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Originally published as JCO Early Release 10.1200/JCO.2005.06.150 on August 8 2005

Journal of Clinical Oncology, Vol 23, No 25 (September 1), 2005: pp. 5960-5972
© 2005 American Society of Clinical Oncology.
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Maintaining Normal Hemoglobin Levels With Epoetin Alfa in Mainly Nonanemic Patients With Metastatic Breast Cancer Receiving First-Line Chemotherapy: A Survival Study

Brian Leyland-Jones, Vladimir Semiglazov, Marek Pawlicki, Tadeusz Pienkowski, Sergei Tjulandin, George Manikhas, Antoly Makhson, Anton Roth, David Dodwell, Jose Baselga, Mikhail Biakhov, Konstantinas Valuckas, Edouard Voznyi, Xiangyang Liu, Els Vercammen

From the Department of Medical Oncology, McGill University, Montreal, Canada; N.N. Petrov Research Institute of Oncology; City Oncology Dispensary, St Petersburg; Cancer Research Center; Semashko Central Clinical Hospital; Russian Scientific Center of Radiology, Moscow; City Clinical Hospital, Moscow Region, Russia; Klinika Chemioterapii Centrum Onkologii, Krakov; Klinika Nowotworów Sutka Centrum Onkologii Instytut, Warsaw, Poland; Klinika za Tumore, Zagreb, Croatia; Johnson & Johnson Pharmaceutical Research & Development, High Wycombe, Bucks, United Kingdom; Lithuanian Oncology Centre, Vilnius, Lithuania; and Johnson & Johnson Pharmaceutical Research & Development, Raritan, NJ

Address reprint requests to and address for reprints: Brian Leyland-Jones, MD, Department of Oncology, McGill University, 546 Pine Avenue W, Montreal, Quebec, Canada H2W 1S6; e-mail: brian.leyland-jones{at}mcgill.ca

PURPOSE: To evaluate the effect on survival and quality of life of maintaining hemoglobin (Hb) in the range of 12 to 14 g/dL with epoetin alfa versus placebo in women with metastatic breast cancer (MBC) receiving first-line chemotherapy.

PATIENTS AND METHODS: Eligible patients were randomly assigned to receive epoetin alfa 40,000 U once weekly or placebo for 12 months. Study drug was initiated if baseline Hb was ≤ 13 g/dL or when Hb decreased to ≤ 13g/dL during the study. The primary end point was 12-month overall survival (OS).

RESULTS: The study drug administration was stopped early in accordance with a recommendation from the Independent Data Monitoring Committee because of higher mortality in the group treated with epoetin alfa. Enrollment had been completed, with 939 patients enrolled (epoetin alfa, n = 469; placebo, n = 470). Most patients had Hb more than 12 g/dL at baseline (median Hb, 12.8 g/dL) or during the study. From the final analysis, 12-month OS was 70% for epoetin alfa recipients and 76% for placebo recipients (P = .01). Optimal tumor response and time to disease progression were similar between groups. The reason for the difference in mortality between groups could not be determined from additional subsequent analyses involving both study data and chart review.

CONCLUSION: In this trial, the use of epoetin alfa to maintain high Hb targets in women with MBC, most of whom did not have anemia at the start of treatment, was associated with decreased survival. Additional research is required to clarify the potential impact of erythropoietic agents on survival when the Hb target range is 10 to 12 g/dL.

Supported by a research grant from Johnson & Johnson Pharmaceutical Research and Development LLC, Raritan, NJ. B.L.-J. was the principal investigator.

Portions of this study were reported previously in Leyland-Jones B, and the BEST Investigators and Study Group: Breast cancer trial with erythropoietin terminated unexpectedly. Lancet Oncol 4:459-460, 2003.

Authors' disclosures of potential conflicts of interest are found at the end of this article.


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P. Kokhaei, A. O. Abdalla, L. Hansson, E. Mikaelsson, M. Kubbies, A. Haselbeck, H. Jernberg-Wiklund, H. Mellstedt, and A. Osterborg
Expression of Erythropoietin Receptor and In vitro Functional Effects of Epoetins in B-Cell Malignancies
Clin. Cancer Res., June 15, 2007; 13(12): 3536 - 3544.
[Abstract] [Full Text] [PDF]

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 NEJMHome page
F. R. Khuri
Weighing the Hazards of Erythropoiesis Stimulation in Patients with Cancer
N. Engl. J. Med., June 14, 2007; 356(24): 2445 - 2448.
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 JCOHome page
M. Henke, D. Mattern, and F. Pajonk
In Reply
J. Clin. Oncol., May 1, 2007; 25(13): 1815 - 1815.
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 Nephrol Dial TransplantHome page
A. Sturiale, S. Campo, E. Crasci, G. Coppolino, D. Bolignano, G. Grasso, and M. Buemi
Erythropoietin and its lost receptor
Nephrol. Dial. Transplant., May 1, 2007; 22(5): 1484 - 1485.
[Full Text] [PDF]

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 The OncologistHome page
R. Boccia, T. Lillie, D. Tomita, and L. Balducci
The Effectiveness of Darbepoetin Alfa Administered Every 3 Weeks on Hematologic Outcomes and Quality of Life in Older Patients With Chemotherapy-Induced Anemia
Oncologist, May 1, 2007; 12(5): 584 - 593.
[Abstract] [Full Text] [PDF]

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 PhysiologyHome page
P. Sonveaux, I. I. Lobysheva, O. Feron, and T. J. McMahon
Transport and Peripheral Bioactivities of Nitrogen Oxides Carried by Red Blood Cell Hemoglobin: Role in Oxygen Delivery
Physiology, April 1, 2007; 22(2): 97 - 112.
[Abstract] [Full Text] [PDF]

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 Ann OncolHome page
F Bellati, M Pernice, N Manci, I Palaia, F Tomao, C Marchetti, M. Zullo, L Muzii, R Angioli, and P. B. Panici
Hemoglobin variation and blood transfusion rates in patients affected by locally advanced cervical cancer undergoing neo-adjuvant chemotherapy followed by radical surgery: the role of erythropoietic growth factors
Ann. Onc., April 1, 2007; 18(4): 722 - 729.
[Abstract] [Full Text] [PDF]

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 BMJHome page
D. P Steensma
Erythropoiesis stimulating agents
BMJ, March 31, 2007; 334(7595): 648 - 649.
[Full Text] [PDF]

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 JCOHome page
J. R. Wright, Y. C. Ung, J. A. Julian, K. I. Pritchard, T. J. Whelan, C. Smith, B. Szechtman, W. Roa, L. Mulroy, L. Rudinskas, et al.
Randomized, Double-Blind, Placebo-Controlled Trial of Erythropoietin in Non-Small-Cell Lung Cancer With Disease-Related Anemia
J. Clin. Oncol., March 20, 2007; 25(9): 1027 - 1032.
[Abstract] [Full Text] [PDF]

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 JCOHome page
J. Crawford
Erythropoietin: High Profile, High Scrutiny
J. Clin. Oncol., March 20, 2007; 25(9): 1021 - 1023.
[Full Text] [PDF]

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 Ann OncolHome page
S Beslija, J Bonneterre, H Burstein, V Cocquyt, M Gnant, P Goodwin, V Heinemann, J Jassem, W. Kostler, M Krainer, et al.
Second consensus on medical treatment of metastatic breast cancer
Ann. Onc., February 1, 2007; 18(2): 215 - 225.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
R. J. Epstein and T. W. Leung
Reversing Hepatocellular Carcinoma Progression by Using Networked Biological Therapies
Clin. Cancer Res., January 1, 2007; 13(1): 11 - 17.
[Abstract] [Full Text] [PDF]

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 BloodHome page
M. A. Weinreich, I. Lintmaer, L. Wang, H. D. Liggitt, M. A. Harkey, and C. A. Blau
Growth factor receptors as regulators of hematopoiesis
Blood, December 1, 2006; 108(12): 3713 - 3721.
[Abstract] [Full Text] [PDF]

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 JCOHome page
S. Y. Lai and J. R. Grandis
Understanding the Presence and Function of Erythropoietin Receptors on Cancer Cells
J. Clin. Oncol., October 10, 2006; 24(29): 4675 - 4676.
[Full Text] [PDF]

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 JCOHome page
M. Henke, D. Mattern, M. Pepe, C. Bezay, C. Weissenberger, M. Werner, and F. Pajonk
Do Erythropoietin Receptors on Cancer Cells Explain Unexpected Clinical Findings?
J. Clin. Oncol., October 10, 2006; 24(29): 4708 - 4713.
[Abstract] [Full Text] [PDF]

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 BloodHome page
M. Henke, A. Verma, G. Acs, S. Elliott, L. Busse, C. Spahr, and A. M. Sinclair
Erythropoietin receptors on cancer cells: exciting perspectives, difficult to appreciate
Blood, August 1, 2006; 108(3): 1107 - 1109.
[Full Text] [PDF]

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 CirculationHome page
Y.-D. Tang and S. D. Katz
Anemia in Chronic Heart Failure: Prevalence, Etiology, Clinical Correlates, and Treatment Options
Circulation, May 23, 2006; 113(20): 2454 - 2461.
[Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
J. Bohlius, J. Wilson, J. Seidenfeld, M. Piper, G. Schwarzer, J. Sandercock, S. Trelle, O. Weingart, S. Bayliss, B. Djulbegovic, et al.
Recombinant human erythropoietins and cancer patients: updated meta-analysis of 57 studies including 9353 patients.
J Natl Cancer Inst, May 17, 2006; 98(10): 708 - 714.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
R. Boccia, I. A. Malik, V. Raja, S. Kahanic, R. Liu, T. Lillie, D. Tomita, B. Clowney, and P. Silberstein
Darbepoetin alfa administered every three weeks is effective for the treatment of chemotherapy-induced anemia.
Oncologist, April 1, 2006; 11(4): 409 - 417.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
K. R. LaMontagne, J. Butler, D. J. Marshall, J. Tullai, Z. Gechtman, C. Hall, A. Meshaw, and F. X. Farrell
Recombinant epoetins do not stimulate tumor growth in erythropoietin receptor-positive breast carcinoma models.
Mol. Cancer Ther., February 1, 2006; 5(2): 347 - 355.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
J. H. Savonije, C. J. van Groeningen, L. W. Wormhoudt, and G. Giaccone
Early intervention with epoetin alfa during platinum-based chemotherapy: an analysis of the results of a multicenter, randomized, controlled trial based on initial hemoglobin level.
Oncologist, February 1, 2006; 11(2): 206 - 216.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. E. Hardee, M. O. Arcasoy, K. L. Blackwell, J. P. Kirkpatrick, and M. W. Dewhirst
Erythropoietin Biology in Cancer
Clin. Cancer Res., January 15, 2006; 12(2): 332 - 339.
[Abstract] [Full Text] [PDF]

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 JCOHome page
T. Grote, A. L. Yeilding, R. Castillo, D. Butler, E. Fishkin, D. H. Henry, M. DeLeo, K. Fink, and D. J. Sullivan
Efficacy and Safety Analysis of Epoetin Alfa in Patients With Small-Cell Lung Cancer: A Randomized, Double-Blind, Placebo-Controlled Trial
J. Clin. Oncol., December 20, 2005; 23(36): 9377 - 9386.
[Abstract] [Full Text] [PDF]

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 JCOHome page
M. Hedenus, J. Vansteenkiste, D. Kotasek, M. Austin, and R. G. Amado
Darbepoetin Alfa for the Treatment of Chemotherapy-Induced Anemia: Disease Progression and Survival Analysis From Four Randomized, Double-Blind, Placebo-Controlled Trials
J. Clin. Oncol., October 1, 2005; 23(28): 6941 - 6948.
[Abstract] [Full Text] [PDF]

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 JCOHome page
D. P. Steensma and C. L. Loprinzi
Erythropoietin Use in Cancer Patients: A Matter of Life and Death?
J. Clin. Oncol., September 1, 2005; 23(25): 5865 - 5868.
[Full Text] [PDF]


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