Memon, S. Weeden, B. M. Uscinska, M. van Glabbeke, et al.
Improvement in Histologic Response But Not Survival in Osteosarcoma Patients Treated With Intensified Chemotherapy: A Randomized Phase III Trial of the European Osteosarcoma Intergroup
J Natl Cancer Inst, January 17, 2007; 99(2): 112 - 128.
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H. Oettle, S. Post, P. Neuhaus, K. Gellert, J. Langrehr, K. Ridwelski, H. Schramm, J. Fahlke, C. Zuelke, C. Burkart, et al.
Adjuvant Chemotherapy With Gemcitabine vs Observation in Patients Undergoing Curative-Intent Resection of Pancreatic Cancer: A Randomized Controlled Trial
JAMA, January 17, 2007; 297(3): 267 - 277.
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 Cancer Res.Home page
A. A. Kamat, T. J. Kim, C. N. Landen Jr., C. Lu, L. Y. Han, Y. G. Lin, W. M. Merritt, P. H. Thaker, D. M. Gershenson, F. Z. Bischoff, et al.
Metronomic Chemotherapy Enhances the Efficacy of Antivascular Therapy in Ovarian Cancer
Cancer Res., January 1, 2007; 67(1): 281 - 288.
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P Piedbois, D Serin, F Priou, P Laplaige, S Greget, E Angellier, E Teissier, J-F Berdah, M Fabbro, B Valenza, et al.
Dose-dense adjuvant chemotherapy in node-positive breast cancer: docetaxel followed by epirubicin/cyclophosphamide (T/EC), or the reverse sequence (EC/T), every 2 weeks, versus docetaxel, epirubicin and cyclophosphamide (TEC) every 3 weeks. AERO B03 randomized phase II study
Ann. Onc., January 1, 2007; 18(1): 52 - 57.
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M. N. Fornier, A. D. Seidman, D. Lake, G. D'Andrea, J. Bromberg, M. Robson, C. Van Poznak, K. S. Panageas, M. Atienza, L. Norton, et al.
Increased Dose Density Is Feasible: A Pilot Study of Adjuvant Epirubicin and Cyclophosphamide followed by Paclitaxel, at 10- or 11-Day Intervals with Filgrastim Support in Women with Breast Cancer
Clin. Cancer Res., January 1, 2007; 13(1): 223 - 227.
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S. M. Tolaney, A. H. Partridge, R. G. Sheib, H. J. Burstein, and E. P. Winer
Pneumocystis Carinii Pneumonia During Dose-Dense Chemotherapy for Breast Cancer
J. Clin. Oncol., November 20, 2006; 24(33): 5330 - 5331.
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M. N. Levine and T. Whelan
Adjuvant Chemotherapy for Breast Cancer -- 30 Years Later
N. Engl. J. Med., November 2, 2006; 355(18): 1920 - 1922.
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M. Gore, A. du Bois, and I. Vergote
Intraperitoneal Chemotherapy in Ovarian Cancer Remains Experimental
J. Clin. Oncol., October 1, 2006; 24(28): 4528 - 4530.
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E Bria, M Di Maio, C Nistico, F Cuppone, E Terzoli, F Cognetti, and D Giannarelli
Factorial design for randomized clinical trials
Ann. Onc., October 1, 2006; 17(10): 1607 - 1608.
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G. Ferretti, P. Papaldo, F. Cognetti, D. C. Dale, P. S. Rosenberg, B. P. Alter, and K. Kaushansky
Lineage-specific hematopoietic growth factors.
N. Engl. J. Med., August 3, 2006; 355(5): 526 - 527.
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T. J. Smith, J. Khatcheressian, G. H. Lyman, H. Ozer, J. O. Armitage, L. Balducci, C. L. Bennett, S. B. Cantor, J. Crawford, S. J. Cross, et al.
2006 Update of Recommendations for the Use of White Blood Cell Growth Factors: An Evidence-Based Clinical Practice Guideline
J. Clin. Oncol., July 1, 2006; 24(19): 3187 - 3205.
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P. Papaldo, G. Ferretti, S. Di Cosimo, D. Giannarelli, P. Marolla, M. Lopez, E. Cortesi, M. Antimi, E. Terzoli, P. Carlini, et al.
Does Granulocyte Colony-Stimulating Factor Worsen Anemia in Early Breast Cancer Patients Treated With Epirubicin and Cyclophosphamide?
J. Clin. Oncol., July 1, 2006; 24(19): 3048 - 3055.
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J. A. Sparano, S. Moulder, A. Kazi, L. Vahdat, T. Li, C. Pellegrino, P. Munster, M. Malafa, D. Lee, S. Hoschander, et al.
Targeted Inhibition of Farnesyltransferase in Locally Advanced Breast Cancer: A Phase I and II Trial of Tipifarnib Plus Dose-Dense Doxorubicin and Cyclophosphamide
J. Clin. Oncol., July 1, 2006; 24(19): 3013 - 3018.
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C. Dang and C. Hudis
Can Granulocyte-Colony Stimulating Factor Worsen Anemia?
J. Clin. Oncol., July 1, 2006; 24(19): 2985 - 2986.
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E. B. Elkin, A. Hurria, N. Mitra, D. Schrag, and K. S. Panageas
Adjuvant Chemotherapy and Survival in Older Women With Hormone Receptor-Negative Breast Cancer: Assessing Outcome in a Population-Based, Observational Cohort
J. Clin. Oncol., June 20, 2006; 24(18): 2757 - 2764.
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 JCOHome page
M. H. Malogolowkin, H. Katzenstein, M. D. Krailo, Z. Chen, L. Bowman, M. Reynolds, M. Finegold, B. Greffe, J. Rowland, K. Newman, et al.
Intensified Platinum Therapy Is an Ineffective Strategy for Improving Outcome in Pediatric Patients With Advanced Hepatoblastoma
J. Clin. Oncol., June 20, 2006; 24(18): 2879 - 2884.
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 The OncologistHome page
I. Sachelarie, M. L. Grossbard, M. Chadha, S. Feldman, M. Ghesani, and R. H. Blum
Primary Systemic Therapy of Breast Cancer
Oncologist, June 1, 2006; 11(6): 574 - 589.
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 ScienceHome page
R. S. Kerbel
Antiangiogenic therapy: a universal chemosensitization strategy for cancer?
Science, May 26, 2006; 312(5777): 1171 - 1175.
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A. C. Wolff, R. J. Jones, N. E. Davidson, S. C. Jeter, and V. Stearns
Myeloid Toxicity in Breast Cancer Patients Receiving Adjuvant Chemotherapy With Pegfilgrastim Support
J. Clin. Oncol., May 20, 2006; 24(15): 2392 - 2394.
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H. D. Bear, S. Anderson, R. E. Smith, C. E. Geyer Jr, E. P. Mamounas, B. Fisher, A. M. Brown, A. Robidoux, R. Margolese, M. S. Kahlenberg, et al.
Sequential Preoperative or Postoperative Docetaxel Added to Preoperative Doxorubicin Plus Cyclophosphamide for Operable Breast Cancer: National Surgical Adjuvant Breast and Bowel Project Protocol B-27
J. Clin. Oncol., May 1, 2006; 24(13): 2019 - 2027.
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J. P. Monk, G. Phillips, R. Waite, J. Kuhn, L. J. Schaaf, G. A. Otterson, D. Guttridge, C. Rhoades, M. Shah, T. Criswell, et al.
Assessment of Tumor Necrosis Factor Alpha Blockade As an Intervention to Improve Tolerability of Dose-Intensive Chemotherapy in Cancer Patients
J. Clin. Oncol., April 20, 2006; 24(12): 1852 - 1859.
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D. A. Berry, C. Cirrincione, I. C. Henderson, M. L. Citron, D. R. Budman, L. J. Goldstein, S. Martino, E. A. Perez, H. B. Muss, L. Norton, et al.
Estrogen-Receptor Status and Outcomes of Modern Chemotherapy for Patients With Node-Positive Breast Cancer
JAMA, April 12, 2006; 295(14): 1658 - 1667.
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A. M. Brade and I. F. Tannock
Scheduling of Radiation and Chemotherapy for Limited-Stage Small-Cell Lung Cancer: Repopulation As a Cause of Treatment Failure?
J. Clin. Oncol., March 1, 2006; 24(7): 1020 - 1022.
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S. Burdette-Radoux and H. B. Muss
Adjuvant chemotherapy in the elderly: whom to treat, what regimen?
Oncologist, March 1, 2006; 11(3): 234 - 242.
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 The OncologistHome page
M. Colozza, E. de Azambuja, F. Cardoso, C. Bernard, and M. J. Piccart
Breast cancer: achievements in adjuvant systemic therapies in the pre-genomic era.
Oncologist, February 1, 2006; 11(2): 111 - 125.
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I. Smith and S. Chua
Medical treatment of early breast cancer. III: chemotherapy
BMJ, January 21, 2006; 332(7534): 161 - 162.
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International Breast Cancer Study Group
Multicycle Dose-Intensive Chemotherapy for Women With High-Risk Primary Breast Cancer: Results of International Breast Cancer Study Group Trial 15-95
J. Clin. Oncol., January 20, 2006; 24(3): 370 - 378.
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N. U. Lin, R. Gelman, and E. P. Winer
Dose Density in Breast Cancer: A Simple Message?
J Natl Cancer Inst, December 7, 2005; 97(23): 1712 - 1714.
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M. Venturini, L. Del Mastro, E. Aitini, E. Baldini, C. Caroti, A. Contu, F. Testore, F. Brema, P. Pronzato, G. Cavazzini, et al.
Dose-Dense Adjuvant Chemotherapy in Early Breast Cancer Patients: Results From a Randomized Trial
J Natl Cancer Inst, December 7, 2005; 97(23): 1724 - 1733.
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 Evid. Based Med.Home page
T. J Smith and J. Khatcheressian
Review: chemotherapy and hormonal therapy reduce recurrence and mortality at 15 years in early breast cancer
Evid. Based Med., December 1, 2005; 10(6): 169 - 169.
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