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Meta-Analysis
. 2014 May 28;2014(5):CD003895.
doi: 10.1002/14651858.CD003895.pub3.

Frequency of administration of erythropoiesis-stimulating agents for the anaemia of end-stage kidney disease in dialysis patients

Deirdre Hahn  1 , June D Cody, Elisabeth M Hodson
Affiliations
Meta-Analysis

Frequency of administration of erythropoiesis-stimulating agents for the anaemia of end-stage kidney disease in dialysis patients

Deirdre Hahn et al. Cochrane Database Syst Rev. .

Abstract

Background: The benefits of erythropoiesis-stimulating agents (ESA) for dialysis patients have been demonstrated. However, it remains unclear whether the efficacy and safety of new, longer-acting ESA given less frequently is equivalent to recombinant human erythropoietin (rHuEPO) preparations. This is an update of a review first published in 2002 and last updated in 2005.

Objectives: This review aimed to establish the optimal frequency of ESA administration in terms of effectiveness (correction of anaemia, and freedom from adverse events) and efficiency (optimal resource use) of different ESA dose regimens.

Search methods: We searched the Cochrane Renal Group's Specialised Register to 21 March 2013 through contact with the Trials' Search Co-ordinator using search terms relevant to this review.

Selection criteria: We included randomised control trials (RCTs) comparing different frequencies of ESA administration in dialysis patients.

Data collection and analysis: Two authors independently assessed study eligibility, risk of bias and extracted data. Results were expressed as risk ratio (RR) or risk differences (RD) with 95% confidence intervals (CI) for dichotomous outcomes. For continuous outcomes the mean difference (MD) or standardised mean difference (SMD) with 95% confidence intervals (CI) was used. Statistical analyses were performed using the random-effects model.

Main results: This review included 33 studies (5526 participants), 22 of which were added for this update. Risk of bias was generally high; only nine studies were assessed at low risk of bias for sequence generation and 14 studies for allocation concealment. Although only four studies were placebo-controlled, all were considered to be at low risk of performance or detection bias because the primary outcome of haemoglobin level was a laboratory-derived assessment and unlikely to be influenced by lack of blinding. We found that 16 studies were at low risk of attrition bias and five were at low risk of selection bias; only one study reporting sources of support was not funded by a pharmaceutical company.We compared four different interventions: Continuous erythropoietin receptor agonists (CERA) versus other ESA (darbepoetin or rHuEPO); different frequencies of darbepoetin administration; darbepoetin versus rHuEPO; and different frequencies of rHuEPO administration.There were no significant differences in maintaining final haemoglobin between CERA administered at two weekly intervals (4 studies, 1762 participants: MD 0.08 g/dL, 95% CI -0.04 to 0.21) or four weekly intervals (two studies, 1245 participants: MD -0.03 g/dL, 95% CI -0.17 to 0.12) compared with rHuEPO administered at two to three weekly intervals. In one study comparing CERA administered every two weeks with darbepoetin administered once/week, there was no significant difference in final haemoglobin (313 participants: MD 0.30 g/dL, 95% CI 0.05 to 0.55). In comparisons of once/week with once every two weeks darbepoetin (two studies, 356 participants: MD 0.04 g/dL, 95% CI -0.45 to 0.52) and once every two weeks with monthly darbepoetin (one study, 64 participants: MD 0.40 g/dL, 95% CI -0.37 to 1.17) there were no significant differences in final haemoglobin levels. There was marked heterogeneity among studies comparing weekly darbepoetin with once every two weeks and was possibly related to different administration protocols. Eight studies compared weekly darbepoetin with rHuEPO given two to three times/week; no statistical difference in final haemoglobin was demonstrated (6 studies, 1638 participants: MD 0.02 g/dL, 95% CI -0.09 to 0.12). Fourteen studies compared different frequencies of rHuEPO. No statistical difference was demonstrated in final haemoglobin (7 studies, 393 participants: SMD -0.17 g/dL, 95% CI -0.39 to 0.05). Adverse events did not differ significantly within comparisons; however, mortality and quality of life were poorly reported, particularly in earlier publications.

Authors' conclusions: Longer-acting ESA (darbepoetin and CERA) administered at one to four week intervals are non-inferior to rHuEPO given one to three times/week in terms of achieving haemoglobin targets without any significant differences in adverse events in haemodialysis patients. Additional RCTs are required to evaluate different frequencies of ESA in peritoneal and paediatric dialysis patients and to compare different longer-acting ESA (such as darbepoetin compared with CERA).

PubMed Disclaimer

Conflict of interest statement

This systematic review was initially one of six funded (in 1996) by Janssen Cilag who manufacture of Eprex (erythropoietin‐α) a recombinant human erythropoietin. Our contract stated that the University of Aberdeen owned the intellectual property rights and we had the right to publish the results without restriction.

No industry funding was sought for the updates of this review.

Figures

1
1
Flow diagram for study selection CERA ‐ continuous erythropoietin receptor agonists; ESA ‐ erythropoiesis‐stimulating agents
2
2
Risk of bias graph: review authors' judgements about each risk of bias item presented as percentages across all included studies
3
3
Risk of bias summary: review authors' judgements about each risk of bias item for each included study
1.1
1.1. Analysis
Comparison 1 CERA versus other ESA, Outcome 1 Final Hb.
1.2
1.2. Analysis
Comparison 1 CERA versus other ESA, Outcome 2 All‐cause mortality.
1.3
1.3. Analysis
Comparison 1 CERA versus other ESA, Outcome 3 Number of adverse events due to hypertension.
1.4
1.4. Analysis
Comparison 1 CERA versus other ESA, Outcome 4 Transfusions.
1.5
1.5. Analysis
Comparison 1 CERA versus other ESA, Outcome 5 Number of adverse events due to access thrombosis.
2.1
2.1. Analysis
Comparison 2 CERA frequencies, Outcome 1 Final haemoglobin.
2.2
2.2. Analysis
Comparison 2 CERA frequencies, Outcome 2 All‐cause mortality.
2.3
2.3. Analysis
Comparison 2 CERA frequencies, Outcome 3 Number of adverse effects due to hypertension.
2.4
2.4. Analysis
Comparison 2 CERA frequencies, Outcome 4 Transfusion.
2.5
2.5. Analysis
Comparison 2 CERA frequencies, Outcome 5 Number of adverse events due to access thrombosis.
3.1
3.1. Analysis
Comparison 3 Darbepoetin every 2 weeks versus once/week, Outcome 1 Final/change in Hb.
3.2
3.2. Analysis
Comparison 3 Darbepoetin every 2 weeks versus once/week, Outcome 2 Final ESA/change in dose.
3.3
3.3. Analysis
Comparison 3 Darbepoetin every 2 weeks versus once/week, Outcome 3 All‐cause‐mortality.
3.4
3.4. Analysis
Comparison 3 Darbepoetin every 2 weeks versus once/week, Outcome 4 Adverse events.
4.1
4.1. Analysis
Comparison 4 Darbepoetin every 2 weeks versus once/month, Outcome 1 Final/change in HB.
4.2
4.2. Analysis
Comparison 4 Darbepoetin every 2 weeks versus once/month, Outcome 2 Adverse events.
5.1
5.1. Analysis
Comparison 5 Darbepoetin versus rHuEPO, Outcome 1 Final/change in Hb.
5.2
5.2. Analysis
Comparison 5 Darbepoetin versus rHuEPO, Outcome 2 Final/change in ESA dose.
5.3
5.3. Analysis
Comparison 5 Darbepoetin versus rHuEPO, Outcome 3 All‐cause mortality.
5.4
5.4. Analysis
Comparison 5 Darbepoetin versus rHuEPO, Outcome 4 Hypertension.
5.5
5.5. Analysis
Comparison 5 Darbepoetin versus rHuEPO, Outcome 5 Transfusion.
5.6
5.6. Analysis
Comparison 5 Darbepoetin versus rHuEPO, Outcome 6 Total treatment‐related adverse events.
5.7
5.7. Analysis
Comparison 5 Darbepoetin versus rHuEPO, Outcome 7 Access thrombosis/vascular complication.
6.1
6.1. Analysis
Comparison 6 rHuEPO once/week versus 2 to 3 times/week, Outcome 1 Final/change in Hb or HCT.
6.2
6.2. Analysis
Comparison 6 rHuEPO once/week versus 2 to 3 times/week, Outcome 2 Final/change in EPO dose.
6.3
6.3. Analysis
Comparison 6 rHuEPO once/week versus 2 to 3 times/week, Outcome 3 Adverse effects.
7.1
7.1. Analysis
Comparison 7 rHuEPO once/week versus every 2 weeks, Outcome 1 Final/change in Hb.
7.2
7.2. Analysis
Comparison 7 rHuEPO once/week versus every 2 weeks, Outcome 2 Final rHuEPO dose.
7.3
7.3. Analysis
Comparison 7 rHuEPO once/week versus every 2 weeks, Outcome 3 Systolic blood pressure.
7.4
7.4. Analysis
Comparison 7 rHuEPO once/week versus every 2 weeks, Outcome 4 Diastolic blood pressure.
8.1
8.1. Analysis
Comparison 8 rHuEPO daily versus weekly, Outcome 1 Final Hb.
8.2
8.2. Analysis
Comparison 8 rHuEPO daily versus weekly, Outcome 2 Final/change in EPO dose.
See this image and copyright information in PMC

Update of

Comment in

References

References to studies included in this review

AMICUS Study 2007 {published data only}
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BA16286 Study 2007 {published data only}
    1. Dougherty FC, Beyer U. No changes in blood pressure in dialysis patients after 12 months of treatment with IV/SC CERA (Continuous Erythropoietin Receptor Activator) [abstract no: W‐PO40131]. Nephrology 2005;10(Suppl 1):A313‐4. [CENTRAL: CN‐00602138]
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    1. Dougherty FC, Loghman‐Adham M, Schultze N, Beyer U. Adequate hemoglobin levels are maintained with continuous erythropoietin receptor activator (CERA) in dialysis patients regardless of gender, age, race and diabetic status [abstract no: MP206]. Nephrology Dialysis Transplantation 2005;20(Suppl 5):v269. [CENTRAL: CN‐00602143]
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Brahm 1999 {published data only}
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Canaud 1995 {published data only}
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Carrera 2003 {published data only}
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Frifelt 1996 {published data only}
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Hori 2004 {published data only}
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Kwan 2005 {published data only}
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Lago 1996 {published data only}
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Lee 2008 {published data only}
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Leung 1995 {published data only}
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Locatelli 2002 {published data only}
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Locatelli 2004 {published data only}
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    1. Locatelli F, Villa G, Backs W, Pino MD. Aranesp® (darbepoetin alfa) maintains hemoglobin (Hb) levels in hemodialysis (HD) patients at extended dosing intervals regardless of previous recombinant human erythropoietin (rHuEPO) dosing frequency. [abstract no: PUB254]. Journal of the American Society of Nephrology 2004;15(Oct):816A.
Lui 1991 {published data only}
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Lui 1992 {published data only}
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MAXIMA Study 2007 {published data only}
    1. Barany P, Besarab A, Macdougall IC, Law A, Ouyang Y, Heifets M. Median hemoglobin (Hb) decline following C.E.R.A. dose interruption is similar to that with other erythropoiesis stimulating agents (ESAs) [abstract no: SU‐PO795]. Journal of the American Society of Nephrology 2007;18(Abstracts Issue):760A. [CENTRAL: CN‐00794522]
    1. Chanu P, Gieschke R, Reigner B, Dougherty FC. Pharmacokinetic parameters of C.E.R.A. and are not affected by age in patients with chronic kidney disease on dialysis [abstract no: SaP351]. Nephrology Dialysis Transplantation 2007;22(Suppl 6):vi351. [CENTRAL: CN‐00757500]
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    1. Fishbane S, Bernardo M, Locatelli F, delAguila M, Edwardes M, Bexon M. Once‐monthly intravenous (IV) C.E.R.A. maintains stable hemoglobin (Hb) in dialysis patients (pts), irrespective of age or gender [abstract no: SU‐PO779]. Journal of the American Society of Nephrology 2007;18(Abstracts Issue):756A. [CENTRAL: CN‐00757405]
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Miranda 1990 {published data only}
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PROTOS Study 2007 {published data only}
    1. Barany P, Besarab A, Macdougall IC, Law A, Ouyang Y, Heifets M. Median hemoglobin (Hb) decline following C.E.R.A. dose interruption is similar to that with other erythropoiesis stimulating agents (ESAs) [abstract no: SU‐PO795]. Journal of the American Society of Nephrology 2007;18(Abstracts Issue):760A. [CENTRAL: CN‐00794522]
    1. Chanu P, Gieschke R, Reigner B, Dougherty FC. Pharmacokinetic parameters of C.E.R.A. and are not affected by age in patients with chronic kidney disease on dialysis [abstract no: SaP351]. Nephrology Dialysis Transplantation 2007;22(Suppl 6):vi351. [CENTRAL: CN‐00757500]
    1. Chanu P, Gieschke R, Reigner B, Dougherty FC. Pharmacokinetics of C.E.R.A. and stable maintenance of haemoglobin (Hb) levels with once‐monthly dosing in patients with chronic kidney disease (CKD) [abstract no: SaP325]. Nephrology Dialysis Transplantation 2007;22(Suppl 6):vi342. [CENTRAL: CN‐00757502]
    1. Fishbane S, Dalton C, Beswick R, Dutka P, Schmidt R. Efficacy of C.E.R.A., a continuous erythropoietin receptor activator, in the treatment of renal anemia: overview of 6 global phase 3 trials [abstract no: 59]. American Journal of Kidney Diseases 2007;49(4):A39. [CENTRAL: CN‐00756571]
    1. Imbasciati E, Bernardo M, Caraman P, David‐Neto E, Harris K, Law A, et al. Stable haemoglobin (Hb) levels are maintained with once‐monthly C.E.R.A. in dialysis patients with varying C‐reactive protein (CRP), albumin or dialysis adequacy [abstract no: SuO005]. Nephrology Dialysis Transplantation 2007;22(Suppl 6):vi412. [CENTRAL: CN‐00758076]
RUBRA Study 2008 {published data only}
    1. Barany P, Besarab A, Macdougall IC, Law A, Ouyang Y, Heifets M. Median hemoglobin (Hb) decline following C.E.R.A. dose interruption is similar to that with other erythropoiesis stimulating agents (ESAs) [abstract no: SU‐PO795]. Journal of the American Society of Nephrology 2007;18(Abstracts Issue):760A. [CENTRAL: CN‐00794522]
    1. Fishbane S, Dalton C, Beswick R, Dutka P, Schmidt R. Efficacy of C.E.R.A., a continuous erythropoietin receptor activator, in the treatment of renal anemia: overview of 6 global phase 3 trials [abstract no: 59]. American Journal of Kidney Diseases 2007;49(4):A39. [CENTRAL: CN‐00756571]
    1. Spinowitz B, Coyne DW, Fraticelli M, Azer M, Dalal S, Villa G, et al. CERA (continuous erythropoietin receptor activator) administered once every 2 weeks via pre‐filled syringe (PFS) maintains stable Hb levels in patients with CKD on dialysis [abstract no: PUB376]. Journal of the American Society of Nephrology 2006;17(Abstracts):895A. [CENTRAL: CN‐00653773]
    1. Spinowitz B, Coyne DW, Lok CE, Fraticelli M, Azer M, Dalal S, et al. CERA maintains stable control of hemoglobin in patients with chronic kidney disease on dialysis when administered once every two weeks. American Journal of Nephrology 2008;28(2):280‐9. [MEDLINE: ] - PubMed
STRIATA Study 2008 {published data only}
    1. Barany P, Besarab A, Macdougall IC, Law A, Ouyang Y, Heifets M. Median hemoglobin (Hb) decline following C.E.R.A. dose interruption is similar to that with other erythropoiesis stimulating agents (ESAs) [abstract no: SU‐PO795]. Journal of the American Society of Nephrology 2007;18(Abstracts Issue):760A. [CENTRAL: CN‐00794522]
    1. Canaud B, Braun J, Locatelli F, Villa G, Vlem B, Sanz Guajardo D, et al. Intravenous (IV) C.E.R.A. (continuous erythropoietin receptor activator) administered once every 2 weeks maintains stable haemoglobin (Hb) levels in patients with chronic kidney disease (CKD) on dialysis [abstract no: SP425]. Nephrology Dialysis Transplantation 2006;21(Suppl 4):iv157. [CENTRAL: CN‐00690645]
    1. Canaud B, Mingardi G, Braun J, Aljama P, Kerr PG, Locatelli F, et al. Intravenous C.E.R.A. maintains stable haemoglobin levels in patients on dialysis previously treated with darbepoetin alfa: results from STRIATA, a randomized phase III study. Nephrology Dialysis Transplantation 2008;23(11):3654‐61. [MEDLINE: ] - PMC - PubMed
    1. Fishbane S, Dalton C, Beswick R, Dutka P, Schmidt R. Efficacy of C.E.R.A., a continuous erythropoietin receptor activator, in the treatment of renal anemia: overview of 6 global phase 3 trials [abstract no: 59]. American Journal of Kidney Diseases 2007;49(4):A39. [CENTRAL: CN‐00756571]
Tessitore 2008 {published data only}
    1. Tessitore N, Mantovani W, Bedogna V, Loss R, Melilli E, Poli A, et al. Cost analysis of switching from epoetin alfa to darbepoetin alfa in chronic hemodialysis patients (HD Pts): a long‐term, randomized, open‐label, cross‐over, pilot study [abstract no: SA‐PO2645]. Journal of the American Society of Nephrology 2008;19(Abstracts Issue):706A. [CENTRAL: SA‐PO2645]
Vanrenterghem 2002 {published data only}
    1. Canaud B. Darbepoetin alfa dose requirements for IV and SC administration are equivalent in anaemic dialysis patients [abstract no: M319]. Nephrology Dialysis Transplantation 2002;17(Suppl 1):137. [CENTRAL: CN‐00550478]
    1. Kerr PG, Harris D, Hawley C, Walker R, European/Australian NESP 970290 Study Group. Novel erythropoiesis stimulating protein (NESP) maintains haemoglobin in ESRD patients with administered once weekly or once every other week [abstract no: 181]. Nephrology 2000;5(3):A112. [CENTRAL: CN‐00509271]
    1. Vanrenterghem Y, Barany P, Mann J, European/Australian NESP 970290 Study Group. Novel erythropoiesis stimulating protein (NESP) maintains hemoglobin (hgb) in ESRD patients when administered once weekly or once every other week [abstract]. Journal of the American Society of Nephrology 1999;10(Program & Abstracts):270A. [CENTRAL: CN‐00583820]
    1. Vanrenterghem Y, Barany P, Mann JF, Kerr PG, Wilson J, Baker NF, et al. Randomized trial of darbepoetin alfa for treatment of renal anemia at a reduced dose frequency compared with rHuEPO in dialysis patients. Kidney International 2002;62(6):2167‐75. [MEDLINE: ] - PubMed
Weiss 2000 {published data only}
    1. Weiss L, Svensson B, Clyne N, Devino J, Frisenette‐Fich C, Kurkus J. Is subcutaneous (s.c.) erythropoietin (EPO) administered once a week for stable hemodialysis (HD) patients sufficient? Results from a Swedish multicenter trial. [abstract no: A1099]. Journal of the American Society of Nephrology 1996;7(9):1468‐9. [CENTRAL: CN‐00583180]
    1. Weiss LG, Clyne N, Divino Fihlho J, Frisenette‐Fich C, Kurkus J, Svensson B. The efficacy of once weekly compared with two or three times weekly subcutaneous epoetin beta: results from a randomized controlled multicentre trial. Swedish Study Group. Nephrology Dialysis Transplantation 2000;15(12):2014‐9. [MEDLINE: ] - PubMed
Yoon 2004 {published data only}
    1. Yoon SY, Bang BK, Kim SG, Han DC, Hwang SD, Park JS, et al. Randomized, controlled trial of darbepoetin alfa for the treatment of renal anemia in hemodialysis patients [abstract no: MP271]. 41st Congress. European Renal Association. European Dialysis and Transplantation Association; 2004 May 15‐18; Lisbon, Portugal. 2004:322. [CENTRAL: CN‐00509573]

References to studies excluded from this review

Allon 2002 {published data only}
    1. Allon M, Kleinman AK, Walczyk M, Kaupke C, Maroni BJ, Heatherington A, et al. The pharmacokinetics of novel erythropoiesis stimulating protein (NESP) following chronic intravenous administration is time‐and dose‐linear [abstract no: A1308]. Journal of the American Society of Nephrology 2000;11(Sept):248A. [CENTRAL: CN‐00626053]
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BA16260 Study 2006 {published data only}
    1. Francisco AL, Sulowicz W, Dougherty FC. Subcutaneous CERA (continuous erythropoiesis receptor activator) has potent erythropoietic activity in dialysis patients with chronic renal anemia: an exploratory multiple‐dose study [abstract]. Journal of the American Society of Nephrology 2003;14(Nov):27A‐8A. [CENTRAL: CN‐00550366]
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Bennett 1991 {published data only}
    1. Bennett WM. A multicenter clinical trial of epoetin beta for anemia of end‐stage renal disease. Journal of the American Society of Nephrology 1991;1(7):990‐8. [MEDLINE: ] - PubMed
Besarab 1998 {published data only}
    1. Besarab A, Bolton WK, Browne JK, Egrie JC, Nissenson AR, Okamoto DM, et al. The effects of normal as compared with low hematocrit values in patients with cardiac disease who are receiving hemodialysis and epoetin. New England Journal of Medicine 1998;339(9):584‐90. [MEDLINE: ] - PubMed
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Bhuiyan 2004 {published data only}
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Brandt 1999 {published data only}
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Brown 1988 {published data only}
    1. Brown CD, Kieran M, Dosunmu BV, Zhao Z, Larson RH, Friedman EA. Raised hematocrit (HCT) persists six‐weeks after stopping treatment with human recombinant erythropoietin (r‐HuEPO) in azotemic anemic patients [abstract]. Kidney International 1988;33(1):184. [CENTRAL: CN‐00602117]
Canadian EPO Study 1990 {published data only}
    1. Anonymous. Effect of recombinant human erythropoietin therapy on blood pressure in hemodialysis patients. Canadian Erythropoietin Study Group. American Journal of Nephrology 1991;11(1):23‐6. [MEDLINE: ] - PubMed
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    1. Canadian Erythropoietin Study Group. The clinical effects and side‐effects of recombinant human erythropoietin (EPO) in anaemic patients on chronic hemodialysis [abstract]. Kidney International 1990;37(1):278. [CENTRAL: CN‐00583134]
    1. Keown PA. Quality of life in end‐stage renal disease patients during recombinant human erythropoietin therapy. The Canadian Erythropoietin Study Group. Contributions to Nephrology 1991;88:81‐9. [MEDLINE: ] - PubMed
Castro 1994 {published data only}
    1. Castro MC, Abensur H, Centeno JR, Romao Jr JE, Marcondes M, Sabbaga E. Comparison between thrice‐weekly intravenous and once‐weekly subcutaneous administration of rHuEPO in hemodialysis patients. Dialysis & Transplantation 1994;23(3):132‐43. [EMBASE: 1994307692]
Chazot 2009 {published data only}
    1. Chazot C, Dumoulin A, Ang KS, Paul GJ, Bernard C, Conference Medicale Group. Haemodialysis patients under subcutaneous recombinant human erythropoietin can be directly switched to intravenous Aranesp® [abstract no: F‐PO682]. Journal of the American Society of Nephrology 2005;16:483A. [CENTRAL: CN‐00740583]
    1. Chazot C, Terrat JC, Ang K, Gassia JP, Chedid K, Maurice F, et al. Intravenous darbepoetin A maintains hemoglobin level in hemodialysis patients converting from subcutaneous recombinant human erythropoietin [abstract no: F‐PO501]. Journal of the American Society of Nephrology 2004;15(Oct):177A. [CENTRAL: CN‐00583168]
    1. Chazot C, Terrat JC, Dumoulin A, Ang KS, Gassia JP, Chedid K, et al. Randomized equivalence study evaluating the possibility of switching hemodialysis patients receiving subcutaneous human erythropoietin directly to intravenous darbepoetin alfa. Annals of Pharmacotherapy 2009;43(2):228‐34. [MEDLINE: ] - PubMed
Dougherty 2004 {published data only}
    1. Dougherty FC, Reigner B, Beyer U. Dose‐dependent erythropoietic responses to subcutaneous CERA (continuous erythropoiesis receptor activator) in multiple‐dose study of dialysis patients with chronic renal anaemia [abstract]. 41st Congress. European Renal Association. European Dialysis and Transplantation Association; 2004 May 15‐18; Lisbon, Portugal. 2004:325. [CENTRAL: CN‐00509162]
Fan 1992 {published data only}
    1. Fan CD, Tsang KK, Wong CM, Chang HC. Therapeutic evaluation of once versus thrice weekly subcutaneous (sc) application of low dose recombinant human erythropoietin (rHuEPO) in hemodialysis patients [abstract]. 9th Asian Colloquium in Nephrology; 1992 May 17‐21; Seoul, Korea. 1992:184. [CENTRAL: CN‐00460720]
Hirakata 2010 {published data only}
    1. Hirakata H, Gejyo F, Suzuki M, Saito A, Lino Y, Watanabe Y, et al. Effect of darbepoetin alfa (KRN321) subcutaneous treatment on hemoglobin levels, health‐related QOL (HRQOL) and left ventricular mass index (LVMI) in patients with chronic kidney disease (CKD) not on dialysis [abstract no: SA‐PO204]. Journal of the American Society of Nephrology 2006;17(Abstracts):618A. [CENTRAL: CN‐00740524]
    1. Hirakata H, Tsubakihara Y, Gejyo F, Nishi S, Iino Y, Watanabe Y, et al. Maintaining high hemoglobin levels improved the left ventricular mass index and quality of life scores in pre‐dialysis Japanese chronic kidney disease patients. Clinical & Experimental Nephrology 2010;14(1):28‐35. [MEDLINE: ] - PubMed
    1. Inaguma D, Tsubakihara Y, Hirakata H, Hiroe M, Hada Y, Akizawa T, et al. Monthly subcutaneous treatment of darbepoetin alfa (KRN321) could maintain higher Hb safely and have beneficial effects on cardiac function of Japanese CKD patients not on dialysis [abstract no: SaP353]. Nephrology Dialysis Transplantation 2007;22(Suppl 6):vi352. [CENTRAL: CN‐00740573]
    1. Suzuki M, Hada Y, Akaishi M, Hiroe M, Aonuma K, Tsubakihara Y, et al. Effects of anemia correction by erythropoiesis‐stimulating agents on cardiovascular function in non‐dialysis patients with chronic kidney disease. International Heart Journal 2012;53(4):238‐43. [MEDLINE: ] - PubMed
Icardi 1990 {published data only}
    1. Icardi A, Paoletti E, Molinelli G. Efficacy of recombinant erythropoietin after subcutaneous or intraperitoneal administration to patients on CAPD. Advances in Peritoneal Dialysis 1990;6:292‐5. [MEDLINE: ] - PubMed
Ifudu 1998 {published data only}
    1. Ifudu O, Dawood M, Homel P. Erythropoietin‐induced elevation in blood pressure is immediate and dose dependent. Nephron 1998;79(4):486‐7. [MEDLINE: ] - PubMed
Iwasaki 2008 {published data only}
    1. Iwasaki T, Kimata N, Sugi O, Sawara Y, Jinnai H, Kikuchi K, et al. Difference in reactivity became more evident by changing of the erythropoiesis‐stimulating agent (ESA) [abstract no: PUB462]. Journal of the American Society of Nephrology 2008;19(Abstracts Issue):914A. [CENTRAL: CN‐00792600]
Kawanishi 2005 {published data only}
    1. Kawanishi H, Iwasaki M, Akizawa T, Koshikawa S, KRN321 SG. Dose‐finding and long‐term studies of intravenous KRN321 (darbepoetin alfa) in chronic renal failure patients (CRF) on hemodialysis (HD) in Japan [abstract no: SA‐PO943]. Journal of the American Society of Nephrology 2005;16:763A. [CENTRAL: CN‐00740571]
Kim 2009a {published data only}
    1. Kim CD, Park SH, Kim DJ, Do JY, Shin SK, Kim BS, et al. Randomized trial to compare the dosage of darbepoetin alfa by administration route in hemodialysis patient [abstract no: TH‐PO370]. Journal of the American Society of Nephrology 2006;17(Abstracts):185A. [CENTRAL: CN‐00740537] - PubMed
    1. Kim CD, Park SH, Kim DJ, Park JW, Do JY, Shin SK, et al. Randomized trial to compare the dosage of darbepoetin alfa by administration route in haemodialysis patients. Nephrology 2009;14(5):482‐7. [MEDLINE: ] - PubMed
Knebel 2008 {published data only}
    1. Knebel W, Palmen M, Dowell JA, Gastonguay M. Population pharmacokinetic modeling of epoetin delta in pediatric patients with chronic kidney disease. Journal of Clinical Pharmacology 2008 Jul;48(7):837‐48. [MEDLINE: ] - PubMed
Locatelli 2008 {published data only}
    1. Locatelli F, Villa G, Messa P, Filippini A, Cannella G, Ferrari G, et al. Efficacy and safety of once‐weekly intravenous epoetin alfa in maintaining hemoglobin levels in hemodialysis patients. Journal of Nephrology 2008;21(3):412‐20. [MEDLINE: ] - PubMed
Macdougall 2003 {published data only}
    1. Macdougall IC. Novel erythropoiesis stimulating protein (NESP) for the treatment of anaemia in ESRD patients [abstract]. 37th Congress. European Renal Association. European Dialysis and Transplantation Association. European Kidney Research Organisation; 2000 Sept 17‐20; Nice, France. 2000:237. [CENTRAL: CN‐00461229]
    1. Macdougall IC. Novel erythropoiesis stimulating protein (NESP) for the treatment of anaemia in ESRD patients [abstract]. Nephrology Dialysis Transplantation 2000;15(9):A160.
    1. Macdougall IC, Matcham J, Gray SJ, NESP Study Group. Correction of anaemia with darbepoetin alfa in patients with chronic kidney disease receiving dialysis. Nephrology Dialysis Transplantation 2003 Mar;18(3):576‐81. [MEDLINE: ] - PubMed
    1. Macdougall IC, UK NESP Study Group. Novel erythropoiesis stimulating protein (NESP) for the treatment of renal anaemia [abstract]. Journal of the American Society of Nephrology 1998;9(Program & Abstracts):258A‐9A. [CENTRAL: CN‐00446518]
Macdougall 2006 {published data only}
    1. Macdougall IC, Reigner B, Dougherty FC. Consistent pharmacokinetic properties of CERA (Continuous Erythropoietin Receptor Activator) in healthy volunteers and in patients with CKD [abstract no: 89]. American Journal of Kidney Diseases 2006;47(4):A41. [CENTRAL: CN‐00583919]
    1. Macdougall IC, Robson R, Opatrna S, Liogier X, Pannier A, Jordan P, et al. Pharmacokinetics and Pharmacodynamics of Intravenous and Subcutaneous Continuous Erythropoietin Receptor Activator (C.E.R.A.) in Patients with Chronic Kidney Disease. Clinical Journal of The American Society of Nephrology: CJASN 2006;1(6):1211‐5. [MEDLINE: ] - PubMed
    1. Macdougall IC, Robson R, Opatrna S, Liogier X, Pannier A, Reigner B, et al. Pharmacologic profile of CERA (continuous erythropoietin receptor activator) in chronic kidney disease (CKD) patients (pts) following intravenous (IV) and subcutaneous (SC) administration [abstract no: SA‐PO926]. Journal of the American Society of Nephrology 2005;16:759A. [CENTRAL: CN‐00795029] - PubMed
Macdougall 2007a {published data only}
    1. Macdougall IC, Ruiz EF. Extending dosing regimens with epoetin delta: a randomized controlled trial [abstract no: SU‐PO785]. Journal of the American Society of Nephrology 2007;18(Abstracts Issue):758A. [CENTRAL: CN‐00765131]
Martin 2007 {published data only}
    1. Martin KJ. Epoetin delta for the management of renal anemia: a one year study [abstract no: TH‐PO374]. Journal of the American Society of Nephrology 2006;17(Abstracts):186A. [CENTRAL: CN‐00765049]
    1. Martin KJ. The first human cell line‐derived erythropoietin, epoetin‐delta (Dynepo), in the management of anemia in patients with chronic kidney disease. Clinical Nephrology 2007;68(1):26‐31. [MEDLINE: ] - PubMed
    1. Martin KJ, ED3001 Study Group. Epoetin delta in the management of renal anaemia: results of a 6‐month study. Nephrology Dialysis Transplantation 2007;22(10):3052‐4. [MEDLINE: ] - PubMed
Moiz 2000 {published data only}
    1. Moiz B, Hashmi KZ, Yazdani I. Erythropoietin induced hypertension. Journal of the College of Physicians & Surgeons Pakistan 2000;10(9):317‐20. [EMBASE: 2000359629]
Muirhead 1992 {published data only}
    1. Muirhead N. Changes in quality of life in chronic renal failure patients treated with recombinant human erythropoietin [abstract]. 9th Asian Colloquium in Nephrology; 1992 May 17‐21; Seoul, Korea. 1992:45‐6. [CENTRAL: CN‐00461371]
Nissenson 1995 {published data only}
    1. Nissenson AR, Korbet S, Faber M, Burkart J, Gentile D, Hamburger R, et al. Multicenter trial of erythropoietin in patients on peritoneal dialysis. Journal of the American Society of Nephrology 1995;5(7):1517‐29. [MEDLINE: ] - PubMed
Parfrey 2005 {published data only}
    1. Foley RN, Curtis BM, Parfrey PS. Erythropoietin therapy, hemoglobin targets, and quality of life in healthy hemodialysis patients: a randomized trial. Clinical Journal of the American Society of Nephrology: CJASN 2009;4(4):726‐33. [MEDLINE: ] - PMC - PubMed
    1. Foley RN, Curtis BM, Parfrey PS. Hemoglobin targets and blood transfusions in hemodialysis patients without symptomatic cardiac disease receiving erythropoietin therapy. Clinical Journal of the American Society of Nephrology: CJASN 2008;3(6):1669‐75. [MEDLINE: ] - PMC - PubMed
    1. Foley RN, Curtis BM, Parfrey PS. Hemoglobin targets, blood transfusions and quality of life in hemodialysis patients without symptomatic cardiac disease [abstract no: SA‐PO2745]. Journal of the American Society of Nephrology 2008;19(Abstracts Issue):730A. [CENTRAL: CN‐00756852] - PMC - PubMed
    1. Foley RN, Curtis BM, Randell EW, Parfrey PS. Left ventricular hypertrophy in new hemodialysis patients without symptomatic cardiac disease. Clinical Journal of the American Society of Nephrology: CJASN 2010;5(5):805‐13. [MEDLINE: ] - PMC - PubMed
    1. Foley RN, Parfrey PS, Wittreich BH, Sullivan DJ, Zagari MJ, Frei D, et al. The effect of higher haemoglobin levels on left ventricular vacity volume in patients starting haemodialysis: a blinded, randomised, controlled trial in 596 patients without symptomatic cardiac disease [abstract]. 41st Congress. European Renal Association. European Dialysis and Transplantation Association; 2004 May 15‐18; Lisbon, Portugal. 2004:217. [CENTRAL: CN‐00509197]
PATRONUS Study 2009 {published data only}
    1. Besarab A, Canaud B, Francisco ALM, Kerr P, Locatelli F, Lok CE, et al. Randomized comparison of IV C.E.R.A. (Continuous Erythropoietin Receptor Activator) and Darbepoetin Alfa (DA) at extended administration intervals for the maintenance of Hb levels in patients with CKD on dialysis: rationale and design [abstract no: PUB377]. Journal of the American Society of Nephrology 2006;17(Abstracts):896A. [CENTRAL: CN‐00740564]
    1. Carrera F. CERA vs darbepoetin alfa as maintenance therapy for anaemia in patients with chronic kidney disease (CKD): The PATRONUS Study [abstract no: M558]. World Congress of Nephrology; 2009 May 22‐26; Milan, Italy. 2009.
    1. Carrera F, Lok CE, Francisco A, Locatelli F, Mann JF, Canaud B, et al. Maintenance treatment of renal anaemia in haemodialysis patients with methoxy polyethylene glycol‐epoetin beta versus darbepoetin alfa administered monthly: a randomized comparative trial. Nephrology Dialysis Transplantation 2010;25(12):4009‐17. [MEDLINE: ] - PMC - PubMed
    1. Locatelli F, PATRONUS Study Group. Once‐monthly C.E.R.A. is superior to darbepoetin alfa for maintaining hemoglobin levels in hemodialysis patients regardless of age, gender, diabetic status or presence of hyperlipidemia [abstract no: SA‐PO2412]. Journal of the American Society of Nephrology 2009;20:663A. [CENTRAL: CN‐00747328]
    1. Mann JF, PATRONUS Study Group. Risk factors for vascular events in hemodialysis patients receiving once‐monthly C.E.R.A. or once‐monthly darbepoetin alfa: post hoc analysis of the PATRONUS Study [abstract no: PUB414]. Journal of the American Society of Nephrology 2009;20:921A. [CENTRAL: CN‐00747329]
Pawlak 2007 {published data only}
    1. Pawlak K, Pawlak D, Mysliwiec M. Long‐term erythropoietin therapy does not affect metalloproteinases and their inhibitor levels, oxidative stress and inflammation in hemodialyzed patients. American Journal of Nephrology 2007;27(3):221‐5. [MEDLINE: ] - PubMed
Provenzano 2006 {published data only}
    1. Provenzano R, Dougherty FC. Subcutaneous (SC) CERA (Continuous Erythropoietin Receptor Activator) administered once every 2 weeks effectively corrects anemia in patients with chronic kidney disease (CKD) on dialysis and not on dialysis [abstract no: 126]. American Journal of Kidney Diseases 2006;47(4):A50. [CENTRAL: CN‐00747315]
Raftery 2000 {published data only}
    1. Raftery MJ, Auinger M, Hertlova M. Safety and tolerability of a multidose formulation of epoetin beta in dialysis patients. Collaborative Study Group. Clinical Nephrology 2000;54(3):240‐5. [MEDLINE: ] - PubMed
Schmitt 2006 {published data only}
    1. Schaefer F, Brummer C, Rosenkranz J, Schmitt CP. Increased subcutaneous injection pain with darbepoetin‐A compared with epoetin‐b in children: results of a randomized, double‐blind study [abstract no: P399]. Pediatric Nephrology 2004;19(9):C191. [CENTRAL: CN‐00740567]
    1. Schmitt CP, Brummer C, Rosenkranz J, Schaefer F. Increased injection pain with darbepoetin‐a compared to epoetin‐b: a double‐blind study in pediatric patients [abstract no: SU‐PO068]. Journal of the American Society of Nephrology 2004;15(Oct):547A. [CENTRAL: CN‐00740568]
    1. Schmitt CP, Brummer C, Rosenkranz J, Schaefer F. Injection pain is increased with darbepoetin‐a compared to epoetin‐b [abstract no: W‐PO40120]. Nephrology 2005;10(Suppl):A311. [CENTRAL: CN‐00740569]
    1. Schmitt CP, Nau B, Brummer C, Rosenkranz J, Schaefer F. Increased injection pain with darbepoetin‐alpha compared to epoetin‐beta in paediatric dialysis patients. Nephrology Dialysis Transplantation 2006;21(12):3520‐4. [MEDLINE: ] - PubMed
Smith 2007 {published data only}
    1. Pratt R. Pharmacokinetics of erythropoietin by a human cell line (Epoetin I): subcutaneous vs intravenous dosing in patients with chronic kidney disease [abstract no: 1137]. Haematologica 2006;91(Suppl 1):414. [CENTRAL: CN‐00716122]
    1. Pratt RD, Dowell J. Pharmacokinetics of epoetin delta: a new erythropoietin produced by gene‐activation in a human cell line [abstract no: TH‐PO378]. Journal of the American Society of Nephrology 2006;17(Abstracts):187A. [CENTRAL: CN‐00644158]
    1. Smith WB, Dowell JA, Pratt RD. Pharmacokinetics and pharmacodynamics of epoetin delta in two studies in healthy volunteers and two studies in patients with chronic kidney disease. Clinical Therapeutics 2007;29(7):1368‐80. [MEDLINE: ] - PubMed
Smyth 2006 {published data only}
    1. Smyth M, Pratt RD. Epoetin delta, erythropoietin produced in a human cell line, is as effective as epoetin alfa in the treatment of anemia [abstract no: 1296]. Blood 2006;108(11):380a. [CENTRAL: CN‐00740519]
Spaia 1995 {published data only}
    1. Spaia S, Gouva H, Petridou P, Kokolou E, Mavropoulou E, Pazarloglu M, et al. Once versus thrice weekly administration of maintenance dose of erythropoietin in haemodialysis patients [abstract]. ISN XIII International Congress of Nephrology; 1995 Jul 2‐6; Madrid, Spain. 1995:508. [CENTRAL: CN‐00509487]
Spinowitz 2006 {published data only}
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References to studies awaiting assessment

EMERALD 1 Study 2013 {published data only}
    1. Besarab A, Schiller B, Macdougall IC, Locatelli F, Wiecek A, Covic A, et al. Comparison of IV and SC peginesatide and epoetin doses in hemodialysis (HD) patients [abstract]. Hemodialysis International 2012;16(1):139‐40. [EMBASE: 70725373]
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EMERALD 2 Study 2013 {published data only}
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References to ongoing studies

NCT00436748 {published data only}
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NCT00717821 {published data only}
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References to other published versions of this review

Cody 2002
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