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Review

Cardiovascular safety of current and emerging drugs to treat anaemia in chronic kidney disease: a safety review

, &
Pages 1179-1191 | Received 22 Jun 2023, Accepted 16 Nov 2023, Published online: 18 Dec 2023

References

  • Go AS, Chertow GM, Fan D, et al. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med. 2004;351(13):1296–1305. doi: 10.1056/NEJMoa041031
  • Lanser L, Fuchs D, Scharnagl H, et al. Anemia of chronic disease in patients with cardiovascular disease. Front Cardiovasc Med. 2021;8:666638. doi: 10.3389/fcvm.2021.666638
  • Coresh J, Astor B, Sarnak MJ. Evidence for increased cardiovascular disease risk in patients with chronic kidney disease. Curr Opin Nephrol Hypertens. 2004;13(1):73–81. doi: 10.1097/00041552-200401000-00011
  • Elliott S, Pham E, Macdougall IC. Erythropoietins: a common mechanism of action. Exp Hematol. 2008;36(12):1573–1584. doi: 10.1016/j.exphem.2008.08.003
  • Lin CS, Lim SK, D’Agati V, et al. Differential effects of an erythropoietin receptor gene disruption on primitive and definitive erythropoiesis. Genes Dev. 1996;10(2):154–164. doi: 10.1101/gad.10.2.154
  • Darnell JE, Kerr IM, Stark G. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science. 1994;264:1415–1420. doi: 10.1126/science.8197455
  • Becker V, Schilling M, Bachmann J, et al. Covering a broad dynamic range: information processing at the erythropoietin receptor. Science. 2010;328(5984):1404–1408. doi: 10.1126/science.1184913
  • Janmaat ML, Heerkens JL, de Bruin AM, et al. Erythropoietin accelerates smooth muscle cell-rich vascular lesion formation in mice through endothelial cell activation involving enhanced PDGF-BB release. Blood. 2010;115:1453–1460. doi: 10.1182/blood-2009-07-230870
  • Ammarguellat F, Llovera M, Kelly PA, et al. Low doses of EPO activate MAP kinases but not JAK2-STAT5 in rat vascular smooth muscle cells. Biochem Biophys Res Commun. 2001;284(4):1031–1038. doi: 10.1006/bbrc.2001.5085
  • Ashley RA, Dubuque SH, Dvorak B, et al. Erythropoietin stimulates vasculogenesis in neonatal rat mesenteric microvascular endothelial cells. Pediatr Res. 2002;51(4):472–478. doi: 10.1203/00006450-200204000-00012
  • Wang XQ, Vaziri ND. Erythropoietin depresses nitric oxide synthase expression by human endothelial cells. Hypertension. 1999;33(3):894–899. doi: 10.1161/01.HYP.33.3.894
  • Larivière R, Lebel M. Endothelin‐1 in chronic renal failure and hypertension. Can J Physiol Pharmacol. 2003;81(6):607–621. doi: 10.1139/y03-012
  • Agarwal R. Mechanisms and mediators of hypertension induced by erythropoietin and related molecules. Nephrol Dial Transplant. 2018;33(10):1690–1698. doi: 10.1093/ndt/gfx324
  • Lee MS, Lee JS, Lee JY. Prevention of erythropoietin-associated hypertension. Hypertension. 2007;50(2):439–445. doi: 10.1161/HYPERTENSIONAHA.107.090423
  • Beleslin-Cokic BB, Cokic VP, Yu X, et al. Erythropoietin and hypoxia stimulate erythropoietin receptor and nitric oxide production by endothelial cells. Blood. 2004;104(7):2073–2080. doi: 10.1182/blood-2004-02-0744
  • Fraser JK, Tan AS, Lin FK, et al. Expression of specific high-affinity binding sites for erythropoietin on rat and mouse megakaryocytes. Exp Hematol. 1989;17(1):10–16.
  • Vaziri ND. Thrombocytosis in EPO-treated dialysis patients may be mediated by EPO rather than iron deficiency. Am J Kidney Dis. 2009;53(5):733–736. doi: 10.1053/j.ajkd.2008.12.030
  • Kadikoylu G, Yavasoglu I, Bolaman Z, et al. Platelet parameters in women with iron deficiency anemia. J Natl Med Assoc. 2006;98:398–402.
  • Demetz G, Laux M, Scherhag A, et al. The influence of erythropoietin on platelet activation, thrombin generation and FVII/active FVII in patients with AMI. Thromb J. 2014;12(1):18. doi: 10.1186/1477-9560-12-18
  • Ruifrok WP, de Boer RA, Westenbrink BD, et al. Erythropoietin in cardiac disease: new features of an old drug. Eur J Pharmacol. 2008;585(2–3):270–277. doi: 10.1016/j.ejphar.2008.01.054
  • Klopsch C, Furlani D, Gäbel R, et al. Intracardiac injection of erythropoietin induces stem cell recruitment and improves cardiac functions in a rat myocardial infarction model. J Cell Mol Med. 2009;13(4):664–679. doi: 10.1111/j.1582-4934.2008.00546.x
  • Fiordaliso F, Chimenti S, Staszewsky L, et al. A nonerythropoietic derivative of erythropoietin protects the myocardium from ischemia-reperfusion injury. Proc Natl Acad Sci U S A. 2005;102(6):2046–2051. doi: 10.1073/pnas.0409329102
  • Westenbrink BD, Oeseburg H, Kleijn L, et al. Erythropoietin stimulates normal endothelial progenitor cell-mediated endothelial turnover, but attributes to neovascularization only in the presence of local ischemia. Cardiovasc Drugs Ther. 2008;22(4):265–274. doi: 10.1007/s10557-008-6094-y
  • Kanellakis P, Pomilio G, Agrotis A, et al. Darbepoetin-mediated cardioprotection after myocardial infarction involves multiple mechanisms independent of erythropoietin receptor-common beta-chain heteroreceptor. Br J Pharmacol. 2010;160(8):2085–2096. doi: 10.1111/j.1476-5381.2010.00876.x
  • Carraway MS, Suliman HB, Jones WS, et al. Erythropoietin activates mitochondrial biogenesis and couples red cell mass to mitochondrial mass in the heart. Circ Res. 2010;106(11):1722–1730. doi: 10.1161/CIRCRESAHA.109.214353
  • Benjanuwattra J, Apaijai N, Chunchai T, et al. The temporal impact of erythropoietin administration on mitochondrial function and dynamics in cardiac ischemia/reperfusion injury. Exp Mol Pathol. 2022;127:104802. doi: 10.1016/j.yexmp.2022.104802
  • Zuo L, Li DD, Ma XX, et al. Erythropoietin promotes myocardial infarction repair in mice by improving the function of Sca-1+ stem cells. Sheng Li Xue Bao. 2023;75(1):36–48.
  • Baker JE, Kozik D, Hsu AK, et al. Darbepoetin alfa protects the rat heart against infarction: dose-response, phase of action and mechanisms. J Cardiovasc Pharmacol. 2007;49:337–345. doi: 10.1097/FJC.0b013e318040cf81
  • Yamada M, Burke C, Colditz P, et al. Erythropoietin protects against apoptosis and increases expression of non-neuronal cell markers in the hypoxia-injured developing brain. J Pathol. 2011;224(1):101–109. doi: 10.1002/path.2862
  • Cherian L, Goodman JC, Robertson C. Improved cerebrovascular function and reduced histological damage with darbepoietin alfa administration after cortical impact injury in rats. J Pharmacol Exp Ther. 2011;337(2):451–456. doi: 10.1124/jpet.110.176602
  • Juenemann M, Braun T, Schleicher N, et al. Neuroprotective mechanisms of erythropoietin in a rat stroke model. Transl Neurosci. 2020;11(1):48–59. doi: 10.1515/tnsci-2020-0008
  • Lee ST, Chu K, Park JE, et al. Erythropoietin improves memory function with reducing endothelial dysfunction and amyloid-beta burden in Alzheimer’s disease models. J Neurochem. 2012;120(1):115–124. doi: 10.1111/j.1471-4159.2011.07534.x
  • Yan W, Guo T, Liu N, et al. Erythropoietin ameliorates cognitive deficits by improving hippocampal and synaptic damage in streptozotocin-induced diabetic mice. Cell Signal. 2023;106:110614. doi: 10.1016/j.cellsig.2023.110614
  • Xu G, Zou T, Deng L, et al. Nonerythropoietic erythropoietin mimetic peptide ARA290 ameliorates chronic stress-induced depression-like behavior and inflammation in mice. Front Pharmacol. 2022;13:896601. doi: 10.3389/fphar.2022.896601
  • Strippoli GF, Craig JC, Manno C, et al. Hemoglobin targets for the anemia of chronic kidney disease: a meta-analysis of randomized, controlled trials. J Am Soc Nephrol. 2004;15(12):3154–3165. doi: 10.1097/01.ASN.0000145436.09176.A7
  • Parfrey PS, Lauve M, Latremouille-Viau D, et al. Erythropoietin therapy and left ventricular mass index in CKD and ESRD patients: a meta-analysis. Clin J Am Soc Nephrol. 2009;4(4):755–762. doi: 10.2215/CJN.02730608
  • Besarab A, Bolton WK, Browne JK, et al. The effects of normal as compared with low hematocrit values in patients with cardiac disease who are receiving hemodialysis and epoetin. N Engl J Med. 1998;339(9):584–590. doi: 10.1056/NEJM199808273390903
  • Singh AK, Szczech L, Tang KL, et al. CHOIR investigators. Correction of anemia with epoetin alfa in chronic kidney disease. N Engl J Med. 2006;355(20):2085–2098. doi: 10.1056/NEJMoa065485
  • Drüeke TB, Locatelli F, Clyne N, et al. CREATE investigators. Normalization of hemoglobin level in patients with chronic kidney disease and anemia. N Engl J Med. 2006;355(20):2071–2084. doi: 10.1056/NEJMoa062276
  • Pfeffer MA, Burdmann EA, Chen CY, et al. TREAT investigators. A trial of darbepoetin alfa in type 2 diabetes and chronic kidney disease. N Engl J Med. 2009;361(21):2019–2032. doi: 10.1056/NEJMoa0907845
  • Szczech LA, Barnhart HX, Inrig JK, et al. Secondary analysis of the CHOIR trial epoetin-alpha dose and achieved hemoglobin outcomes. Kidney Int. 2008;74(6):791–798. doi: 10.1038/ki.2008.295
  • RED-HF Committees, Swedberg K, Young JB, et al. RED-HF investigators. Treatment of anemia with darbepoetin alfa in systolic heart failure. N Engl J Med. 2013;368(13):1210–1219.
  • Skali H, Parving HH, Parfrey PS, et al. TREAT investigators. Stroke in patients with type 2 diabetes mellitus, chronic kidney disease, and anemia treated with Darbepoetin Alfa: the trial to reduce cardiovascular events with Aranesp therapy (TREAT) experience. Circulation. 2011;124(25):2903–2908. doi: 10.1161/CIRCULATIONAHA.111.030411
  • Parfrey PS, Foley RN, Wittreich BH, et al. Double-blind comparison of full and partial anemia correction in incident hemodialysis patients without symptomatic heart disease. J Am Soc Nephrol. 2005;16(7):2180–2189. doi: 10.1681/ASN.2004121039
  • Chung EY, Palmer SC, Saglimbene VM, et al. Erythropoiesis-stimulating agents for anaemia in adults with chronic kidney disease: a network meta-analysis. Cochrane Database Syst Rev. 2023;2(2). CD010590. doi: 10.1002/14651858.CD010590.pub3
  • KDOQI NKF. KDOQI clinical practice guidelines and clinical practice recommendations for anemia in chronic kidney disease. Am J Kidney Dis. 2006;47(5 Suppl 3):S11–145.
  • Wish JB. Erythropoiesis-stimulating agent hyporesponsiveness and adverse outcomes: guilty as charged? Kidney Med. 2020;2(5):526–528. doi: 10.1016/j.xkme.2020.08.002
  • Luo J, Jensen DE, Maroni BJ, et al. Spectrum and burden of erythropoiesis-stimulating agent hyporesponsiveness among contemporary hemodialysis patients. Am J Kidney Dis. 2016;68(5):763–771. doi: 10.1053/j.ajkd.2016.05.031
  • Ogawa T, Nitta K. Erythropoiesis-stimulating agent hyporesponsiveness in end-stage renal disease patients. Contrib Nephrol. 2015;185:76–86.
  • Solomon SD, Uno H, Lewis EF, et al. Trial to reduce cardiovascular events with aranesp therapy (TREAT) investigators. Erythropoietic response and outcomes in kidney disease and type 2 diabetes. N Engl J Med. 2010;363(12):1146–1155. doi: 10.1056/NEJMoa1005109
  • Kim T, Streja E, Soohoo M, et al. Serum ferritin variations and mortality in incident hemodialysis patients. Am J Nephrol. 2017;46(2):120–130. doi: 10.1159/000478735
  • Narita I, Hayashi T, Maruyama S, et al. Hyporesponsiveness to erythropoiesis-stimulating agent in non-dialysis-dependent CKD patients: the BRIGHTEN study. PLoS One. 2022;17(11):e0277921. doi: 10.1371/journal.pone.0277921
  • Cizman B, Smith HT, Camejo RR, et al. Clinical and Economic Outcomes of Erythropoiesis-Stimulating Agent Hyporesponsiveness in the Post-Bundling Era. Kidney Med. 2020;2(5):589–599. doi: 10.1016/j.xkme.2020.06.008
  • Sibbel SP, Koro CE, Brunelli SM, et al. Characterization of chronic and acute ESA hyporesponse: a retrospective cohort study of hemodialysis patients. BMC Nephrol. 2015;16(1):144. doi: 10.1186/s12882-015-0138-x
  • El-Komy MH, Schmidt RL, Widness JA, et al. Differential pharmacokinetic analysis of in vivo erythropoietin receptor interaction with erythropoietin and continuous erythropoietin receptor activator in sheep. Biopharm Drug Dispos. 2011;32(5):276–288. doi: 10.1002/bdd.757
  • Wilhelm-Leen ER, Winkelmayer WC. Mortality risk of darbepoetin alfa versus epoetin alfa in patients with CKD: systematic review and meta-analysis. Am J Kidney Dis. 2015;66(1):69–74. doi: 10.1053/j.ajkd.2014.12.012
  • Sakaguchi Y, Hamano T, Wada A, et al. Types of erythropoietin-stimulating agents and mortality among patients undergoing hemodialysis. J Am Soc Nephrol. 2019;30(6):1037–1048. doi: 10.1681/ASN.2018101007
  • Karaboyas A, Port FK, Massy ZA, et al. Long- versus short-acting erythropoiesis-stimulating agent type and mortality. Kidney Int Rep. 2021;6(1):214–218. doi: 10.1016/j.ekir.2020.10.003
  • Locatelli F, Hannedouche T, Fishbane S, et al. Cardiovascular safety and all-cause mortality of methoxy polyethylene glycol-epoetin beta and other erythropoiesis-stimulating agents in anemia of CKD: a randomized noninferiority trial. Clin J Am Soc Nephrol. 2019;14(12):1701–1710. doi: 10.2215/CJN.01380219
  • Minutolo R, Garofalo C, Chiodini P, et al. Types of erythropoiesis-stimulating agents and risk of end-stage kidney disease and death in patients with non-dialysis chronic kidney disease. Nephrol Dial Transplant. 2021;36(2):267–274. doi: 10.1093/ndt/gfaa088
  • Kidney Disease: Improving Global Outcomes (KDIGO) Anemia Work Group. KDIGO clinical practice guideline for anemia in chronic kidney disease. Kidney Int Suppl. 2012;2:279–335.
  • Locatelli F, Bárány P, Covic A, et al. ERA-EDTA ERBP Advisory Board. Kidney Disease: Improving Global Outcomes guidelines on anaemia management in chronic kidney disease: a European Renal Best Practice position statement. Nephrol Dial Transplant. 2013;28(6):1346–1359. doi: 10.1093/ndt/gft033
  • Heikkilä M, Pasanen A, Kivirikko KI, et al. Roles of the human hypoxia-inducible factor (HIF)-3α variants in the hypoxia response. Cell Mol Life Sci. 2011;68(23):3885–3901. doi: 10.1007/s00018-011-0679-5
  • Chan Tak MD, Pecoits-Filho R, Rastogi A, et al. Roxadustat vs. placebo or epoetin alfa has no clinically meaningful effect on blood pressure in patients with anemia of CKD. [PO2114] Abstract presented at the 2020 Kidney Week, American Society of Nephrology ASN 2020
  • Semenza GL. Hypoxia-inducible factors in physiology and medicine. Cell. 2012;148(3):399–408. doi: 10.1016/j.cell.2012.01.021
  • Yu T, Tang B, Sun X. Development of inhibitors targeting hypoxia-inducible factor 1 and 2 for cancer therapy. Yonsei Med J. 2017;58(3):489–496. doi: 10.3349/ymj.2017.58.3.489
  • Ong SG, Hausenloy DJ. Hypoxia-inducible factor as a therapeutic target for cardioprotection. Pharmacol Ther. 2012;136(1):69–81. doi: 10.1016/j.pharmthera.2012.07.005
  • Wei H, Bedja D, Koitabashi N, et al. Endothelial expression of hypoxia-inducible factor 1 protects the murine heart and aorta from pressure overload by suppression of TGF-beta signaling. Proc Natl Acad Sci, USA. 2012;109:E841–E850. doi: 10.1073/pnas.1202081109
  • Rahtu-Korpela L, Määttä J, Dimova EY, et al. Hypoxia-inducible factor prolyl 4-hydroxylase-2 inhibition protects against development of atherosclerosis. Arterioscler Thromb Vasc Biol. 2016;36(4):608–617. doi: 10.1161/ATVBAHA.115.307136
  • Villa-Roel N, Ryu K, Gu L, et al. Hypoxia inducible factor 1α inhibitor PX-478 reduces atherosclerosis in mice. Atherosclerosis. 2022;344:20–30. doi: 10.1016/j.atherosclerosis.2022.01.002
  • Liu D, Lei L, Desir M, et al. Smooth muscle hypoxia-inducible factor 1α links intravascular pressure and atherosclerosis–brief report. Arterioscler Thromb Vasc Biol. 2016;36:442–445. doi: 10.1161/ATVBAHA.115.306861
  • Christoph M, Pfluecke C, Mensch M, et al. Myeloid PHD2 deficiency accelerates neointima formation via Hif-1α. Mol Immunol. 2022 Sep;149:48–58.
  • Aarup A, Pedersen TX, Junker N, et al. Hypoxia-inducible factor-1α expression in macrophages promotes development of atherosclerosis. Arterioscler Thromb Vasc Biol. 2016;36:1782–1790.
  • Janaszak-Jasiecka A, Siekierzycka A, Płoska A, et al. Endothelial dysfunction driven by hypoxia-the influence of oxygen deficiency on NO bioavailability. Biomolecules. 2021;11(7):982. doi: 10.3390/biom11070982
  • Lambden S, Cowburn AS, Macias D, et al. Endothelial cell regulation of systemic haemodynamics and metabolism acts through the HIF transcription factors. Intensive Care Med Exp. 2021;9(1):28. doi: 10.1186/s40635-021-00390-y
  • Abdi Sarabi M, Shiri A, Aghapour M, et al. Normoxic HIF-1α stabilization caused by local inflammatory factors and its consequences in human coronary artery endothelial cells. Cells. 2022;11(23):3878. doi: 10.3390/cells11233878
  • Querfeld U, Mak RH, Pries AR. Microvascular disease in chronic kidney disease: the base of the iceberg in cardiovascular comorbidity. Clin Sci (Lond). 2020;134(12):1333–1356. doi: 10.1042/CS20200279
  • Tóth A, Csiki DM, B N Jr, et al. Daprodustat accelerates high phosphate-induced calcification through the activation of HIF-1 signaling. Front Pharmacol. 2022;13:798053. doi: 10.3389/fphar.2022.798053.
  • Wang S, Zhao L, Liu H, et al. Lanthanum hydroxide inhibits vascular calcification by regulating the HIF-1 pathway. Cell Biol Int. 2022;46(8):1275–1187. doi: 10.1002/cbin.11811
  • Gupta N, Zhao YY, Evans CE. The stimulation of thrombosis by hypoxia. Thromb Res. 2019 Sep;181:77–83. doi: 10.1016/j.thromres.2019.07.013
  • Zhao J, Xu Y, Xie J, et al. Roxadustat does not affect platelet production, activation, and thrombosis formation. Arterioscler Thromb Vasc Biol. 2021;41(10):2523–2537. doi: 10.1161/ATVBAHA.121.316495
  • Gu W, Qi J, Zhang S, et al. Inhibition of hypoxia-inducible factor prolyl-hydroxylase modulates platelet function. Thromb Haemost. 2022;122(10):1693–1705. doi: 10.1055/a-1837-7797
  • Barratt J, Andric B, Tataradze A, et al. Roxadustat for the treatment of anaemia in chronic kidney disease patients not on dialysis: a phase 3, randomized, open-label, active-controlled study (DOLOMITES). Nephrol Dial Transplant. 2021;36(9):1616–1628. doi: 10.1093/ndt/gfab191
  • Chertow GM, Pergola PE, Farag YMK, et al. PRO2TECT Study Group. Vadadustat in patients with anemia and non-dialysis-dependent CKD. N Engl J Med. 2021;384(17):1589–1600. doi: 10.1056/NEJMoa2035938
  • Singh AK, Carroll K, McMurray JJV, et al. ASCEND-ND Study Group. Daprodustat for the treatment of anemia in patients not undergoing dialysis. N Engl J Med. 2021;385(25):2313–2124. doi: 10.1056/NEJMoa2113380.
  • Provenzano R, Szczech L, Leong R, et al. Efficacy and cardiovascular safety of roxadustat for treatment of anemia in patients with non-dialysis-dependent CKD: pooled results of three randomized clinical trials. Clin J Am Soc Nephrol. 2021;16(8):1190–1200. doi: 10.2215/CJN.16191020
  • Barratt J, Dellanna F, Portoles J, et al. Safety of roxadustat versus erythropoiesis-stimulating agents in patients with anemia of non-dialysis-dependent or incident-to-dialysis chronic kidney disease: pooled analysis of four phase 3 studies. Adv Ther. 2023;40(4):1546–1559. doi: 10.1007/s12325-023-02433-0
  • Eckardt KU, Agarwal R, Aswad A, et al. Safety and efficacy of vadadustat for anemia in patients undergoing dialysis. N Engl J Med. 2021;384(17):1601–1612. doi: 10.1056/NEJMoa2025956
  • Locatelli F, Del Vecchio L, Elliott S. The anaemia treatment journey of CKD patients: from epoetins to hypoxia-inducible factor– prolyl hydroxylase inhibitors (HIF-PHIs). Nephrol Dial Transplant 2023. Accepted for publication
  • Singh AK, Carroll K, Carroll K et al. ASCEND-D Study Group. Daprodustat for the treatment of anemia in patients undergoing dialysis. N Engl J Med. 2021;385(25):2325–2335.
  • Petrie MC, Jhund PS, Connolly E, et al. PIVOTAL investigators and committees. High-dose intravenous iron reduces myocardial infarction in patients on haemodialysis. Cardiovasc Res. 2023;119(1):213–220. doi: 10.1093/cvr/cvab317
  • Joharapurkar AA, Patel VJ, Kshirsagar SG, et al. Prolyl hydroxylase inhibitor desidustat improves anemia in erythropoietin hyporesponsive state. Curr Res Pharmacol Drug Discov. 2022;3:100102. doi: 10.1016/j.crphar.2022.100102
  • Barratt J, Sulowicz W, Schömig M, et al. Efficacy and cardiovascular safety of roxadustat in dialysis-dependent chronic kidney disease: pooled analysis of four phase 3 studies. Adv Ther. 2021;38(10):5345–5360. doi: 10.1007/s12325-021-01903-7
  • Fatima K, Ahmed W, Fatimi AS, et al. Evaluating the safety and efficacy of daprodustat for anemia of chronic kidney disease: a meta-analysis of randomized clinical trials. Eur J Clin Pharmacol. 2022;78(12):1867–1875. doi: 10.1007/s00228-022-03395-y
  • Mark PB, Jhund PS, Walters MR, et al. PIVOTAL investigators. Stroke in hemodialysis patients randomized to different intravenous iron strategies: a prespecified analysis from the PIVOTAL trial. Kidney360. 2021;2(11):1761–1769. doi: 10.34067/KID.0004272021
  • Macdougall IC, White C, Anker SD, et al. PIVOTAL investigators and committees. Intravenous iron in patients undergoing maintenance hemodialysis. N Engl J Med. 2019;380(5):447–458. doi: 10.1056/NEJMoa1810742
  • Ku E, Del Vecchio L, Eckardt KU, et al.; for Conference Participants. Novel anemia therapies in chronic kidney disease: conclusions from a kidney disease: improving Global outcomes (KDIGO) Controversies Conference. Kidney Int. 2023 May 24;104(4):655–680. Epub ahead of print doi: 10.1016/j.kint.2023.05.009
  • Tokuyama A, Kadoya H, Obata A, et al. Roxadustat and thyroid-stimulating hormone suppression. Clin Kidney J. 2021;14(5):1472–1474. doi: 10.1093/ckj/sfab007
  • Chen H, Cheng Q, Wang J, et al. Long-term efficacy and safety of hypoxia-inducible factor prolyl hydroxylase inhibitors in anaemia of chronic kidney disease: a meta-analysis including 13,146 patients. J Clin Pharm Ther. 2021;46(4):999–1009. doi: 10.1111/jcpt.13385
  • Singh AK, Causland FRM, Claggett BL, et al. Analysis of on-treatment cancer safety events with daprodustat versus conventional erythropoiesis-stimulating agents - post hoc analyses of the ASCEND-ND and ASCEN-D trials. Nephrol Dial Transplant. 2023;38(8):1890–1897. doi: 10.1093/ndt/gfac342

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