Burden of anemia in kidney transplant patients: Epidemiology, pathophysiology, and management

Keywords: anemia, kidney transplantation, erythropoietin, iron deficiencies, sodium-glucose transporter 2 inhibitors, graft rejection, graft survival, quality of life.

Abstract

Anemia following kidney transplantation (KTx) is a prevalent complication that adversely affects allograft function, graft survival, and patient survival. Its etiology is multifactorial, encompassing general causes of anemia and KTx-specific factors, such as immunosuppression and reduced erythropoietin production. Management primarily involves iron supplementation and erythropoiesis-stimulating agents (ESAs); however, specific guidelines for post-KTx anemia are lacking, and the optimal methods for treating iron deficiency in KTx recipients remain undefined. Emerging evidence suggests that sodium-glucose cotransporter-2 inhibitors may improve hemoglobin and hematocrit levels in patients with chronic kidney disease and KTx recipients.

To review recent advances in the pathogenesis, epidemiology, treatment, and outcomes of post-KTx anemia, we conducted a literature search using PubMed, Google Scholar, and Google, with keywords including "anemia in kidney transplantation," "anemia etiology in KTx recipients," "iron deficiency in renal transplantation," and "short- and long-term effects of anemia in KTx recipients."

This review synthesizes evidence indicating that effective management of post-KTx anemia, through ESAs and supplementation of erythropoiesis essentials (iron, folate, vitamin B12), is safe and may confer renoprotective benefits. Targeted anemia correction enhances quality of life, reduces mortality, improves transplanted kidney function, and lowers the risk of graft rejection, underscoring the need for standardized treatment protocols.

Downloads

Download data is not yet available.

Author Biography

Amnna Rayani, Tripoli Children Hospital, Tripoli University, Tripoli, Libya

The institute is Open Libyan University/TCH

References

Fraser SDS, Roderick PJ. Kidney disease in the Global Burden of Disease Study 2017. Nat Rev Nephrol 2019;15:193–194. https://doi.org/10.1038/s41581-019-0120-0.

Kovesdy CP. Epidemiology of chronic kidney disease: an update 2022. Kidney Int Suppl (2011). 2022;12(1):7-11. doi: 10.1016/j.kisu.2021.11.003.

Okoro RN, Farate VT. The use of nephrotoxic drugs in patients with chronic kidney disease. Int J Clin Pharm. 2019;41(3):767-775. doi: 10.1007/s11096-019-00811-9.

Nwose EU, Obianke J, Richards RS, Bwitit PT, Igumbor EO. Prevalence and correlations of hepatorenal functions in diabetes and cardiovascular disease among stratified adults. Acta Biomed. 2019;90(1):97-103. doi: 10.23750/abm.v90i1.6576.

Liyanage T, Ninomiya T, Jha V, Neal B, Patrice HM, Okpechi I, Zhao MH, et al. Worldwide access to treatment for end-stage kidney disease: a systematic review. Lancet. 2015;385(9981):1975-82. doi: 10.1016/S0140-6736(14)61601-9.

Tonelli M, Nkunu V, Varghese C, Abu-Alfa AK, Alrukhaimi MN, Fox L, et al. Framework for establishing integrated kidney care programs in low- and middle-income countries. Kidney Int Suppl (2011).2020 ;10(1):e19-e23. doi: 10.1016/j.kisu.2019.11.002.

Davidson B, Du Toit T, Jones ESW, Barday Z, Manning K, Mc Curdie F, et al. Outcomes and challenges of a kidney transplant programme at Groote Schuur Hospital, Cape Town: A South African perspective. PLoS One. 2019;14(1):e0211189. doi: 10.1371/journal.pone.0211189.

Mudiayi D, Shojai S, Okpechi I, Christie EA, Wen K, Kamaleldin M, et al. Global Estimates of Capacity for Kidney Transplantation in World Countries and Regions. Transplantation. 2022;106(6):1113-1122. doi: 10.1097/TP.0000000000003943.

Kasiske BL, Vazquez MA, Harmon WE, Brown RS, Danovitch GM, Gaston RS, et al. Recommendations for the outpatient surveillance of renal transplant recipients. American Society of Transplantation. Recommendations for the outpatient surveillance of renal transplant recipients. J Am Soc Nephrol. 2000:11 Suppl 15:S1-86.

Habas E Sr, Al Adab A, Arryes M, Alfitori G, Farfar K, Habas AM, et al. Anemia and Hypoxia Impact on Chronic Kidney Disease Onset and Progression: Review and Updates. Cureus. 2023;15(10):e46737. doi: 10.7759/cureus.46737.

Bonomini M, Del Vecchio L, Sirolli V, Locatelli F. New treatment approaches for the anemia of CKD. Am J Kidney Dis. 2016;67(1):133–142. doi: 10.1053/j.ajkd.2015.06.030.

Gafter-Gvili A, Ayalon-Dangur I, Cooper L, Shochat T, Rahamimov R, Gafter U, et al. Post-transplantation anemia in kidney transplant recipients: a retrospective cohort study. Medicine. 2017;96(32):e7735. doi: 10.1097/MD.0000000000007735.

Schechter A, Gafter-Gvili A, Shepshelovich D, Rahamimov R, Gafter U, Mor E, et al. Post renal transplantation anemia: causes, severity and their association with graft and patient survival. BMC Nephrol. 2019;20(1):51. doi: 10.1186/s12882-019-1244-y.

Malyszko J, Basak G, Batko K, Capasso G, Capasso A, Drozd-Sokolowska J, et al. Haematological disorders following kidney transplantation. Nephrol Dial Transplant. 2022;37(3):409–20. doi: 10.1093/ndt/gfaa219.

Molina M, Sorolla C, Samsó E, Carcaña M, Martín ML, Jatem E, et al. Quality of life in long-term renal transplant patients: a controversial subject. Transplant Proc. 2022;54(1):91–93. doi: 10.1016/j.transproceed.2021.11.025.

Bonomini M, Di Liberato L, Sirolli V. Treatment Options for Anemia in Kidney Transplant Patients: A Review. Kidney Med. 2023;5(8):100681. doi: 10.1016/j.xkme.2023.100681.

Gafter-Gvili A, Cohen E, Avni T, Grossman A, Vidal L, Garty M, et al Predicting the emergence of anemia—A large cohort study. Eur J Intern Med. 2015;26(5):338–43. doi: 10.1016/j.ejim.2015.04.010.

Lorenz M, Kletzmayr J, Perschl A, Furrer A, Hörl WH, Sunder-Plassmann G. Anemia and iron deficiencies among long-term renal transplant recipients. J Am Soc Nephrol. 2002;13(3):794-797. doi: 10.1681/ASN.V133794.

Huang Z, Song T, Fu L, Rao Z, Zeng D, Qiu Y, Wang X, et al. Post-renal transplantation anemia at 12 months: prevalence, risk factors, and impact on clinical outcomes. Int Urol Nephrol. 2015;47(9):1577-85. doi: 10.1007/s11255-015-1069-y.

Vanrenterghem Y, Ponticelli C, Morales JM, Abramowicz D, Baboolal K, Eklund B, et al. Prevalence and management of anemia in renal transplant recipients: a European survey. Am J Transplant. 2003;3(7):835–45. doi: 10.1034/j.1600-6143.2003.00133.x.

Garrigue V, Szwarc I, Giral M, Soulillou JP, Legendre C, Kreis H, et al Influence of anemia on patient and graft survival after renal transplantation: results from the French DIVAT cohort. Transplantation. 2014;97(2):168–75. doi: 10.1097/TP.0b013e3182a94a4d.

Tang Y, Guo J, Zhou J, Wan Z, Li J, Qiu T. Risk factors and current state of therapy for anemia after kidney transplantation. Front Med (Lausanne). 2024;10:1170100. doi: 10.3389/fmed.2023.1170100.

Goldsmith D, Al-Khoury S, Shah N, Covic A. Anemia after renal transplantation—role of immunosuppressive drugs and a pathophysiological appraisal. Nephron Clin Pract. 2006;104:c69–74. doi: 10.1159/000093992.

Huang G, Wu LW, Yang SC, Fei JG, Deng SX, Li J, Chen GD, et al. Factors Influencing Graft Outcomes Following Diagnosis of Polyomavirus -Associated Nephropathy after Renal Transplantation. PLoS One. 2015;10(11):e0142460. doi: 10.1371/journal.pone.0142460.

Mekraksakit P, Leelaviwat N, Benjanuwattra J, Duangkham S, Del Rio-Pertuz G, Thongprayoon C, et al. A Systematic Review and Meta-Analysis of Posttransplant Anemia With Overall Mortality and Cardiovascular Outcomes Among Kidney Transplant Recipients. Prog Transplant. 2023;33(1):78-89. doi: 10.1177/15269248221145046.

Lentine KL, Schnitzler MA, Abbott KC, Li L, Burroughs TE, Irish W, et al. De novo congestive heart failure after kidney transplantation: a common condition with poor prognostic implications. Am J Kidney Dis. 2005;46(4):720-33. doi: 10.1053/j.ajkd.2005.06.019.

Shah N, Al-Khoury S, Afzali B, Covic A, Roche A, Marsh J, et al. Post-transplantation anemia in adult renal allograft recipients: prevalence and predictors. Transplantation. 2006;81(8):1112-8. doi: 10.1097/01.tp.0000205174.97275.b5.

Górska M, Kurnatowska I. Nutrition Disturbances and Metabolic Complications in Kidney Transplant Recipients: Etiology, Methods of Assessment and Prevention-A Review. Nutrients. 2022;14(23):4996. doi: 10.3390/nu14234996.

Kalantzi M, Kalliakmani P, Papachristou E, Papasotiriou M, Savvidaki E, Zavvos V, et al. Parameters influencing blood erythropoietin levels of renal transplant recipients during the early post-transplantation period. Transplant Proc. 2014;46(9):3179-82. doi: 10.1016/j.transproceed.2014.10.035.

Afzali B, Al-Khoury S, Shah N, Mikhail A, Covic A, Goldsmith D. Anemia after renal transplantation. Am J Kidney Dis. 2006;48(4):519-36. doi: 10.1053/j.ajkd.2006.07.006.

Besarab A, Caro J, Jarrell BE, Francos G, Erslev AJ.. Dynamics of erythropoiesis following renal transplantation. Kidney Int. 1987;32(4):526-36. doi: 10.1038/ki.1987.241.

Vinke JSJ, Francke MI, Eisenga MF, Hesselink DA, de Borst MH. Iron deficiency after kidney transplantation. Nephrol Dial Transplant. 2021;36:1976–85. doi: 10.1093/ndt/gfaa123.

Moore LW, Smith SO, Winsett RP, Acchiardo SR, Gaber AO. Factors affecting erythropoietin production and correction of anemia in kidney transplant recipients. Clin Transplant. [Internet].1994;8(4):358–64. Available from: https://pubmed.ncbi.nlm.nih.gov/7949539/.

Nissaisorakarn V, Nissaisorakarn P, Kantachuvesiri S. The current therapeutic approach for anaemia after kidney transplant. Curr Opin Nephrol Hypertens. 2023;32(1):35–40. doi: 10.1097/MNH.0000000000000842.

Saad EJ, Fernández P, Cardozo Azua AE, Ellena V, Diz C, Giordano G, Borgogno P, et al. Infections in the first year after renal transplant. Medicina (B Aires). [Internet]. 2020;80(6):611-621. Available from: https://pubmed.ncbi.nlm.nih.gov/33254105/.

Baradaran H, Hashem Zadeh A, Dashti-Khavidaki S, Laki B. Management of drug-induced neutropenia, thrombocytopenia, and anaemia after solid organ transplantation: a comprehensive review. J Clin Pharm Ther. 2022;47(12):1895–1912. doi: 10.1111/jcpt.13775.

Habas E, Khammaj A, Rayani A. Hematologic side effects of azathioprine and mycophenolate in kidney transplantation. Transplant Proc. 2011;43(2):504-6. doi: 10.1016/j.transproceed.2011.01.077.

Al Qahtani SA. Drug-induced megaloblastic, aplastic, and hemolytic anemias: current concepts of pathophysiology and treatment. Int J Clin Exp Med. [Internet]. 2018;11(6):5501–12. Available from: https://e-century.us/files/ijcem/11/6/ijcem0068128.pdf.

Boonpheng B, Thongprayoon C, Bathini T, Sharma K, Mao MA, Cheungpasitporn W. Proton pump inhibitors and adverse effects in kidney transplant recipients: A meta-analysis. World J Transplant. 2019;9(2):35-47. doi: 10.5500/wjt.v9.i2.35.

Tsuchimoto A, Masutani K, Haruyama N, Nagata M, Noguchi H, Okabe Y, et al. Renal interstitial fibrosis in 0-hour biopsy as a predictor of post-transplant anemia. Am J Nephrol. 2013;38(4):267-74. doi: 10.1159/000354647.

Moore LW, Smith SO, Winsett RP, Acchiardo SR, Gaber AO. Factors affecting erythropoietin production and correction of anemia in kidney transplant recipients. Clin Transplant. [Internet]. 1994;8(4):358–64. Available from: https://pubmed.ncbi.nlm.nih.gov/7949539/.

Watts D, Gaete D, Rodriguez D, Hoogewijs D, Rauner M, Sormendi S, et al. Hypoxia Pathway Proteins are Master Regulators of Erythropoiesis. Int J Mol Sci. 2020;21(21):8131. doi: 10.3390/ijms21218131.

Imoagene-Oyedeji AE, Rosas SE, Doyle AM, Goral S, Bloom RD. Post-transplantation anemia at 12 months in kidney recipients treated with mycophenolate mofetil: risk factors and implications for mortality. J Am Soc Nephrol. 2006;17(11):3240–7. doi: 10.1681/ASN.2006010027.

Shibagaki Y, Shetty A. Anaemia is common after kidney transplantation, especially among African Americans. Nephrol Dial Transplant. 2004;19(9):2368–73. doi 10.1093/ndt/gfh256.

Molnar MZ, Czira M, Ambrus C, Szeifert L, Szentkiralyi A, Beko G, et al. Anemia is associated with mortality in kidney-transplanted patients--a prospective cohort study. Am J Transplant. 2007;7(4):818-24. doi: 10.1111/j.1600-6143.2006.01727.x.

Alotaibi NE, Mohsin B, Alharbi S, Odah NO, Sindi D, Bargawi S, Abid RB, et al. Postrenal transplant anemia and its effects on patients and graft outcomes: Seven years follow-up. Saudi Pharm J. 2023;31(8):101696. doi: 10.1016/j.jsps.2023.101696.

Heinze G, Mitterbauer C, Regele H, Kramar R, Winkelmayer WC, Curhan GC, et al. Angiotensin-converting enzyme inhibitor or angiotensin II type 1 receptor antagonist therapy is associated with prolonged patient and graft survival after renal transplantation. J Am Soc Nephrol. 2006;17(3):889-99. doi: 10.1681/ASN.2005090955.

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(4):1168-74. doi: 10.2215/CJN.04641007.

Sert I, Colak H, Tugmen C, Dogan SM, Karaca C. Anemia in living donor kidney transplantation. Transplant Proc. 2013;45(6):2238-43. doi: 10.1016/j.transproceed.2012.12.008.

Winkelmayer WC, Chandraker A, Alan Brookhart M, Kramar R, Sunder-Plassmann G. A prospective study of anaemia and long-term outcomes in kidney transplant recipients. Nephrol Dial Transplant. 2006;21(12):3559-66. doi: 10.1093/ndt/gfl457.

Schjelderup P, Dahle DO, Holdaas H, Mjøen G, Nordby G, Abedini S, et al. Anemia is a predictor of graft loss but not cardiovascular events and all-cause mortality in renal transplant recipients: follow-up data from the ALERT study. Clin Transplant. 2013;27(6):636-43. doi: 10.1111/ctr.12220.

Kamar N, Rostaing L, Ignace S, Villar E. Impact of post-transplant anemia on patient and graft survival rates after kidney transplantation: a meta-analysis. Clin Transplant. 2012;26(3):461–9. doi: 10.1111/j.1399-0012.2011.01545.x.

Freiberg M, Chiurchiu C, Capra R, Eckhardt A, De La Fuente J, Douthat W, et al. [Associated factors and clinical implications of post transplant renal anemia]. Medicina (B Aires). [Internet]. 2013;73(2):136–40. Available from:

https://pubmed.ncbi.nlm.nih.gov/23570761/.>

Eisenga MF, De Jong MA, Van der Meer P, Leaf DE, Huls G, Nolte IM, et al. Iron deficiency, elevated erythropoietin, fibroblast growth factor 23, and mortality in the general population of the Netherlands: A cohort study. PLoS Med. 2019;16(6):e1002818. doi: 10.1371/journal.pmed.1002818.

Vaugier C, Amano MT, Chemouny JM, Dussiot M, Berrou C, Matignon M, et al. Serum Iron Protects from Renal Postischemic Injury. J Am Soc Nephrol. 2017;28(12):3605-15. doi: 10.1681/ASN.2016080926.

Eisenga MF, Minović I, Berger SP, Kootstra-Ros JE, van den Berg E, Riphagen IJ, et al. Iron deficiency, anemia, and mortality in renal transplant recipients. Transpl Int. 2016;29(11):1176-83. doi: 10.1111/tri.12821.

Rigatto C, Foley R, Jeffery J, Negrijn C, Tribula C, Parfrey P. Electrocardiographic left ventricular hypertrophy in renal transplant recipients: prognostic value and impact of blood pressure and anemia. J Am Soc Nephrol. 2003;14(2):462-8. doi: 10.1097/01.asn.0000043141.67989.39.

Birdwell KA, Park M. Post-Transplant Cardiovascular Disease. Clin J Am Soc Nephrol. 2021;16(12):1878-89. doi: 10.2215/CJN.00520121.

Malyala R, Rapi L, Nash MM, Prasad GVR. Pre-Transplant Left Ventricular Geometry and Major Adverse Cardiovascular Events After Kidney Transplantation. Ann Transplant. 2019;24:100-7. doi: 10.12659/AOT.913649.

Kensinger C, Hernandez A, Bian A, Fairchild M, Chen G, Lipworth L, et al. Longitudinal assessment of cardiac morphology and function following kidney transplantation. Clin Transplant. 2017;31(1):e12864. doi: 10.1111/ctr.12864.

Paoletti E, Bellino D, Signori A, Pieracci L, Marsano L, Russo R, et al. Regression of asymptomatic cardiomyopathy and clinical outcome of renal transplant recipients: a long-term prospective cohort study. Nephrol Dial Transplant. 2016;31(7):1168-74. doi: 10.1093/ndt/gfv354.

Laskar SR, Dries DL. The prognostic significance of renal dysfunction in patients with chronic systolic heart failure. Curr Cardiol Rep. 2003;5(3):205-10. doi: 10.1007/s11886-003-0050-z.

Fujikura K, Peltzer B, Tiwari N, Shim HG, Dinhofer AB, Shitole SG, et al. Reduced global longitudinal strain is associated with increased risk of cardiovascular events or death after kidney transplant. Int J Cardiol. 2018;272:323-8. doi: 10.1016/j.ijcard.2018.07.088.

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(2):360-8. doi: 10.1681/ASN.2011060546.

Tsujita M, Kosugi T, Goto N, Futamura K, Nishihira M, Okada M, et al. The effect of maintaining high hemoglobin levels on long-term kidney function in kidney transplant recipients: a randomized controlled trial. Nephrol Dial Transplant. 2019;34(8):1409-16. doi: 10.1093/ndt/gfy365.

Molnar MZ, Czira M, Ambrus C, Szeifert L, Szentkiralyi A, Beko G, et al. Anemia is associated with mortality in kidney-transplanted patients--a prospective cohort study. Am J Transplant. 2007;7(4):818-24. doi: 10.1111/j.1600-6143.2006.01727.x.

Majernikova M, Rosenberger J, Prihodova L, Jarcuskova M, Roland R, Groothoff JW, et al. Posttransplant Anemia as a Prognostic Factor of Mortality in Kidney-Transplant Recipients. Biomed Res Int. 2017;2017:6987240. doi: 10.1155/2017/6987240.

Gafter-Gvili A, Gafter U. Post-transplantation Anemia in Kidney Transplant Recipients. Acta Haematol. 2019;142(1):37-43. doi: 10.1159/000496140.

Winkelmayer WC, Lorenz M, Kramar R, Hörl WH, Sunder-Plassmann G. Percentage of hypochromic red blood cells is an independent risk factor for mortality in kidney transplant recipients. Am J Transplant. 2004;4(12):2075-81. doi: 10.1046/j.1600-6143.2004.00604.x.

Ribeiro M, Fonseca L, Anjos JS, Capo-Chichi JCC, Borges NA, Burrowes J, et al. Oral iron supplementation in patients with chronic kidney disease: can it be harmful to the gut microbiota? Nutr Clin Pract. 2021;37(1):81–93. doi: 10.1002/ncp.10662.

Ardalan M, Vahed SZ. Gut microbiota and renal transplant outcome. Biomed Pharmacother. 2017;90:229-236. doi: 10.1016/j.biopha.2017.02.114.

Shepshelovich D, Rozen-Zvi B, Avni T, Gafter U, Gafter-Gvili A. Intravenous Versus Oral Iron Supplementation for the Treatment of Anemia in CKD: An Updated Systematic Review and Meta-analysis. Am J Kidney Dis. 2016;68(5):677-90. doi: 10.1053/j.ajkd.2016.04.018.

Rozen-Zvi B, Gafter-Gvili A, Zingerman B, Levy-Drummer RS, Levy L, Mor E, et al. Intravenous iron supplementation after kidney transplantation. Clin Transplant. 2012;26(4):608–14. doi: 10.1111/j.1399-0012.2012.01602.x.

Mudge DW, Tan KS, Miles R, Johnson DW, Badve SV, Campbell SB, et al. A randomized controlled trial of intravenous or oral iron for posttransplant anemia in kidney transplantation. Transplantation. 2012;93(8):822–6. doi: 10.1097/TP.0b013e318248375a.

Bazeley J, Wish J. Recent and emerging therapies for iron deficiency in anemia of CKD: a review. Am J Kidney Dis. 2022;79(6):868–6. doi: 10.1053/j.ajkd.2021.09.017.

Grimmelt AC, Cohen CD, Fehr T, Serra AL, Wuethrich RP. Safety and tolerability of ferric carboxymaltose (FCM) for treatment of iron deficiency in patients with chronic kidney disease and in kidney transplant recipients. Clin Nephrol. 2009;71(2):125–9. doi: 10.5414/cnp71125.

Schaefer B, Tobiasch M, Viveiros A, Tilg H, Kennedy NA, Wolf M, et al. Hypophosphataemia after treatment of iron deficiency with intravenous ferric carboxymaltose or iron isomaltoside—a systematic review and meta-analysis. Br J Clin Pharmacol. 2021;87(5):2256–73. doi: 10.1111/bcp.14643.

Sari V, Atiqi R, Hoorn EJ, Heijboer AC, van Gelder T, Hesselink DA. Ferric carboxymaltose-induced hypophosphataemia after kidney transplantation. Neth J Med. [Internet]. 2017;75(2):65-73. Available from: https://pubmed.ncbi.nlm.nih.gov/28276325/.

Kassianides X, Bhandari S. Hypophosphataemia, fibroblast growth factor 23 and third-generation intravenous iron compounds: a narrative review. Drugs Context. 2021;10:1-29. doi: 10.7573/dic.2020-11-3.

Portoles J, Crespo M, Martínez Belotto M, Martínez Morales E, Calatayud Aristoy E, Mora Lopez P, et al. Post-transplant renal anemia: a call to action from a national study in routine clinical practice. Clin Kidney J. 2024;17(10):sfae269. doi: 10.1093/ckj/sfae269.

Alshamsi I. Extended literature review of the role of erythropoietin stimulating agents (ESA) use in the management of post renal transplant anaemia. Transplant Rep. 2022;7(2): 100097. doi: 10.1016/j.tpr.2022.100097.

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(3):367-8. doi: 10.1097/01.tp.0000150370.51700.99.

Yasari F, Nafar M, Alipour Abdei B, Ahmadpoor P, Pour-Reza-Gholi F, Samadian F, et al. Effect of erythropoietin on kidney allograft survival: early use after transplantation. Iran J Kidney Dis. [Internet]. 2012;6(1):44-8. Available from: https://pubmed.ncbi.nlm.nih.gov/22218119/.

Pile T, Raftery M, Thuraisingham R, Kirwan CJ, Harwood S, Yaqoob MM. Treating posttransplant anemia with erythropoietin improves quality of life but does not affect progression of chronic kidney disease. Exp Clin Transplant. 2020;18(1):27–33. doi: 10.6002/ect.2018.0283.

Obi Y, Ichimaru N, Sakaguchi Y, Iwadoh K, Ishii D, Sakai K, et al. ANDLE-KIT Trial Investigators. Correcting anemia and native vitamin D supplementation in kidney transplant recipients: a multicenter, 2 × 2 factorial, open-label, randomized clinical trial. Transpl Int. 2021; 34(7):1212-1225. doi: 10.1111/tri.13885.

Elliott S, Tomita D, Endre Z. Erythropoiesis stimulating agents and reno-protection: a meta-analysis. BMC Nephrol. 2017 ;18(1):14. doi: 10.1186/s12882-017-0438-4.

Cassis P, Gallon L, Benigni A, Mister M, Pezzotta A, Solini S, et al. Erythropoietin, but not the correction of anemia alone, protects from chronic kidney allograft injury. Kidney Int. 2012;81(9):903-18. doi: 10.1038/ki.2011.473.

Purroy C, Fairchild RL, Tanaka T, Baldwin WM 3rd, Manrique J, Madsen JC, et al. Erythropoietin Receptor-Mediated Molecular Crosstalk Promotes T Cell Immunoregulation and Transplant Survival. J Am Soc Nephrol. 2017;28(8):2377-92. doi: 10.1681/ASN.2016101100.

Cao Y. Erythropoietin in cancer: a dilemma in risk therapy. Trends Endocrinol Metab. 2013;24(4):190-9. doi: 10.1016/j.tem.2012.10.007.

Kliger AS, Foley RN, Goldfarb DS, Goldstein SL, Johansen K, Singh A, et al. KDOQI US commentary on the 2012 KDIGO Clinical Practice Guideline for Anemia in CKD. Am J Kidney Dis. 2013;62(5):849-59. doi: 10.1053/j.ajkd.2013.06.008.

Chienwichai K, Phirom S, Wuttiputhanun T, Leelahavanichkul A, Townamchai N, Avihingsanon Y, et al. A systematic review and meta-analysis of factors contributing to post-kidney transplant anemia and the effect of erythropoietin-stimulating agents. Syst Rev. 2024;13(1):278. doi: 10.1186/s13643-024-02709-8.

Singh AK, Szczech L, Tang KL, Barnhart H, Sapp S, Wolfson M, Reddan D; CHOIR Investigators. Correction of anemia with epoetin alfa in chronic kidney disease. N Engl J Med. 2006;355(20):2085-98. doi: 10.1056/NEJMoa065485.

Olivas-Martinez A, Corona-Rodarte E, Nuñez-Zuno A, Barrales-Benítez O, Oca DM, Mora JD, et al. Causes of erythrocytosis and its impact as a risk factor for thrombosis according to etiology: experience in a referral center in Mexico City. Blood Res. 2021;56(3):166-174. doi: 10.5045/br.2021.2021111.

Gaiffe E, Vernerey D, Bardiaux L, Leroux F, Meurisse A, Bamoulid J, et al. Early Post-Transplant Red Blood Cell Transfusion Is Associated With an Increased Risk of Transplant Failure: A Nationwide French Study. Front Immunol. 2022;13:854850. doi: 10.3389/fimmu.2022.854850.

Silva BDPC, Lasmar MF, Nascimento E, Fabreti-Oliveira RA. Impact of early blood transfusion after kidney transplantation on the clinical outcomes and allograft survival. Transpl Immunol. 2023;77:101807. doi: 10.1016/j.trim.2023.101807.

Goel R, Patel EU, Cushing MM, Frank SM, Ness PM, Takemoto CM, et al. Association of perioperative red blood cell transfusions with venous thromboembolism in a north American registry. JAMA Surg. 2018;153(9):826–33. doi: 10.1001/jamasurg.2018.1565.

Massicotte-Azarniouch D, Sood MM, Fergusson DA, Chassé M, Tinmouth A, et al. The association of venous thromboembolism with blood transfusion in kidney transplant patients. Transfusion. 2022;62(12):2480–9. doi: 10.1111/trf.17154.

Lam NN, Garg AX, Knoll GA, Kim SJ, Lentine KL, McArthur E, et al. Venous thromboembolism and the risk of death and graft loss in kidney transplant recipients. Am J Nephrol. 2017;46(4):343–54. doi: 10.1159/000480304.

Koury MJ, Haase VH. Anaemia in kidney disease: harnessing hypoxia responses for therapy. Nat Rev Nephrol. 2015;11(7):394-410. doi: 10.1038/nrneph.2015.82.

Miki K, Nakamura Y, Yokoyama T, Kamiyama M, Ishii Y. Therapeutic effect of roxadustat on patients with posttransplant anemia. Transplant Proc. 2022;54(3):671–77. doi: 10.1016/j.transproceed.2022.02.004.

Li J, Ma K, Wang L, Qi H, Lv J, Rao Y, Peng W. Efficacy and safety of roxadustat in the treatment of renal allograft anemia patients: a case series. Ann Palliat Med. 2021;10(11):11859-67. doi: 10.21037/apm-21-2916.

Naganuma T, Iwai T, Takemoto Y, Uchida J. Experience with the use of a novel agent, hypoxia-inducible factor prolyl hydroxylase inhibitor, for posttransplant anemia in renal transplant recipients: a case report. Transplant Proc. 2022;54(2):544–48. doi: 10.1016/j.transproceed.2021.10.022.

Abdelazeem B, Shehata J, Abbas KS, El-Shahat NA, Malik B, Savarapu P, et al. The efficacy and safety of roxadustat for the treatment of anemia in non-dialysis dependent chronic kidney disease patients: An updated systematic review and meta-analysis of randomized clinical trials. PLoS One. 2022;17(4):e0266243. doi: 10.1371/journal.pone.0266243.

Turshudzhyan A. Post-renal transplant malignancies: Opportunities for prevention and early screening. Cancer Treat Res Commun. 2021;26:100283. doi: 10.1016/j.ctarc.2020.100283.

Basheeruddin M, Qausain S. Hypoxia-Inducible Factor 1-Alpha (HIF-1α) and Cancer: Mechanisms of Tumor Hypoxia and Therapeutic Targeting. Cureus. 2024;16(10):e70700. doi: 10.7759/cureus.70700.

Shirole NH, Kaelin WG Jr. von-Hippel Lindau and Hypoxia-Inducible Factor at the Center of Renal Cell Carcinoma Biology. Hematol Oncol Clin North Am. 2023;37(5):809-25. doi: 10.1016/j.hoc.2023.04.011.

KDIGO 2023 Clinical Practice Guideline for the Care of Kidney Transplant Recipients. Kidney Int Suppl. [Internet]. 2023;13(1):1–164. Available from: https://consultorsalud.com/wp-content/uploads/2023/09/KDIGO-2023-CKD-Guideline-Public-Review-Draft_5-July-2023.pdf.

Saeedi P, Petersohn I, Salpea P, Malanda B, Karuranga S, Unwin N, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the International Diabetes Federation Diabetes Atlas, 9th edition. Diabetes Res Clin Pract. 2019;157:107843. doi: 10.1016/j.diabres.2019.107843.

Wright EM, Hirayama BA, Loo DF. Active sugar transport in health and disease. J Intern Med. 2007;261(1):32–43. doi: 10.1111/j.1365-2796.2006.01746.x.

Vallon V, Verma S. Effects of SGLT2 inhibitors on kidney and cardiovascular function. Annu Rev Physiol. 2021;83:503–28. doi: 10.1146/annurev-physiol-031620-095920.

Yoshida Y, Takahashi K, Hashimoto R, Oya T, Sato J. Relationship Between SGLT2 Inhibitors and Hemoglobin Levels: A Retrospective Observational Study. In Vivo. 2023;37(5):2327-33. doi: 10.21873/invivo.13336.

Lemke A, Brokmeier HM, Leung SB, Mara KC, Mour GK, Wadei HM, et al. Sodium-glucose co-transporter 2 inhibitors for treatment of diabetes mellitus after kidney transplantation. Clin Transplant. 2022;36(8):e14718. doi: 10.1111/ctr.14718.

Chewcharat A, Prasitlumkum N, Thongprayoon C, Bathini T, Medaura J, Vallabhajosyula S, Cheungpasitporn W, et al. Efficacy and safety of SGLT-2 inhibitors for treatment of diabetes mellitus among kidney transplant patients: A systematic review and meta-analysis. Med Sci (Basel). 2020;8(4):47. doi: 10.3390/medsci8040047.

Carro C, Raba A, Deras E, Sánchez LA, Cecilio RV, López-Gómez JJ, et al. FC 116: SGLT2 Inhibitors in Kidney Transplantation: A Multicenter Study, Nephrology Dialysis Transplantation. 2022;37(3):884–87. doi 10.1093/ndt/gfac124.001.

Halden TAS, Kvitne KE, Midtvedt K, Rajakumar L, Robertsen I, Brox J, et al. Efficacy and safety of empagliflozin in renal transplant recipients with posttransplant diabetes mellitus. Diabetes Care. 2019; 42(6):1067–74. doi: 10.2337/dc19-0093.

Ferreira JP, Anker SD, Butler J, Filippatos G, Iwata T, Salsali A, et al. Impact of anaemia and the effect of empagliflozin in heart failure with reduced ejection fraction: findings from EMPEROR-Reduced. Eur J Heart Fail. 2022;24(4):708-15. doi: 10.1002/ejhf.2409.

Schwarz Y, Klein P, Lev-Shalem L. Masked anemia and hematocrit elevation under sodium glucose transporter inhibitors: findings from a large real-world study. Acta Diabetol.2024;61(1):99-105. doi: 10.1007/s00592-023-02174-0.

Pham PT, Pham PT. Optimal use of SGLT2 inhibitors in diabetic kidney transplant recipients. Front Nephrol. 2022;2:1014241. doi: 10.3389/fneph.2022.1014241.

Packer M. Mechanisms of enhanced renal and hepatic erythropoietin synthesis by sodium-glucose co-transporter 2 inhibitors. Eur Heart J. 2023;44(48):5027-35. doi: 10.1093/eurheartj/ehad235.

Hu JC, Shao SC, Tsai DH, Chuang AT, Liu KH, Lai EC. Use of SGLT2 Inhibitors vs GLP-1 RAs and Anemia in Patients With Diabetes and CKD. JAMA Netw Open. 2024;7(3):e240946. doi: 10.1001/jamanetworkopen.2024.0946.

Ku E, Del Vecchio L, Eckardt KU, Haase VH, Johansen KL, Nangaku M, et al. Novel anemia therapies in chronic kidney disease: conclusions from a Kidney Disease: Improving Global Outcomes (KDIGO) Controversies Conference. Kidney Int. 2023;104(4):655-80. doi: 10.1016/j.kint.2023.05.009.

Ujjawal A, Schreiber B, Verma A. Sodium-glucose cotransporter-2 inhibitors (SGLT2i) in kidney transplant recipients: what is the evidence? Ther Adv Endocrinol Metab. 2022;13:20420188221090001. doi: 10.1177/20420188221090001.

Mazer CD, Hare GMT, Connelly PW, Gilbert RE, Shehata N, Quan A, et al. Effect of empagliflozin on erythropoietin levels, iron stores, and red blood cell morphology in patients with type 2 diabetes mellitus and coronary artery disease. Circulation. 2020;141(8):704–7. doi: 10.1161/CIRCULATIONAHA.119.044235.

Yabu JM, Winkelmayer WC. Post-transplantation anemia: mechanisms and management. Clin J Am Soc Nephrol. 2011;6(7):1794-801. doi: 10.2215/CJN.01190211.

Koshino A, Schechter M, Chertow GM, Vart P, Jongs N, Toto RD, et al. Dapagliflozin and anemia in patients with chronic kidney disease. NEJM Evidence. 2023;2(6):EVIDoa2300049. doi: 10.1056/EVIDoa2300049.

Hai An HP, Diem HT, Cuong NT. Parvovirus B19-Associated Anemia in Kidney Transplant Recipients: A Single-Center Experience. Transplant Proc. 2019;51(8):2693-96. doi: 10.1016/j.transproceed.2019.03.076.


Abstract views: 1291
PDF Downloads: 295
Published
2025-06-13
How to Cite
Habas, E., Rayani, A., Habas, A., Afitori, G., Habas, A., Farfar, K., Habas, E., Alarbi, K., Bagi, M., Errayes, A., Hamad, A., & Elzouki, A.-N. (2025). Burden of anemia in kidney transplant patients: Epidemiology, pathophysiology, and management. Ukrainian Journal of Nephrology and Dialysis, (2(86), 71-89. https://doi.org/10.31450/ukrjnd.2(86).2025.08

Most read articles by the same author(s)