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Meta-Analysis
. 2009 Jul 8;2009(3):CD007303.
doi: 10.1002/14651858.CD007303.pub2.

Erythropoietin or Darbepoetin for patients with cancer--meta-analysis based on individual patient data

Julia Bohlius  1 , Kurt Schmidlin, Corinne Brillant, Guido Schwarzer, Sven Trelle, Jerome Seidenfeld, Marcel Zwahlen, Mike J Clarke, Olaf Weingart, Sabine Kluge, Margaret Piper, Maryann Napoli, Dirk Rades, David Steensma, Benjamin Djulbegovic, Martin F Fey, Isabelle Ray-Coquard, Volker Moebus, Gillian Thomas, Michael Untch, Martin Schumacher, Matthias Egger, Andreas Engert
Affiliations
Meta-Analysis

Erythropoietin or Darbepoetin for patients with cancer--meta-analysis based on individual patient data

Julia Bohlius et al. Cochrane Database Syst Rev. .

Abstract

Background: Erythropoiesis-stimulating agents (ESAs) reduce anemia in cancer patients and may improve quality of life, but there are concerns that ESAs might increase mortality.

Objectives: Our objectives were to examine the effect of ESAs and identify factors that modify the effects of ESAs on overall survival, progression free survival, thromboembolic and cardiovascular events as well as need for transfusions and other important safety and efficacy outcomes in cancer patients.

Search strategy: We searched the Cochrane Library, Medline, Embase and conference proceedings for eligible trials. Manufacturers of ESAs were contacted to identify additional trials.

Selection criteria: We included randomized controlled trials comparing epoetin or darbepoetin plus red blood cell transfusions (as necessary) versus red blood cell transfusions (as necessary) alone, to prevent or treat anemia in adult or pediatric cancer patients with or without concurrent antineoplastic therapy.

Data collection and analysis: We performed a meta-analysis of randomized controlled trials comparing epoetin alpha, epoetin beta or darbepoetin alpha plus red blood cell transfusions versus transfusion alone, for prophylaxis or therapy of anemia while or after receiving anti-cancer treatment. Patient-level data were obtained and analyzed by independent statisticians at two academic departments, using fixed-effects and random-effects meta-analysis. Analyses were according to the intention-to-treat principle. Primary endpoints were on study mortality and overall survival during the longest available follow-up, regardless of anticancer treatment, and in patients receiving chemotherapy. Tests for interactions were used to identify differences in effects of ESAs on mortality across pre-specified subgroups. The present review reports only the results for the primary endpoint.

Main results: A total of 13933 cancer patients from 53 trials were analyzed, 1530 patients died on-study and 4993 overall. ESAs increased on study mortality (combined hazard ratio [cHR] 1.17; 95% CI 1.06-1.30) and worsened overall survival (cHR 1.06; 95% CI 1.00-1.12), with little heterogeneity between trials (I(2) 0%, p=0.87 and I(2) 7.1%, p=0.33, respectively). Thirty-eight trials enrolled 10441 patients receiving chemotherapy. The cHR for on study mortality was 1.10 (95% CI 0.98-1.24) and 1.04; 95% CI 0.97-1.11) for overall survival. There was little evidence for a difference between trials of patients receiving different cancer treatments (P for interaction=0.42).

Authors' conclusions: ESA treatment in cancer patients increased on study mortality and worsened overall survival. For patients undergoing chemotherapy the increase was less pronounced, but an adverse effect could not be excluded.

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Conflict of interest statement

Julia Bohlius received honoraria and travel grants from Amgen. Andreas Engert received research funding and honoraria from Amgen, Roche and Johnson & Johnson. Gillian Thomas received research funding for the GOG‐191 study by Johnson & Johnson. Benjamin Djulbegovic received research funding from OrthoBiotech and consulted for Amgen. Volker Moebus received research funding and honoraria from Amgen, Bristol‐Myers Squibb, GlaxoSmithKline, Johnson & Johnson, Novartis, Pfizer, and Roche. Michael Untch received research funding for the PREPARE study from Amgen and Bristol‐Myers Squibb. Margaret Piper ist employed by the Blue Cross and Blue Shield Association, the trade organization for the independent US Blue Cross Blue Shield health insurance plans, but is not involved in the determination of coverage and reimbursement policy for individual plans. All other members of the Steering Committee, the Statistical Analysis Team and Reviewers declared to have no conflict of interest.

Figures

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Baseline characteristics, a)
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Baseline characteristics b)
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Baseline characteristics c)
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Identification of eligible trials
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On study mortality: censoring meta‐analysis, HRs < 1,0 indicate that more patients in the control arm had the event ("censoring"), HRs > 1,0 indicate that more patients in the ESA arm had the event ("censoring") compared to controls.
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Forest plot for on study mortality in all cancer patients based on two stage log‐rank fixed‐effects meta‐analysis
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Funnel plot (based on log‐rank estimates) for on study mortality in all cancer patients Explanation of terms used: Full text: highest publication achieved is a full text publication Abstract: highest publication achieved is an abstract publication ODAC: highest publication achieved is reporting of study results in documents presented at ODAC hearings Unpublished: to date the study was not published in any of the sources mentioned above Date of reference: June 26th 2008
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Influence analysis for on study mortality in all cancer patients
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Forest plot for on study mortality in chemotherapy trials based on two‐stage log‐rank fixed‐effect meta‐analysis
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Funnel plot (based on log‐rank estimates) for on study mortality in chemotherapy trials Explanation of terms used: Full text: highest publication achieved is a full text publication Abstract: highest publication achieved is an abstract publication ODAC: highest publication achieved is reporting of study results in documents presented at ODAC hearings Unpublished: to date the study was not published in any of the sources mentioned above Date of reference: June 26th 2008
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Influence analysis for on study mortality in chemotherapy trials
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Forest plot for overall survival in all cancer patients based on two‐stage log‐rank fixed effect meta‐analysis
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Funnel plot (based on log‐rank estimates) for overall survival in all cancer patients Explanation of terms used: Full text: highest publication achieved is a full text publication Abstract: highest publication achieved is an abstract publication ODAC: highest publication achieved is reporting of study results in documents presented at ODAC hearings Unpublished: to date the study was not published in any of the sources mentioned above Date of reference: June 26th 2008
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Influence analysis for overall survival in all cancer patients
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Forest plot for overall survival in chemotherapy trials based on two‐stage log‐rank fixed‐effect meta‐analysis
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Funnel plot (based on log‐rank estimates) for overall survival in chemotherapy trials (subset analysis) Explanation of terms used: Full text: highest publication achieved is a full text publication Abstract: highest publication achieved is an abstract publication ODAC: highest publication achieved is reporting of study results in documents presented at ODAC hearings Unpublished: to date the study was not published in any of the sources mentioned above Date of reference: June 26th 2008
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Influence analysis for overall survival in chemotherapy trials
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Comparing studies with last patient randomized before 2000 or after 2000
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Pooled Kaplan Meier plot for on study mortality in all cancer patients
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Pooled Kaplan Meier plot for on study mortality in chemotherapy patients
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Pooled Kaplan Meier plot for overall survival in all cancer trials
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Pooled Kaplan Meier plot for overall survival in chemotherapy trials (subset analysis)
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Baseline imbalances ECOG
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Level of EPO serum
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BMI
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Time from cancer diagnosis to date of randomization
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Hemoglobin
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Hematocrit
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Age
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Sex
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ECOG low versus high
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History of thromboembolic events
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History of cardiovascular events
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History of hypertension
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History of diabetes
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References

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Osterborg 1996 {published data only}
    1. Osterborg A, Boogaerts MA, Cimino R, Essers U, Holowiecki J, Juliusson G, et al. Recombinant human erythropoietin in transfusion‐dependent anemic patients with multiple myeloma and non‐Hodgkin's lymphoma ‐ a randomized multicenter study. Blood 1996;87(7):2675‐82. - PubMed
Osterborg 2002 {published data only}
    1. Osterborg A, Brandberg Y, Hedenus M. Impact of epoetin‐ß on survival of patients with lymphoproliferative malignancies: long‐term follow up of a large randomized study. British Journal of Haematology 2005;129:206‐9. - PubMed
    1. Osterborg A, Brandberg Y, Molostova V, Iosava G, Abdulkadyrov K, Hedenus M, et al. Randomized, double‐blind, placebo‐controlled trial of recombinant human erythropoietin, epoetin beta, in hematologic malignancies. Journal of Clinical Oncology 2002;20(10):2486‐94. - PubMed
Pirker 2008 {published data only}
    1. Amgen. Aranesp(R) ``145 Study'' Shows No Difference in Survival in Patients with Small‐Cell Lung Cancer. Amgen Thousand Oaks, CA, 2007; Vol. http://wwwext.amgen.com/media/media_pr_detail.jsp?year=2007&releaseI... [date of last access April 28, 2009].
    1. Pirker R, Ramlau RA, Schuette W, Zatloukal P, Ferreira I, Lillie T, et al. Safety and Efficacy of Darbepoetin Alfa in Previously Untreated Extensive‐Stage Small‐Cell Lung Cancer Treated With Platinum Plus Etoposide. Journal of Clinical Oncology 2008;26(14):2342‐9. - PubMed
Pronzato 2002 {published data only}
    1. Pronzato P, Cortesi E, Rijt C, Moreno‐Nogueria A, Raimundo D, Ostler P, et al. Early intervention with epoetin alfa in breast cancer (BC) patients (pts) undergoing chemotherapy (CT): results of a randomized, multicenter, phase IIIb study (EPO‐INT‐47 Study Group). Annals of Oncology 2002; Vol. 13, issue Suppl 5:168.
Quirt 1996 {published data only}
    1. Quirt I, Micucci S, Moran LA, Pater J, Browman G. The role of recombinant human erythropoietin (EPO) in reducing red blood cell transfusions and maintaining quality of life (QOL) in patients with lymphoma and solid tumors receiving cytotoxic chemotherapy. Results of a randomized, double‐blind, placebo‐controlled clinical trial. Blood 1996; Vol. 88, issue 10 Suppl 1:347a, abstract 1378.
Ray‐Coquard 2006 {published data only}
    1. Ray‐Coquard I, Dussart S, Goillot C, Mayeur D, Debourdeau P, Ghesquieres H, et al. A risk model for severe anemia to select cancer patients for primary prophylaxis with epoetin {alpha}: a prospective randomized controlled trial of the ELYPSE study group. Annals of Oncology 2009, issue doi:10.1093/annonc/mdn750. - PubMed
    1. Ray‐Coquard I, Perol D, Debourdeau P, Chabaud S, Chelghoum M, Mayeur D, et al. ELYPSE 4: A prospective randomized trial comparing Epo A in primary prophylaxis of severe anemia requiring red cells transfusion in high risk patients. Annals of Oncology 2006;17(Suppl 9):ix294.
Razzouk 2006 {published data only}
    1. Hinds PS, Hockenberry M, Feusner J, Hord JD, Rackoff W, Rozzouk BI. Hemoglobin response and improvements in quality of life in anemic children with cancer receiving myelosuppressive chemotherapy. Journal of Supportive Oncology 2005;3(6 Suppl 4):10‐1. - PubMed
    1. Razzouk BI, Hockenberry M, Hinds PS, Feusner J, Rackoff W, Hord JD. Influence of hemoglobin response to epoetin alfa on quality‐of‐life in anemic children with cancer receiving myelosuppressive chemotherapy. Blood 2004; Vol. 104, issue 11:abstract 221.
    1. Razzouk BI, Hockenberry M, Hinds PS, Rackoff W, Hord JD. A double‐blind, placebo‐controlled study of once‐weekly epoetin alfa in children with cancer undergoing myelosuppressive chemotherapy. Journal of Clinical Oncology 2004; Vol. 22, issue 14S:abstract 8527. - PubMed
    1. Razzouk BI, Hord JD, Hockenberry M, Hinds PS, Feusner J, Williams D, et al. Double‐blind, placebo‐controlled study of quality of life, hematologic end points, and safety of weekly epoetin alfa in children with cancer receiving myelosuppressive chemotherapy. Journal of Clinical Oncology 2006;24(22):3583‐9. - PubMed
Rose 1994 {published data only}
    1. Rose E, Rai K, Revicki D, et al. Clinical and health status assessments in anemic chronic lymphocytic leukemia (CLL) patients treated with epoetin alfa (EPO). Blood 1994; Vol. 84, issue 10 Suppl 1:526a.
Savonije 2005 {published data only}
    1. Savonije J, Groeningen C, Bochove A, Pinedo H, Giaccone G. Early intervention with epoetin‐alfa during platinum‐based chemotherapy. Journal of Clinical Oncology 2004; Vol. 22, issue 14S:abstract 8111.
    1. Savonije JH, Groeningen CJ, Bochove A, Honkoop AH, Felius CL, Wormhoudt LW, et al. Effects of early intervention with epoetin alfa on transfusion requirement, hemoglobin level and survival during platinum‐based chemotherapy: Results of a multicenter randomised controlled trial. European Journal of Cancer 2005;41(11):1560‐9. - PubMed
    1. Savonije JH, Groeningen CJ, Wormhoudt LW, Giaccone G. Early Intervention with epoetin alfa during platinum‐based chemotherapy: an analysis of quality‐of‐life results of a multicenter, randomized, controlled trial compared with population normative data. The oncologist 2006;11(2):197‐205. - PubMed
Smith 2008 {published data only}
    1. 20010103. Continuing reassessment of the risks of erythropoiesis‐stimulating agents (ESAs) administered for the treatment of anemia associated with cancer chemotherapy. Department of Health and Human Services, Food and Drugs Administration, Center for Drug Evaluation and Research, Oncologic Drugs Advisory Committee, Rockville (MD), USA, 2007; Vol. http://www.fda.gov/ohrms/dockets/ac/07/briefing/2007‐4301b2‐02‐ FDA.pdf.
    1. Glaspy J, Smith RE, Aapro M, Ludwig H, Pinter T, Smakal M, et al. Results from a phase 3 randomized, double blind, placebo controlled study of darbepoetin alfa for the treatment of anemia in cancer patients not receiving chemotherapy or radiotherapy. Haematologica 2007; Vol. 92, issue Suppl 1:136. - PubMed
    1. Smith RE, Aapro MS, Ludwig H, Pinter T, Smakal M, Ciuleanu TE, et al. Darbepoetin Alfa for the Treatment of Anemia in Patients With Active Cancer Not Receiving Chemotherapy or Radiotherapy: Results of a Phase III, Multicenter, Randomized, Double‐Blind, Placebo‐Controlled Study. Journal of Clinical Oncology 2008;26(7):1040‐50. - PubMed
Strauss 2008 {published data only}
    1. Strauss H, Haendgen G, Dunst.J, Koelbl H. Effects of anaemia correction with epoetin beta in patients with advanced cervical cancer. Proceedings of the American Society of Clinical Oncology 2003:abstract 5121.
    1. Strauss HG, Haendgen G, Dunst J, Haywrad CRW, Burger HU, Scherhag A, et al. Effects of anemia correction with epoetin beta in patients receiving radiochemotherapy for advanced cervical cancer. International Journal of Gynecological Cancer 2008;18(Suppl 3):515‐24. - PubMed
Taylor 2005 {published data only}
    1. Taylor K, Ganly P, Charu V, DiBenedetto J, Kracht K, Rossi G, et al. Randomized, double‐blind, placebo‐controlled study of darbepoetin alfa every 3 weeks for the treatment of chemotherapy‐induced anemia. Blood 2005; Vol. 106, issue 11:abstract 3556.
Ten Bokkel Huinink 1998 {published data only}
    1. Reed N, Rhan S, Hayward C, Burger H, Bokkel Huinink W. Impact of epoetin beta on the survival of anemic patients with ovarian cancer receiving platinum‐based chemotherapy. Proceedings of the American Society of Clinical Oncology 2003; Vol. 23, issue 16s:abstract 5102.
    1. Bokkel Huinink WW, Swart CA, Toorn DW, Morack G, Breed WP, Hillen HF, et al. Controlled multicentre study of the influence of subcutaneous recombinant human erythropoietin on anaemia and transfusion dependency in patients with ovarian carcinoma treated with platinum‐based chemotherapy. Medical Oncology 1998;15(3):174‐82. - PubMed
Thatcher 1999 {published data only}
    1. Campos E, Radford J, Steward Milroy R, Dougal M, Swindell R, et al. Clinical and in vitro effects of recombinant human erythropoietin in patients receiving intensive chemotherapy for small‐cell lung cancer. Journal of Clinical Oncology 1995;13(7):1623‐31. - PubMed
    1. Thatcher N, Campos ES, Bell DR, Steward WP, Varghese G, Morant R, et al. Epoetin alpha prevents anaemia and reduces transfusion requirements in patients undergoing primarily platinum‐based chemotherapy for small cell lung cancer. British Journal of Cancer 1999;80(3‐4):396‐402. - PMC - PubMed
Thomas 2002 {published data only}
    1. Thomas H, McAdam KF, Thomas RJ, Joffe JK, Sugden EM, Awwad ST, et al. Early intervention with epoetin alfa for treatment of anaemia and improvement of quality of life in cancer patients undergoing myelotoxic chemotherapy. Annals of Oncology 2002; Vol. 13, issue Suppl 5:177.
Thomas 2008 {published data only}
    1. Luksenburg H, Weir A, Wager R. GOG‐191: Safety concerns associated with Aranesp (darbepoetin alfa) Amgen Inc. and Procrit (epoetin alfa) Ortho Biotech L.P., for the treatment of Anemia associated with cancer chemotherapy. Department of Health and Human Services, Food and Drug Administration, Center for Drug Evaluation and Research, Oncologic Drugs Advisory Committee, Rockville (MD), USA, 2004; Vol. http://www.fda.gov/ohrms/dockets/ac/04/briefing/4037b2_04.pdf [date of last access March 27, 2009].
    1. Thomas G, Ali S, Hoebers FJP, Darcy KM, Rodgers WH, Patel M, et al. Phase III trial to evaluate the efficacy of maintaining hemoglobin levels above 12.0 g/dL with erythropoietin vs above 10.0 g/dL without erythropoietin in anemic patients receiving concurrent radiation and cisplatin for cervical cancer. Gynecologic Oncology 2008;108(2):317‐25. - PMC - PubMed
Untch 2008 {published data only}
    1. Untch M, Fascing PA, Bauernfeind I, Conrad U, Camara O, Fett W, et al. PREPARE trial. A randomized phase III trial comparing preoperative, dose‐dense, dose‐intensified chemotherapy with epirubicin, paclitaxel and CMF with a standard dosed epirubicin/cyclophosphamide followed by paclitaxel +/‐ darbepoetin alfa in primary breast cancer: A preplanned interim analysis of efficacy at surgery. Journal of Clinical Oncology 2008; Vol. 26, issue Suppl:abstract 517.
Vadhan‐Raj 2004 {published data only}
    1. Vadhan‐Raj S, Skibber JM, Crane C, Buesos‐Ramos CE, Rodriguez‐Bigas MA, Feig BW, et al. Randomized, double‐blind, placebo‐controlled trial of epoetin alfa (Procrit) in patients with rectal and gastric cancer undergoing chemo‐radiotherapy (CT/RT) followed by surgery: early termination of the trial due to increased incidence of thromboembolic events (TEE). Blood 2004; Vol. 104, issue 11:797a, abstract 2915.
Vansteenkiste 2002 {published data only}
    1. Kallich JD, Tchekmedyian NS, Damiano AM, Shi J, Black JT, Erder MH. Psychological outcomes associated with anemia‐related fatigue in cancer patients. Oncology (Huntingt) 2002;16(9 Suppl 10):117‐24. - PubMed
    1. Pirker R, Vansteenkiste J, Gateley J, Yates P, Colowick A, Musil J. A phase 3, double‐blind, placebo‐controlled, randomized study of novel erythropoiesis stimulating protein (NESP) in patients undergoing platinum treatment for lung cancer. Proceedings of the American Society of Clinical Oncology 2001; Vol. 20:abstract 1572.
    1. Tchekmedyian NS, Kallich J, McDermott A, Fayers P, Erder MH. The relationship between psychologic distress and cancer‐related fatigue. Cancer 2003;98(1):198‐203. - PubMed
    1. Tchekmedyian S, Glaspy J, Colowick A, Tomita D, Rossi G. Effect of darbepoetin alfa and recombinant human erythropoietin (rHuEPO) on early hemoglobin (Hb) changes in anemic cancer patients (pts). Annals of Oncology 2002; Vol. 13, issue Suppl 5:184.
    1. Vansteenkiste J, Pirker R, Massuti B, Barata F, Font A, Fiegl M, et al. Double‐blind, placebo‐controlled, randomized phase III trial of darbepoetin alfa in lung cancer patients receiving chemotherapy. Journal of the National Cancer Institute 2002;94:1211‐20. - PubMed
Wilkinson 2006 {published data only}
    1. Wilkinson PM, Antonopoulos M, Lahousen M, Lind M, Kosmidis P, Epo INT. Epoetin alfa in platinum‐treated ovarian cancer patients: results of a multinational, multicentre, randomised trial. British Journal of Cancer 2006;94(7):947‐54. - PMC - PubMed
Witzig 2005 {published data only}
    1. Dicato M, Vercammen E, Liu KL, Xiu LX, Bowers P. Relationship of body weight to efficacy of a fixed‐dose regimen of epoetin alfa vs placebo in anemic cancer patients. Haematologica 2005; Vol. 90, issue Suppl 2:abstract 0077.
    1. Witzig TE, Silberstein PT, Loprinzi CL, Sloan JA, Novotny PJ, Mailliard JA, et al. Phase III, randomized, double‐blind study of epoetin alfa compared with placebo in anemic patients receiving chemotherapy. Journal of Clinical Oncology 2005;23(12):2606‐17. - PubMed
Wright 2007 {published data only}
    1. Luksenburg H, Weir A, Wager R. EPO‐CAN‐20: Safety concerns associated with Aranesp (darbepoetin alfa) Amgen Inc and Procrit (epoetin alfa) Ortho Biotech L.P. for the treatment of anemia associated with cancer chemotherapy. Oncologic Drugs Advisory Committee, Department of Health and Human Services, Food and Drug Administration, Center for Drug Evaluation and Research, Rockville (MD), USA, 2004; Vol. http://www.fda.gov/ohrms/dockets/ac/04/briefing/4037b2_04.pdf [date of last access March 27, 2009].
    1. Wright JR, Ung YC, Julian JA, Pritchard KI, Whelan TJ, Smith C, et al. Randomized, double‐blind, placebo‐controlled trial of erythropoietin in non‐small‐cell lung cancer with disease‐related anemia. Journal of Clinical Oncology 2007;25(9):1027‐32. - PubMed

References to studies excluded from this review

Abdelrazik 2007 {published data only}
    1. Abdelrazik N, Fouda M. Once weekly recombinant human erythropoietin treatment for cancer‐induced anemia in children with acute lymphoblastic leukemia receiving maintenance chemotherapy: A randomized case‐controlled study. Hematology 2007;12(6):533‐41. - PubMed
Alexopoulos 2004 {published data only}
    1. Alexopoulos C, Kotsori A. A randomized comparison of rHuEPO with darbepoetin for cancer related anemia. Annals of Oncology 2004;15 Suppl 3:abstract 832P.
Antonadou 2001 {published data only}
    1. Antonadou D, Cardamakis E, Puglisi M, Malamos N, Throuvalas N. Erythropoietin enhances radiation treatment efficacy in patients with pelvic malignancies. Final results of a randomized phase III study. European Journal of Cancer 2001; Vol. 37, issue Suppl 6:S144.
Aravantinos 2003 {published data only}
    1. Aravantinos G, Linardou H, Makridaki D, Laiou E, Zafiropoulos A, Janninis J, et al. Recombinant human erythropoietin for platinum‐based chemotherapy‐induced anaemia: A single‐centre randomised study. Journal of the Balkan Union of Oncology 2003;8(2):127‐32. - PubMed
Auerbach 2004 {published data only}
    1. Auerbach M, Ballard H, Trout JR, McIlwain M, Ackerman A, Bahrain H, et al. Intravenous iron optimizes the response to recombinant human erythropoietin in cancer patients with chemotherapy‐related anemia: a multicenter, open‐label, randomized trial. Journal of Clinical Oncology 2004;22(7):1301‐7. - PubMed
Aziz 2001 {published data only}
    1. Aziz K, Hashem T, Mobarek N, Bary N, Ghoneimy I, Haddad S. Does Recombinant Human Erythropoietin Improve the Outcome of Radiation Therapy in Head and Neck Cancer Patients. Proceedings of the American Society for Therapeutic Radiology and Oncology 2001:abstract 2274.
Bamias 2003 {published data only}
    1. Bamias A, Aravantinos G, Kalofonos C, Timotheadou N, Siafaka V, Vlahou I, et al. Prevention of anemia in patients with solid tumors receiving platinum‐based chemotherapy by recombinant human erythropoietin (rHuEpo): A prospective, open label, randomized trial by the Hellenic Cooperative Oncology Group. Oncology 2003;64(2):102‐10. - PubMed
Beggs 2003 {published data only}
    1. Beggs VL, Disalvo WM, Meyer LP, Gragnev KH, Gibson JJ, Hoopes PJ, et al. Fatigue and plasma cytokines in a randomized double‐blind placebo‐controlled trial of epoetin alfa in patients undergoing combined modality therapy for unresectable non‐small cell lung cancer (NSCLC). Proceedings of the American Society of Clinical Oncology 2003; Vol. 22:abstract 2948.
Bessho 1997 {published data only}
    1. Bessho M, Hirashima K, Asano S, Ikeda Y, Ogawa N, Tomonaga M, et al. Treatment of the anemia of aplastic anemia patients with recombinant human erythropoietin in combination with granulocyte colony‐stimulating factor: a multicenter randomized controlled study. Multicenter Study Group. European Journal of Haematology 1997;58(4):265‐72. - PubMed
Bindi 2004 {published data only}
    1. Bindi M, Montemaggi P, Sabatino M, Paolelli L, Petrioli R, Morelli R, et al. Reticulocytes can represent an early indicator of the erythropoietic response to Darbepoetin alfa in the anemia by chemotherapy. Journal of Clinical Oncology 2004; Vol. 22, issue 14s:786, abstract 8245.
Blayney 2003 {published data only}
    1. Blayney D, Fesen M, Mirtsching BC, Katz D, Tomita D. Every‐2‐Week Darbepoetin Alfa improves hemoglobin in anemic patients with cancer undergoing chemotherapy: A stratified analysis by tumor type. Blood 2003; Vol. 102 (11):abstract 3779.
Blohmer 2003 {published data only}
    1. Blohmer JU, Petry K, Kolben M, Kimmig R, Boehmer D, Wuerschmidt J, et al. Adjuvant sequential chemo‐radiotherapy with vs. without erythropoietin in high‐risk patients with carcinoma of the cervix. Proceedings of the American Society of Clinical Oncology 2001; Vol. 20:abstract: 823.
    1. Blohmer JU, Wurschmidt F, Petry U, Weise G, Sehouli J, Kimming R, et al. Results with sequential adjuvant chemo‐radiotherapy with vs without epoetin alfa for patients with high‐risk cervical cancer: Results of a prospective, randomized, open and controlled AGO‐ and NOGGO‐intergroup study. Annals of Oncology 2004;15 (Suppl 3):abstract 447PD.
    1. Blohmer U, Wurschmidt U, Petry G, Weise J, Sehouli J, Kimmig R, et al. 6th interim analysis of a prospective, randomized, open and controlled AGO‐ and NOGGO‐intergroup study: Sequential adjuvant chemo‐radiotherapy with vs without epoetin alfa for pts with high‐risk cervical cancer. Proceedings of the American Society of Clinical Oncology 2003; Vol. 22:abstract 1789.
Candelaria 2005 {published data only}
    1. Candelaria M, Cetina L, Duenas‐Gonzalez A. Anemia in cervical cancer patients: implications for iron supplementation therapy. Medical Oncology 2005;22(2):161‐8. - PubMed
Canon 2006 {published data only}
    1. Canon JL, Vansteenkiste J, Bodoky G, Mateos MV, Bastit L, Ferreira I, et al. Randomized, double‐blind, active‐controlled trial of every‐3‐week darbepoetin alfa for the treatment of chemotherapy‐induced anemia. Journal of the National Cancer Institute 2006;98(4):273‐84. - PubMed
    1. Canon JL, Vansteenkiste J, Bodoky G, Mateos MV, Bastit L, Ferreira I, et al. Results of a randomised, double‐blind, active‐controlled trial of darbepoetin alfa administered once every 3 weeks for the treatment of anaemia in patients receiving multicycle chemotherapy. Haematologica 2005; Vol. 90, issue Suppl 2:abstract 471.
Carabantes 1999 {published data only}
    1. Carabantes FJ, Alonso CJ, Rius F, Benavides M, Hebrero ML, Garcia S, et al. Epoetin alfa (EPO) prevents anaemia and improves quality of life (QOL) in cancer patients (PTS) undergoing platinum‐based chemotherapy. European Journal of Cancer 1999; Vol. 35, issue S4:abstract 1482.
    1. Carabantes FJ, Benavides M, Trujillo R, Cobo M, Hebrero ML, Garcia S, et al. Epoetin alfa in the prevention of anemia in cancer patients undergoing platinum‐based chemotherapy (CT). A prospective randomized study. Proceedings of the American Society of Clinical Oncology 1999; Vol. 18:abstract 2303.
Casadevall 2004 {published data only}
    1. Casadevall N, Durieux P, Dubois S, Hemery F, Lepage E, Quarre MC, et al. Health, economic, and quality‐of‐life effects of erythropoietin and granulocyte colony‐stimulating factor for the treatment of myelodysplastic syndromes: a randomized, controlled trial. Blood 2004;104(2):321‐7. - PubMed
    1. Casadevall N, Lepage E, Durieux P, Dubois S, Dreyfus F, Quarre MC, et al. Erythropoietin (RHUEPO) plus G‐CSF in the treatment of anemia in myelodysplastic syndromes (MDS): results of a randomised trial with impact on quality of life and costs. The Hematology Journal 2001, issue Suppl 1:abstract 687.
Cascinu 1994 {published data only}
    1. Cascinu S, Fedeli A, Ferro E, Fedeli SL, Catalano G. Recombinant human erythropoietin treatment in cisplatin‐associated anemia: a randomized, double‐blind trial with placebo. Journal of Clinical Oncology 1994;12:1058‐62. - PubMed
Cazzola 2003 {published data only}
    1. Cazzola M, Beguin Y, Kloczko J, Spicka I, Coiffier B. Once‐weekly epoetin beta is highly effective in treating anaemic patients with lymphoproliferative malignancy and defective endogenous erythropoietin production. British Journal of Haematology 2003;122(3):386‐93. - PubMed
    1. Cazzola M, Coiffier B, Kloczko J, Spika I. Once weekly NeoRecormon® (epoetin beta) for the treatment of anemia associated with lymphoproliferative malignancies: results of the NOW (NeoRecormon® once weekly) study. Hematology Journal 2002, issue 3 Suppl 1:abstract 0182.
Chan 1995 {published data only}
    1. Chan AT, Leung WT, Lin J, Yeo W, Johnson PJ. Recombinant human erythropoietin for anaemia in Chinese cancer patients on chemotherapy. Clinical Oncology (Royal College of Radiologists) 1995;7(4):272. - PubMed
Charu 2007a {published data only}
    1. Charu V, Belani CP, Gill AN, Bhatt M, Ben Jacob A, Tomita D, et al. A controlled, randomized, open‐label study to evaluate the effect of every‐2‐week darbepoetin alfa for anemia of cancer. Annual Meeting Proceedings of the American Society of Clinical Oncology 2004:abstract 8084.
    1. Charu V, Saidman B, Ben Jacob A, Justice GR, Maniam AS, Tomita D, et al. A randomized, open‐label, multicenter trial of immediate versus delayed intervention with darbepoetin alfa for chemotherapy‐induced anemia. Oncologist 2007;12(10):1253‐63. - PubMed
Christodoulakis 2005 {published data only}
    1. Christodoulakis M, Tsiftsis DD, Hellenic Surgical Oncology Perioperative EPO Study Group. Preoperative epoetin alfa in colorectal surgery: a randomized, controlled study. Annals of Surgical Oncology 2005;12(9):718‐25. - PubMed
Crawford 1997 {published data only}
    1. Crawford J, Blackwell S, Shoemaker D, Pupa MR, Sparrow T, Herndon J, et al. Prevention of chemotherapy‐related anemia by recombinant human erythropoietin (EPO) in patients with small cell lung cancer receiving cyclophosphamide, doxorubicin, and etoposide (CAE) chemotherapy with G‐CSF support. Lung Cancer 1997; Vol. 18 (Suppl 1):abstract 796.
Crawford 2003 {published data only}
    1. Crawford J, Robert F, Perry M, Belani CP, Sarokhan B. Epoetin alfa 40,000 u once weekly maintains hemoglobin in advanced non‐small‐cell lung cancer patients receiving first‐line chemotherapy. Proceedings of the American Society of Clinical Oncology 2003;22:628, abstract 2527.
Crawford 2007 {published data only}
    1. Crawford J, Robert F, Perry MC, Belani C, Williams D, Anemia Prevention in NSCLC Group. A randomized trial comparing immediate versus delayed treatment of anemia with once‐weekly epoetin alfa in patients with non‐small cell lung cancer scheduled to receive first‐line chemotherapy. Journal of thoracic oncology : official publication of the International Association for the Study of Lung Cancer 2007;2(3):210‐20. - PubMed
Daneryd 1998 {published data only}
    1. Daneryd P, Svanberg E, Körner U, Lindholm E, Sandström R, Brevinge H, et al. Protection of metabolic and exercise capacity in unselected weight‐losing cancer patients following treatment with recombinant erythropoietin: A randomized prospective study. Cancer Research 1998;58:5374‐9. - PubMed
    1. Lindholm E, Daneryd P, Korner U, Hyltander A, Fouladiun M, Lundholm K. Effects of recombinant erythropoietin in palliative treatment of unselected cancer patients. Clinical Cancer Research 2004;10(20):6855‐64. - PubMed
    1. Lonnroth C, Svensson M, Wang W, Korner U, Daneryd P, Nilsson O, et al. Survival and erythropoietin receptor protein in tumours from patients randomly treated with rhEPO for palliative care. Medical Oncology 2008;25(1):22‐9. - PubMed
Dannemann 2004 {published data only}
    1. Dannemann B, Wacholtz M, Lau H, Cheung W. Pharmacokinetics (PK) and pharmacodynamics (PD) of epoetin alfa in cancer patients with anemia receiving cyclic chemotherapy. Journal of Clinical Oncology 2004; Vol. 22, issue 14s:775, abstract 8203.
Del Mastro 1997 {published data only}
    1. Mastro L, Venturini M, Lionetto R, Garrone O, Melioli G, Pasquetti W, et al. Randomized phase III trial evaluating the role of erythropoietin in the prevention of chemotherapy‐induced anemia. Journal of Clinical Oncology 1997;15(7):2715‐21. - PubMed
Dunphy 1999 {published data only}
    1. Dunphy FR, Harrison BR, Dunleavy TL, Rodriguez JJ, Hilton JG, Boyd JH. Erythropoietin Reduces Anemia and Transfusions. Cancer 1999;86:1362‐7. - PubMed
Elsaid 2001 {published data only}
    1. Elsaid A, Farouk M. Significance of anemia and role of erythropoietin in radiation induced mucositis in head and neck cancer patients. International Journal of Radiation Oncology Biology Physics 2001; Vol. 51, issue 3 Suppl 1:368.
Freeman 2006 {published data only}
    1. Freeman III BB, Hinds P, Iacono LC, Razzouk BI, Burghen E, Stewart CF. Pharmacokinetics and pharmacodynamics of intravenous epoetin alfa in children with cancer. Pediatric Blood & Cancer 2006;47(5):572‐9. - PubMed
Garton 1995 {published data only}
    1. Garton JP, Gertz MA, Witzig TE, Greipp PR, Lust JA, Schroeder G, et al. Epoetin alfa for the treatment of the anemia of multiple myeloma. Archives of Internal Medicine 1995;155:2069‐74. - PubMed
Gebbia 1992 {published data only}
    1. Gebbia V, Gebbia N, Testa A, Valenza R, Borsellino N, Rausa L, et al. Subcutaneous recombinant human erythropoietin prevents chemotherapy‐related anemia in patients with advanced cancer. International Journal of Oncology 1992;1:341‐5. - PubMed
Glaspy 2002 {published data only}
    1. Glaspy JA, Jadeja JS, Justice G, Kessler J, Richards D, Schwartzberg L, et al. Darbepoetin alfa given every 1 or 2 weeks alleviates anaemia associated with cancer chemotherapy. British Journal of Cancer 2002;87(3):268‐76. - PMC - PubMed
    1. Glaspy JA, Tchekmedyian NS. Darbepoetin alfa administered every 2 weeks alleviates anemia in cancer patients receiving chemotherapy. Oncology (Huntingt) 2002;16(10 Suppl 11):23‐9. - PubMed
Glaspy 2003 {published data only}
    1. Glaspy JA, Jadeja JS, Justice G, Fleishman A, Rossi G, Colowick AB. A randomized, active‐control, pilot trial of front‐loaded dosing regimens of darbepoetin‐alfa for the treatment of patients with anemia during chemotherapy for malignant disease. Cancer 2003;97:1312‐20. - PubMed
Glaspy 2005 {published data only}
    1. Glaspy J, Henry D, Patel R, Tchekmedyian S, Applebaum S, Berdeaux D, et al. Effects of chemotherapy on endogenous erythropoietin levels and the pharmacokinetics and erythropoietic response of darbepoetin alfa: A randomised clinical trial of synchronous versus asynchronous dosing of darbepoetin alfa. European Journal of Cancer 2005;41(8):1140‐9. - PubMed
Glaspy 2006 {published data only}
    1. Glaspy J, Jadeja J, Justice G, Fleishman A, Rossi G, Colowick A. Optimizing the management of anemia in patients with cancer: a randomized, active‐controlled, study investigating the dosing of darbepoetin alfa. Hematology Journal 2002:abstract 0109.
    1. Glaspy J, Vadhan‐Raj S, Patel R, Bosserman L, Hu E, Lloyd RE, et al. Randomized comparison of every‐2‐week darbepoetin alfa and weekly epoetin alfa for the treatment of chemotherapy‐induced anemia: the 20030125 Study Group Trial. Journal of Clinical Oncology 2006;24(15):2290‐7. - PubMed
Glimelius 1998 {published data only}
    1. Glimelius B, Linne T, Hoffman K, Larsson L, Svensson JH, Nasman P, et al. Epoetin beta in the treatment of anemia in patients with advanced gastrointestinal cancer. Journal of Clinical Oncology 1998;16(2):434‐40. - PubMed
Glossmann 2003 {published data only}
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    1. Granetto C, Ricci S, Martoni A, Pezzella G, Testore F, Mattioli R, et al. Comparing the efficacy and safety of fixed versus weight‐based dosing of epoetin alpha in anemic cancer patients receiving platinum‐based chemotherapy. Oncology Reports 2003;10(5):1289‐96. - PubMed
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Henry 2007 {published data only}
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Italian 1998 {published data only}
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Jitnuyanont 2001 {published data only}
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Johansson 2001 {published data only}
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Justice 2005 {published data only}
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Kosmadakis 2003 {published data only}
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Kotasek 2007 {published data only}
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Pierelli 1999 {published data only}
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Policarpo 2007 {published data only}
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Porter 1996 {published data only}
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Rau 1998 {published data only}
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Rearden 2004 {published data only}
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Sakai 2004 {published data only}
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Watanabe 2006 {published data only}
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Zhang 2003 {published data only}
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