Erythropoiesis stimulating agents and reno-protection: a meta-analysis

BMC Nephrology

Volumn 18, Issue 1, 2017, Pages 1-16

  Elliott, Steve ^a   Tomita, Dianne ^a   Endre, Zoltan ^b  

^a AMGEN INC   (United States)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

AKI (acute kidney injury); Anemia; Clinical trial; EPO; Erythropoietin; ESA; Meta analysis; Progression of CKD; Reno protection; Tissue protection; Transplant

Indexed keywords

ANTIANEMIC AGENT; CREATININE; HEMOGLOBIN; NOVEL ERYTHROPOIESIS STIMULATING PROTEIN; RECOMBINANT ERYTHROPOIETIN; UREA; URINARY TRACT AGENT;

ACUTE KIDNEY FAILURE; ANEMIA; ARTICLE; CHRONIC KIDNEY FAILURE; CREATININE BLOOD LEVEL; DATA BASE; DELAYED GRAFT FUNCTION; DISEASE COURSE; ESTIMATED GLOMERULAR FILTRATION RATE; GRAFT SURVIVAL; HEMOGLOBIN BLOOD LEVEL; HUMAN; INCIDENCE; KIDNEY FUNCTION; KIDNEY GRAFT; META ANALYSIS; OUTCOME ASSESSMENT; PATIENT RISK; RANDOMIZED CONTROLLED TRIAL (TOPIC); RENAL PROTECTION; RISK REDUCTION; TREATMENT OUTCOME; TREND STUDY; ADULT; AGED; COMORBIDITY; FEMALE; MALE; MIDDLE AGED; PREVALENCE; RISK FACTOR; VERY ELDERLY;

ACUTE KIDNEY INJURY; ADULT; AGED; AGED, 80 AND OVER; ANEMIA; COMORBIDITY; FEMALE; HEMATINICS; HUMANS; MALE; MIDDLE AGED; PREVALENCE; RENAL AGENTS; RISK FACTORS; TREATMENT OUTCOME;

EID: 85009227763     PISSN: None     EISSN: 14712369     Source Type: Journal    
DOI: 10.1186/s12882-017-0438-4     Document Type: Article

References (76)

1. Elliott S, Sinclair AM. The effect of erythropoietin on normal and neoplastic cells. Biologics: Targets Therapy. 2012;6:163-89.
2. Lin FK, Suggs S, Lin CH, Browne JK, Smalling R, Egrie JC, et al. Cloning and expression of the human erythropoietin gene. Proc Natl Acad Sci U S A. 1985;82:7580-4.
3. Sico JJ, Concato J, Wells CK, Lo AC, Nadeau SE, Williams LS, et al. Anemia is associated with poor outcomes in patients with less severe ischemic stroke. J Stroke Cerebrovasc Dis. 2013;22:271-8.
4. Kosiborod M, Smith GL, Radford MJ, Foody JM, Krumholz HM. The prognostic importance of anemia in patients with heart failure. Am J Med. 2003;114:112-9.
5. Abramson JL, Jurkovitz CT, Vaccarino V, Weintraub WS, McClellan W. Chronic kidney disease, anemia, and incident stroke in a middle-aged, community-based population: the ARIC Study. Kidney Int. 2003;64:610-5.
6. 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. Int Heart J. 2012;53:2012.
7. Bahlmann FH, Fliser D. Erythropoietin and renoprotection. Curr Opin Nephrol Hypertens. 2009;18:15-20.
8. Moore E, Bellomo R. Erythropoietin (EPO) in acute kidney injury. Ann Intensive Care. 2011;1:3.
9. Togel FE, Ahlstrom JD, Yang Y, Hu Z, Zhang P, Westenfelder C. Carbamylated Erythropoietin Outperforms Erythropoietin in the Treatment of AKI-on-CKD and Other AKI Models. J Am Soc Nephrol. 2016;27(11):3394-404.
10. Elliott S, Busse L, Swift S, McCaffery I, Rossi J, Kassner P, et al. Lack of expression and function of erythropoietin receptors in the kidney. Nephrol Dial Transplant. 2012;27:2733-45.
11. Choukroun G, Kamar N, Dussol B, Etienne I, Cassuto-Viguier E, Toupance O, et al. Correction of postkidney transplant anemia reduces progression of allograft nephropathy. J Am Soc Nephrol. 2012;23:360-8.
12. Vasquez EM, Pollak R. Effect of pretransplant erythropoietin therapy on renal allograft outcome. Transplantation. 1996;62:1026-8.
13. Linde T, Ekberg H, Forslund T, Furuland H, Holdaas H, Nyberg G, et al. The use of pretransplant erythropoietin to normalize hemoglobin levels has no deleterious effects on renal transplantation outcome. Transplantation. 2001;71:79-82.
14. Lietz K, Lao M, Paczek L, Gorski A, Gaciong Z. The impact of pretransplant erythropoietin therapy on late outcomes of renal transplantation. Ann Transplant. 2003;8:17-24.
15. Fernandez-Lucas M, Marcen R, Villafruela J, Teruel JL, Tato A, Rivera M, et al. Effect of rHuEpo therapy in dialysis patients on endogenous erythropoietin synthesis after renal transplantation. Nephron. 1996;73:54-7.
16. Oh SW, Chin HJ, Chae DW, Na KY. Erythropoietin improves long-term outcomes in patients with acute kidney injury after coronary artery bypass grafting. J Korean Med Sci. 2012;27:506-11.
17. Song YR, Lee T, You SJ, Chin HJ, Chae DW, Lim C, et al. Prevention of acute kidney injury by erythropoietin in patients undergoing coronary artery bypass grafting: a pilot study. Am J Nephrol. 2009;30:253-60.
18. Revicki DA, Brown RE, Feeny DH, Henry D, Teehan BP, Rudnick MR, et al. Health-related quality of life associated with recombinant human erythropoietin therapy for predialysis chronic renal disease patients. Am J Kidney Dis. 1995;25:548-54.
19. Roth D, Smith RD, Schulman G, Steinman TI, Hatch FE, Rudnick MR, et al. Effects of recombinant human erythropoietin on renal function in chronic renal failure predialysis patients. Am J Kidney Dis. 1994;24:777-84.
20. Park J, Gage BF, Vijayan A. Use of EPO in critically ill patients with acute renal failure requiring renal replacement therapy. Am J Kidney Dis. 2005;46:791-8.
21. Olweny EO, Mir SA, Park SK, Tan YK, Faddegon S, Best SL, et al. Intra-operative erythropoietin during laparoscopic partial nephrectomy is not renoprotective. World J Urol. 2012;30:519-24.
22. Jadad AR, Moore RA, Carroll D, Jenkinson C, Reynolds DJ, Gavaghan DJ, et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials. 1996;17:1-12.
23. Kamar N, Reboux A-H, Cointault O, Esposito L, Cardeau-Desangles I, Lavayssiere L, et al. Impact of very early high doses of recombinant erythropoietin on anemia and allograft function in de novo kidney-transplant patients. Transpl Int. 2010;23:277-84.
24. Dardashti A, Ederoth P, Algotsson L, Bronden B, Grins E, Larsson M, et al. Erythropoietin and protection of renal function in cardiac surgery (the EPRICS Trial). Anesthesiology. 2014;121:582-90.
25. De SS, Ponte B, Weiss L, Pugin J, Romand JA, Martin P-Y, et al. Epoetin administrated after cardiac surgery: Effects on renal function and inflammation in a randomized controlled study. BMC Nephrol. 2012;13:132.
26. Endre ZH, Walker RJ, Pickering JW, Shaw GM, Frampton CM, Henderson SJ, et al. Early intervention with erythropoietin does not affect the outcome of acute kidney injury (the EARLYARF trial). Kidney Int. 2010;77:1020-30.
27. Kim J-H, Shim J-K, Song J-W, Song Y, Kim H-B, Kwak Y-L. Effect of erythropoietin on the incidence of acute kidney injury following complex valvular heart surgery: A double blind, randomized clinical trial of efficacy and safety. Crit Care. 2013;17:R254.
28. Tasanarong A, Duangchana S, Sumransurp S, Homvises B, Satdhabudha O. Prophylaxis with erythropoietin versus placebo reduces acute kidney injury and neutrophil gelatinase-associated lipocalin in patients undergoing cardiac surgery: A randomized, double-blind controlled trial. BMC Nephrol. 2013;14:136.
29. Yoo Y-C, Shim J-K, Kim J-C, Jo Y-Y, Lee J-H, Kwak Y-L. Effect of single recombinant human erythropoietin injection on transfusion requirements in preoperatively anemic patients undergoing valvular heart surgery. Anesthesiology. 2011;115:929-37.
30. Coupes B, de Freitas DG, Roberts S, Read I, Riad H, Brenchley PE, et al. rhErythropoietin-b as a tissue protective agent in kidney transplantation: a pilot randomized controlled trial. BMC Res Notes. 2015;8:1.
31. Aydin Z, Mallat MJK, Schaapherder AFM, van Zonneveld AJ, Van KC, Rabelink TJ, et al. Randomized trial of short-course high-dose erythropoietin in donation after cardiac death kidney transplant recipients. Am J Transplant. 2012;12(7):1793-800.
32. Hafer C, Becker T, Kielstein JT, Bahlmann E, Schwarz A, Grinzoff N, et al. High-dose erythropoietin has no effect on short-or long-term graft function following deceased donor kidney transplantation. Kidney Int. 2012;81:314-20.
33. Martinez F, Kamar N, Pallet N, Lang P, Durrbach A, Lebranchu Y, et al. High dose epoetin beta in the first weeks following renal transplantation and delayed graft function: Results of the Neo-PDGF study: Brief communication. Am J Transplant. 2010;10:1704-9.
34. Sureshkumar KK, Hussain SM, Ko TY, Thai NL, Marcus RJ. Effect of high-dose erythropoietin on graft function after kidney transplantation: A randomized, double-blind clinical trial. Clin J Am Soc Nephrol. 2012;7:1498-506.
35. Van Biesen W, Vanholder R, Veys N, Verbeke F, Lameire N. Efficacy of erythropoietin administration in the treatment of anemia immediately after renal transplantation. Transplantation. 2005;79:367-8.
36. Van Loo A, Vanholder R, Bernaert P, Deroose J, Lameire N. Recombinant human erythropoietin corrects anaemia during the first weeks after renal transplantation - a randomized prospective study. Nephrol Dial Transplant. 1996;11:1815-21.
37. Siedlecki A, Irish W, Brennan DC. Delayed graft function in the kidney transplant. Am J Transplant. 2011;11:2279-96.
38. Abraham PA, Opsahl JA, Rachael KM, Asinger R, Halstenson CE. Renal function during erythropoietin therapy for anemia in predialysis chronic renal failure patients. Am J Nephrol. 1990;10:128-36.
39. Clyne N, Jogestrand T. Effect of erythropoietin treatment on physical exercise capacity and on renal function in predialytic uremic patients. Nephron. 1992;60:390-6.
40. Kleinman KS, Schweitzer SU, Perdue ST, Bleifer KH, Abels RI. The use of recombinant human erythropoietin in the correction of anemia in predialysis patients and its effect on renal function: a double-blind, placebo-controlled trial. Am J Kidney Dis. 1989;14:486-95.
41. Kuriyama S, Tomonari H, Yoshida H, Hashimoto T, Kawaguchi Y, Sakai O. Reversal of anemia by erythropoietin therapy retards the progression of chronic renal failure, especially in nondiabetic patients. Nephron. 1997;77:176-85.
42. Lim VS, DeGowin RL, Zavala D, Kirchner PT, Abels R, Perry P, et al. Recombinant human erythropoietin treatment in pre-dialysis patients. A double-blind placebo-controlled trial. Ann Intern Med. 1989;110:108-14.
43. Lim VS, Fangman J, Flanigan MJ, DeGowin RL, Abels RT. Effect of recombinant human erythropoietin on renal function in humans. Kidney Int. 1990;37:131-6.
44. Akizawa T, Gejyo F, Nishi S, Iino Y, Watanabe Y, Suzuki M, et al. Positive outcomes of high hemoglobin target in patients with chronic kidney disease not on dialysis: a randomized controlled study. Ther Apher Dial. 2011;15:431-40.
45. Cianciaruso B, Ravani P, Barrett BJ, Levin A, ITA EPO. Italian randomized trial of hemoglobin maintenance to prevent or delay left ventricular hypertrophy in chronic kidney disease. J Nephrol. 2008;21:861-70.
46. Drueke TB, Locatelli F, Clyne N, Eckardt KU, Macdougall IC, Tsakiris D, et al. Normalization of hemoglobin level in patients with chronic kidney disease and anemia. N Engl J Med. 2006;355:2071-84.
47. Gouva C, Nikolopoulos P, Ioannidis JP, Siamopoulos KC. Treating anemia early in renal failure patients slows the decline of renal function: a randomized controlled trial. Kidney Int. 2004;66:753-60.
48. Levin A, Djurdjev O, Thompson C, Barrett B, Ethier J, Carlisle E, et al. Canadian randomized trial of hemoglobin maintenance to prevent or delay left ventricular mass growth in patients with CKD. Am J Kidney Dis. 2005;46:799-811.
49. Macdougall IC, Temple RM, Kwan JT. Is early treatment of anaemia with epoetin-alpha beneficial to pre-dialysis chronic kidney disease patients? Results of a multicentre, open-label, prospective, randomized, comparative group trial. Nephrol Dial Transplant. 2007;22:784-93.
50. Pfeffer MA, Burdmann EA, Chen CY, Cooper ME, de Zeeuw D, Eckardt KU, et al. A Trial of Darbepoetin Alfa in Type 2 Diabetes and Chronic Kidney Disease. N Engl J Med. 2009;361:2019-32.
51. Ritz E, Laville M, Bilous RW, O’Donoghue D, Scherhag A, Burger U, et al. Target level for hemoglobin correction in patients with diabetes and CKD: primary results of the Anemia Correction in Diabetes (ACORD) Study.[Erratum appears in Am J Kidney Dis. 2007 Apr;49(4):562]. Am J Kidney Dis. 2007;49:194-207.
52. Roger SD, McMahon LP, Clarkson A, Disney A, Harris D, Hawley C, et al. Effects of early and late intervention with epoetin alpha on left ventricular mass among patients with chronic kidney disease (stage 3 or 4): results of a randomized clinical trial. J Am Soc Nephrol. 2004;15:148-56.
53. Rossert J, Levin A, Roger SD, Horl WH, Fouqueray B, Gassmann-Mayer C, et al. Effect of early correction of anemia on the progression of CKD. Am J Kidney Dis. 2006;47:738-50.
54. Singh AK, Szczech L, Tang KL, Barnhart H, Sapp S, Wolfson M, et al. Correction of anemia with epoetin alfa in chronic kidney disease. N Engl J Med. 2006;355:2085-98.
55. Villar E, Lievre M, Kessler M, Lemaitre V, Alamartine E, Rodier M, et al. Anemia normalization in patients with type 2 diabetes and chronic kidney disease: results of the NEPHRODIAB2 randomized trial. J Diabetes Complications. 2011;25:237-43.
56. Chhabra D, Grafals M, Skaro AI, Parker M, Gallon L. Impact of anemia after renal transplantation on patient and graft survival and on rate of acute rejection. Clin J Am Soc Nephrol. 2008;3:1168-74.
57. Kamar N, Rostaing L. Negative impact of one-year anemia on long-term patient and graft survival in kidney transplant patients receiving calcineurin inhibitors and mycophenolate mofetil. Transplantation. 2008;85:1120-4.
58. Tie HT, Luo MZ, Lin D, Zhang M, Wan JY, Wu QC. Erythropoietin administration for prevention of cardiac surgery-associated acute kidney injury: a meta-analysis of randomized controlled trials. Eur J Cardiothorac Surg. 2015;48:32-9.
59. Cody J, Daly C, Campbell M, Donaldson C, Khan I, Rabindranath K, et al. Recombinant human erythropoietin for chronic renal failure anaemia in pre-dialysis patients. Cochrane Database Syst Rev. 2005;20(3):CD003266.
60. Palmer SC, Navaneethan SD, Craig JC, Johnson DW, Tonelli M, Garg AX, et al. Meta-analysis: erythropoiesis-stimulating agents in patients with chronic kidney disease. Ann Intern Med. 2010;153:23-33.
61. Covic A, Nistor I, Donciu M-D, Dumea R, Bolignano D, Goldsmith D. Erythropoiesis-stimulating agents (ESA) for preventing the progression of chronic kidney disease: A meta-analysis of 19 studies. Am J Nephrol. 2014;40:13.
62. Koulouridis I, Alfayez M, Trikalinos TA, Balk EM, Jaber BL. Dose of Erythropoiesis-Stimulating Agents and Adverse Outcomes in CKD: A Metaregression Analysis. Am J Kidney Dis. 2013;61:44-56.
63. Solling C. Organ-protective and immunomodulatory effects of erythropoietin - an update on recent clinical trials. Basic Clin Pharmacol Toxicol. 2012;110:113-21.
64. Li J, Xu H, Gao Q, Wen Y. Effect of erythropoiesis-stimulating agents in acute ST-segment elevation myocardial infarction: a systematic review. Eur J Clin Pharmacol. 2012;68:469-77.
65. Wen Y, Xu J, Ma X, Gao Q. High-dose erythropoietin in acute ST-segment elevation myocardial infarction: A meta-analysis of randomized controlled trials. Am J Cardiovasc Drugs. 2013;13:435-42.
66. Desai A, Lewis E, Solomon S, McMurray JJV, Pfeffer M. Impact of erythropoiesis-stimulating agents on morbidity and mortality in patients with heart failure: An updated, post-TREAT meta-analysis. Eur J Heart Fail. 2010;12:936-42.
67. Ohlsson A, Aher SM. Early erythropoietin for preventing red blood cell transfusion in preterm and/or low birth weight infants. Cochrane Database Syst Rev. 2014;4:CD004863.
68. Robertson CS, Hannay HJ, Yamal JM, Gopinath S, Goodman JC, Tilley BC, et al. Effect of erythropoietin and transfusion threshold on neurological recovery after traumatic brain injury: a randomized clinical trial. JAMA. 2014;312:36-47.
69. Nichol A, French C, Little L, Haddad S, Presneill J, Arabi Y, et al. Erythropoietin in traumatic brain injury (EPO-TBI): a double-blind randomised controlled trial. Lancet. 2015;386:2499-506.
70. Ehrenreich H, Weissenborn K, Prange H, Schneider D, Weimar C, Wartenberg K, et al. Recombinant human erythropoietin in the treatment of acute ischemic stroke. Stroke. 2009;40:e647-56.
71. Uzu T, Kida Y, Yamauchi A, Kume S, Isshiki K, Araki S, et al. The effects of blood pressure control levels on the renoprotection of type 2 diabetic patients without overt proteinuria. J Am Soc Hypertens. 2012;6:124-31.
72. Imai E, Ito S, Haneda M, Harada A, Kobayashi F, Yamasaki T, et al. Effects of blood pressure on renal and cardiovascular outcomes in Asian patients with type 2 diabetes and overt nephropathy: a post hoc analysis (ORIENT-blood pressure). Nephrol Dial Transplant. 2016;31:447-54.
73. Ruggenenti P, Perna A, Loriga G, Ganeva M, Ene-Iordache B, Turturro M, et al. Blood-pressure control for renoprotection in patients with non-diabetic chronic renal disease (REIN-2): multicentre, randomised controlled trial. Lancet. 2005;365:939-46.
74. Sinclair AM, Coxon A, McCaffery I, Kaufman S, Paweletz K, Liu L, et al. Functional erythropoietin receptor is undetectable in endothelial, cardiac, neuronal, and renal cells. Blood. 2010;115:4264-72.
75. Elliott S, Busse L, Bass MB, Lu H, Sarosi I, Sinclair AM, et al. Anti-Epo receptor antibodies do not predict Epo receptor expression. Blood. 2006;107:1892-5.
76. DeSeigneux S, Ponte B, Weiss L, Pugin J, Romand JA, Martin P-Y, et al. Epoetin administrated after cardiac surgery: Effects on renal function and inflammation in a randomized controlled study. BMC Nephrol. 2012;13:132.