Skip to main content
Top
Published in: Pediatric Nephrology 2/2016

01-02-2016 | Original Article

Anemia in children following renal transplantation—results from the ESPN/ERA-EDTA Registry

Authors: Leah A. Krischock, Karlijn J. van Stralen, Enrico Verrina, E. Jane Tizard, Marjolein Bonthuis, György Reusz, Farida K Hussain, Augustina Jankauskiene, Gregor Novljan, Brankica Spasojević-Dimitrijeva, Ludmila Podracka, Vera Zaller, Kitty J. Jager, Franz Schaefer, on behalf of the ESPN/ERA-EDTA Registry

Published in: Pediatric Nephrology | Issue 2/2016

Login to get access

Abstract

Background

Our aim was to determine the prevalence of sub-target hemoglobin (Hb) levels in children with a renal allograft and to identify potential determinants associated with these Hb levels.

Methods

Data from 3669 children with a functioning renal allograft, aged <18 years between 1 January 2000 and 31 December 2012, from 20 European countries were retrieved from the ESPN/ERA-EDTA Registry, providing 16,170 Hb measurements.

Results

According to the NKF/KDOQI classification and the UK-NICE guidelines, 49.8 and 7.8 % of the patients, respectively, were anemic. Hb levels were strongly associated with graft function, with Hb levels of 12.6 g/dl in children with chronic kidney disease (CKD) stage 1, declining to 10.7 g/dl in children with CKD stage 5 (P < 0.001). Higher Hb levels were associated with the use of tacrolimus compared to ciclosporin (0.14 g/dl; 95 % confidence interval 0.02–0.27; P = 0.002). Low Hb levels were associated with an increased risk of graft failure (P = 0.01) or combined graft failure and death (P < 0.01), but not with death alone (not significant).

Conclusions

Anemia is present in a significant proportion of European pediatric kidney transplant recipients and is associated with renal allograft dysfunction and type of immunosuppressants used. In our patient cohort, higher Hb levels were associated with better graft and patient survival and less hypertension.
Literature
1.
go back to reference National Kidney Foundation (2006) KDOQI clinical practice recommendations for 2006 updates: hemodialysis adequacy, peritoneal dialysis adequacy and vascular access. Am J Kidney Dis 48:S1–S322CrossRef National Kidney Foundation (2006) KDOQI clinical practice recommendations for 2006 updates: hemodialysis adequacy, peritoneal dialysis adequacy and vascular access. Am J Kidney Dis 48:S1–S322CrossRef
2.
go back to reference Kidney Disease Outcomes Quality Initiative, National Kidney Foundation (2006) KDOQI Clinical practice guidelines and clinical practice recommendations for anemia in chronic kidney disease. Am J Kidney Dis 47:S11–S145CrossRef Kidney Disease Outcomes Quality Initiative, National Kidney Foundation (2006) KDOQI Clinical practice guidelines and clinical practice recommendations for anemia in chronic kidney disease. Am J Kidney Dis 47:S11–S145CrossRef
3.
go back to reference Lewis MA, Shaw J, Sinha MD, Adalat S, Hussain F, Castledine C, van Schalkwyk D, Inward C (2010) UK Renal Registry 12th Annual Report (December 2009): chapter 14: demography of the UK paediatric renal replacement therapy population in 2008. Nephron Clin Pract 115[Suppl 1]:c279–c288PubMedCrossRef Lewis MA, Shaw J, Sinha MD, Adalat S, Hussain F, Castledine C, van Schalkwyk D, Inward C (2010) UK Renal Registry 12th Annual Report (December 2009): chapter 14: demography of the UK paediatric renal replacement therapy population in 2008. Nephron Clin Pract 115[Suppl 1]:c279–c288PubMedCrossRef
4.
go back to reference White CT, Schisler T, Er L, Djurdjev O, Matsuda-Abedini M (2008) CKD following kidney transplantation in children and adolescents. Am J Kidney Dis 51:996–1004PubMedCrossRef White CT, Schisler T, Er L, Djurdjev O, Matsuda-Abedini M (2008) CKD following kidney transplantation in children and adolescents. Am J Kidney Dis 51:996–1004PubMedCrossRef
5.
go back to reference Al-Khoury S, Shah N, Afzali B, Covic A, Taylor J, Goldsmith D (2006) Post-transplantation anaemia in adult and paediatric renal allograft recipients—Guy’s Hospital experience. Nephrol Dial Transplant 21:1974–1980PubMedCrossRef Al-Khoury S, Shah N, Afzali B, Covic A, Taylor J, Goldsmith D (2006) Post-transplantation anaemia in adult and paediatric renal allograft recipients—Guy’s Hospital experience. Nephrol Dial Transplant 21:1974–1980PubMedCrossRef
6.
go back to reference Al-Uzri A, Yorgin PD, Kling PJ (2003) Anemia in children after transplantation: etiology and the effect of immunosuppressive therapy on erythropoiesis. Pediatr Transplant 7:253–264PubMedCrossRef Al-Uzri A, Yorgin PD, Kling PJ (2003) Anemia in children after transplantation: etiology and the effect of immunosuppressive therapy on erythropoiesis. Pediatr Transplant 7:253–264PubMedCrossRef
7.
go back to reference El-Husseini AA, Sobh MA, Ghoneim MA (2008) Complications of pediatric live-donor kidney transplantation: a single center’s experience in Egypt. Pediatr Nephrol 23:2067–2073PubMedCrossRef El-Husseini AA, Sobh MA, Ghoneim MA (2008) Complications of pediatric live-donor kidney transplantation: a single center’s experience in Egypt. Pediatr Nephrol 23:2067–2073PubMedCrossRef
8.
go back to reference Feber J, Wong H, Geier P, Chaudry B, Filler G (2008) Complications of chronic kidney disease in children post-renal transplantation—a single center experience. Pediatr Transplant 12:80–84PubMedCrossRef Feber J, Wong H, Geier P, Chaudry B, Filler G (2008) Complications of chronic kidney disease in children post-renal transplantation—a single center experience. Pediatr Transplant 12:80–84PubMedCrossRef
9.
go back to reference Kausman JY, Powell HR, Jones CL (2004) Anemia in pediatric renal transplant recipients. Pediatr Nephrol 19:526–530PubMedCrossRef Kausman JY, Powell HR, Jones CL (2004) Anemia in pediatric renal transplant recipients. Pediatr Nephrol 19:526–530PubMedCrossRef
10.
go back to reference Mitsnefes MM, Subat-Dezulovic M, Khoury PR, Goebel J, Strife CF (2005) Increasing incidence of post-kidney transplant anemia in children. Am J Transplant 5:1713–1718PubMedCrossRef Mitsnefes MM, Subat-Dezulovic M, Khoury PR, Goebel J, Strife CF (2005) Increasing incidence of post-kidney transplant anemia in children. Am J Transplant 5:1713–1718PubMedCrossRef
11.
go back to reference Petrone H, Arriola M, Re L, Taylor F, Bruzzone M, Chiurchu C, Schiavelli R, Comite Renal de la Sociedad Argentina de Trasplantes (2010) National survey of anemia prevalence after kidney transplantation in Argentina. Transplant Proc 42:288–290PubMedCrossRef Petrone H, Arriola M, Re L, Taylor F, Bruzzone M, Chiurchu C, Schiavelli R, Comite Renal de la Sociedad Argentina de Trasplantes (2010) National survey of anemia prevalence after kidney transplantation in Argentina. Transplant Proc 42:288–290PubMedCrossRef
12.
go back to reference White CT, Barrett BJ, Madore F, Moist LM, Klarenbach SW, Foley RN, Culleton BF, Tonelli M, Manns BJ; Canadian Society of Nephrology (2008) Clinical practice guidelines for evaluation of anemia. Kidney Int Suppl (110):S4–6 White CT, Barrett BJ, Madore F, Moist LM, Klarenbach SW, Foley RN, Culleton BF, Tonelli M, Manns BJ; Canadian Society of Nephrology (2008) Clinical practice guidelines for evaluation of anemia. Kidney Int Suppl (110):S4–6
13.
go back to reference Yorgin PD, Belson A, Sanchez J, Al Uzri AY, Sarwal M, Bloch DA, Oehlert J, Salvatierra O, Alexander SR (2002) Unexpectedly high prevalence of posttransplant anemia in pediatric and young adult renal transplant recipients. Am J Kidney Dis 40:1306–1318PubMedCrossRef Yorgin PD, Belson A, Sanchez J, Al Uzri AY, Sarwal M, Bloch DA, Oehlert J, Salvatierra O, Alexander SR (2002) Unexpectedly high prevalence of posttransplant anemia in pediatric and young adult renal transplant recipients. Am J Kidney Dis 40:1306–1318PubMedCrossRef
14.
go back to reference Blosser CD, Bloom RD (2010) Posttransplant anemia in solid organ recipients. Transplant Rev (Orlando) 24:89–98CrossRef Blosser CD, Bloom RD (2010) Posttransplant anemia in solid organ recipients. Transplant Rev (Orlando) 24:89–98CrossRef
15.
go back to reference Winkelmayer WC, Kewalramani R, Rutstein M, Gabardi S, Vonvisger T, Chandraker A (2004) Pharmacoepidemiology of anemia in kidney transplant recipients. J Am Soc Nephrol 15:1347–1352PubMedCrossRef Winkelmayer WC, Kewalramani R, Rutstein M, Gabardi S, Vonvisger T, Chandraker A (2004) Pharmacoepidemiology of anemia in kidney transplant recipients. J Am Soc Nephrol 15:1347–1352PubMedCrossRef
16.
go back to reference Gheith O, Wafa E, Hassan N, Mostafa A, Sheashaa HA, Mahmoud K, Shokeir A, Ghoneim MA (2009) Does posttransplant anemia at 6 months affect long-term outcome of live-donor kidney transplantation? A single-center experience. Clin Exp Nephrol 13:361–366PubMedCrossRef Gheith O, Wafa E, Hassan N, Mostafa A, Sheashaa HA, Mahmoud K, Shokeir A, Ghoneim MA (2009) Does posttransplant anemia at 6 months affect long-term outcome of live-donor kidney transplantation? A single-center experience. Clin Exp Nephrol 13:361–366PubMedCrossRef
17.
go back to reference Chavers BM, Roberts TL, Herzog CA, Collins AJ, St Peter WL (2004) Prevalence of anemia in erythropoietin-treated pediatric as compared to adult chronic dialysis patients. Kidney Int 65:266–273PubMedCrossRef Chavers BM, Roberts TL, Herzog CA, Collins AJ, St Peter WL (2004) Prevalence of anemia in erythropoietin-treated pediatric as compared to adult chronic dialysis patients. Kidney Int 65:266–273PubMedCrossRef
19.
go back to reference Joist H, Brennan DC, Coyne DW (2006) Anemia in the kidney-transplant patient. Adv Chronic Kidney Dis 13:4–10PubMedCrossRef Joist H, Brennan DC, Coyne DW (2006) Anemia in the kidney-transplant patient. Adv Chronic Kidney Dis 13:4–10PubMedCrossRef
20.
go back to reference Molnar MZ, Czira M, Ambrus C, Szeifert L, Szentkiralyi A, Beko G, Rosivall L, Remport A, Novak M, Mucsi I (2007) Anemia is associated with mortality in kidney-transplanted patients—a prospective cohort study. Am J Transplant 7:818–824PubMedCrossRef Molnar MZ, Czira M, Ambrus C, Szeifert L, Szentkiralyi A, Beko G, Rosivall L, Remport A, Novak M, Mucsi I (2007) Anemia is associated with mortality in kidney-transplanted patients—a prospective cohort study. Am J Transplant 7:818–824PubMedCrossRef
21.
go back to reference Kidney Disease Outcomes Quality Initiative (2007) KDOQI Clinical Practice Guideline and Clinical Practice Recommendations for anemia in chronic kidney disease: 2007 update of hemoglobin target. Am J Kidney Dis 50:471–530CrossRef Kidney Disease Outcomes Quality Initiative (2007) KDOQI Clinical Practice Guideline and Clinical Practice Recommendations for anemia in chronic kidney disease: 2007 update of hemoglobin target. Am J Kidney Dis 50:471–530CrossRef
24.
go back to reference Tizard EJ, Verrina E, van Stralen KJ, Jager KJ (2009) Progress with the European Society for Paediatric Nephrology (ESPN)/ERA-EDTA Registry for children with established renal failure (ERF). Nephrol Dial Transplant 24:2615–2617PubMedPubMedCentralCrossRef Tizard EJ, Verrina E, van Stralen KJ, Jager KJ (2009) Progress with the European Society for Paediatric Nephrology (ESPN)/ERA-EDTA Registry for children with established renal failure (ERF). Nephrol Dial Transplant 24:2615–2617PubMedPubMedCentralCrossRef
25.
go back to reference Schwartz GJ, Munoz A, Schneider MF, Mak RH, Kaskel F, Warady BA, Furth SL (2009) New equations to estimate GFR in children with CKD. J Am Soc Nephrol 20:629–637PubMedPubMedCentralCrossRef Schwartz GJ, Munoz A, Schneider MF, Mak RH, Kaskel F, Warady BA, Furth SL (2009) New equations to estimate GFR in children with CKD. J Am Soc Nephrol 20:629–637PubMedPubMedCentralCrossRef
26.
go back to reference von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP, STROBE Initiative (2007) The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 370:1453–1457CrossRef von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP, STROBE Initiative (2007) The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 370:1453–1457CrossRef
28.
go back to reference National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents (2004) The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics 114:555–576CrossRef National High Blood Pressure Education Program Working Group on High Blood Pressure in Children and Adolescents (2004) The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics 114:555–576CrossRef
29.
go back to reference van Stralen KJ, Jager KJ, Verrina E, Schaefer FS, Emma F (2011) Suggested revision of the National High Blood Pressure Education Program blood pressure standardization for use in severely growth retarded children. Pediatr Nephrol 26:819–820PubMedPubMedCentralCrossRef van Stralen KJ, Jager KJ, Verrina E, Schaefer FS, Emma F (2011) Suggested revision of the National High Blood Pressure Education Program blood pressure standardization for use in severely growth retarded children. Pediatr Nephrol 26:819–820PubMedPubMedCentralCrossRef
30.
go back to reference van Stralen KJ, Dekker FW, Zoccali C, Jager KJ (2010) Confounding. Nephron Clin Pract 116:c143–c147PubMedCrossRef van Stralen KJ, Dekker FW, Zoccali C, Jager KJ (2010) Confounding. Nephron Clin Pract 116:c143–c147PubMedCrossRef
31.
go back to reference Chadban SJ, Baines L, Polkinghorne K, Jefferys A, Dogra S, Kanganas C, Irish A, Eris J, Walker R (2007) Anemia after kidney transplantation is not completely explained by reduced kidney function. Am J Kidney Dis 49:301–309PubMedCrossRef Chadban SJ, Baines L, Polkinghorne K, Jefferys A, Dogra S, Kanganas C, Irish A, Eris J, Walker R (2007) Anemia after kidney transplantation is not completely explained by reduced kidney function. Am J Kidney Dis 49:301–309PubMedCrossRef
32.
go back to reference Jacobsen T, Sifontis N (2010) Drug interactions and toxicities associated with the antiviral management of cytomegalovirus infection. Am J Health Syst Pharm 67:1417–1425PubMedCrossRef Jacobsen T, Sifontis N (2010) Drug interactions and toxicities associated with the antiviral management of cytomegalovirus infection. Am J Health Syst Pharm 67:1417–1425PubMedCrossRef
33.
go back to reference Vannucchi AM, Grossi A, Bosi A, Rafanelli D, Statello M, Guidi S, Saccardi R, Rossi-Ferrini P (1993) Effects of cyclosporin A on erythropoietin production by the human Hep3B hepatoma cell line. Blood 82:978–984PubMed Vannucchi AM, Grossi A, Bosi A, Rafanelli D, Statello M, Guidi S, Saccardi R, Rossi-Ferrini P (1993) Effects of cyclosporin A on erythropoietin production by the human Hep3B hepatoma cell line. Blood 82:978–984PubMed
34.
go back to reference Cortinovis M, Gotti E, Pradini S, Gaspari F, Perico N (2011) Renal graft function and low-dose cyclosporine affect mycophenolic acid pharmacokinetics in kidney transplantation. Transplantation 92:550–556PubMedCrossRef Cortinovis M, Gotti E, Pradini S, Gaspari F, Perico N (2011) Renal graft function and low-dose cyclosporine affect mycophenolic acid pharmacokinetics in kidney transplantation. Transplantation 92:550–556PubMedCrossRef
35.
go back to reference Fishbane S, Frei GL, Maesaka J (1995) Reduction in recombinant human erythropoietin doses by the use of chronic intravenous iron supplementation. Am J Kidney Dis 26:41–46PubMedCrossRef Fishbane S, Frei GL, Maesaka J (1995) Reduction in recombinant human erythropoietin doses by the use of chronic intravenous iron supplementation. Am J Kidney Dis 26:41–46PubMedCrossRef
36.
go back to reference Friend P, Russ G, Oberbauer R, Murgia MG, Tufveson G, Chapman J, Blancho G, Mota A, Grandaliano G, Campistol JM, Brault Y, Burke JT, Rapamune Maintenance Regimen (RMR) Study Group (2007) Incidence of anemia in sirolimus-treated renal transplant recipients: the importance of preserving renal function. Transpl Int 20:754–760PubMedCrossRef Friend P, Russ G, Oberbauer R, Murgia MG, Tufveson G, Chapman J, Blancho G, Mota A, Grandaliano G, Campistol JM, Brault Y, Burke JT, Rapamune Maintenance Regimen (RMR) Study Group (2007) Incidence of anemia in sirolimus-treated renal transplant recipients: the importance of preserving renal function. Transpl Int 20:754–760PubMedCrossRef
37.
go back to reference Grinyo JM, Cruzado JM (2006) Mycophenolate mofetil and sirolimus combination in renal transplantation. Am J Transplant 6:1991–1999PubMedCrossRef Grinyo JM, Cruzado JM (2006) Mycophenolate mofetil and sirolimus combination in renal transplantation. Am J Transplant 6:1991–1999PubMedCrossRef
38.
go back to reference Sica DA, Mannino R (2007) Antihypertensive medications and anemia. J Clin Hypertens (Greenwich) 9:723–727CrossRef Sica DA, Mannino R (2007) Antihypertensive medications and anemia. J Clin Hypertens (Greenwich) 9:723–727CrossRef
39.
go back to reference Borzych-Duzalka D, Bilginer Y, Ha IS, Bak M, Rees L, Cano F, Munarriz RL, Chua A, Pesle S, Emre S, Urzykowska A, Quiroz L, Ruscasso JD, White C, Pape L, Ramela V, Printza N, Vogel A, Kuzmanovska D, Simkova E, Muller-Wiefel DE, Sander A, Warady BA, Schaefer F, International Pediatric Peritoneal Dialysis Network (IPPN) Registry (2013) Management of anemia in children receiving chronic peritoneal dialysis. J Am Soc Nephrol 24:665–676PubMedPubMedCentralCrossRef Borzych-Duzalka D, Bilginer Y, Ha IS, Bak M, Rees L, Cano F, Munarriz RL, Chua A, Pesle S, Emre S, Urzykowska A, Quiroz L, Ruscasso JD, White C, Pape L, Ramela V, Printza N, Vogel A, Kuzmanovska D, Simkova E, Muller-Wiefel DE, Sander A, Warady BA, Schaefer F, International Pediatric Peritoneal Dialysis Network (IPPN) Registry (2013) Management of anemia in children receiving chronic peritoneal dialysis. J Am Soc Nephrol 24:665–676PubMedPubMedCentralCrossRef
40.
go back to reference Winkelmayer WC, Chandraker A, Alan Brookhart M, Kramar R, Sunder-Plassmann G (2006) A prospective study of anaemia and long-term outcomes in kidney transplant recipients. Nephrol Dial Transplant 21:3559–3566PubMedCrossRef Winkelmayer WC, Chandraker A, Alan Brookhart M, Kramar R, Sunder-Plassmann G (2006) A prospective study of anaemia and long-term outcomes in kidney transplant recipients. Nephrol Dial Transplant 21:3559–3566PubMedCrossRef
41.
go back to reference Imoagene-Oyedeji AE, Rosas SE, Doyle AM, Goral S, Bloom RD (2006) Posttransplantation anemia at 12 months in kidney recipients treated with mycophenolate mofetil: risk factors and implications for mortality. J Am Soc Nephrol 17:3240–3247PubMedCrossRef Imoagene-Oyedeji AE, Rosas SE, Doyle AM, Goral S, Bloom RD (2006) Posttransplantation anemia at 12 months in kidney recipients treated with mycophenolate mofetil: risk factors and implications for mortality. J Am Soc Nephrol 17:3240–3247PubMedCrossRef
42.
go back to reference Sterne JA, White IR, Carlin JB, Spratt M, Royston P, Kenward MG, Wood AM, Carpenter JR (2009) Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. BMJ 338:b2393PubMedPubMedCentralCrossRef Sterne JA, White IR, Carlin JB, Spratt M, Royston P, Kenward MG, Wood AM, Carpenter JR (2009) Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. BMJ 338:b2393PubMedPubMedCentralCrossRef
Metadata
Title
Anemia in children following renal transplantation—results from the ESPN/ERA-EDTA Registry
Authors
Leah A. Krischock
Karlijn J. van Stralen
Enrico Verrina
E. Jane Tizard
Marjolein Bonthuis
György Reusz
Farida K Hussain
Augustina Jankauskiene
Gregor Novljan
Brankica Spasojević-Dimitrijeva
Ludmila Podracka
Vera Zaller
Kitty J. Jager
Franz Schaefer
on behalf of the ESPN/ERA-EDTA Registry
Publication date
01-02-2016
Publisher
Springer Berlin Heidelberg
Published in
Pediatric Nephrology / Issue 2/2016
Print ISSN: 0931-041X
Electronic ISSN: 1432-198X
DOI
https://doi.org/10.1007/s00467-015-3201-8

Other articles of this Issue 2/2016

Pediatric Nephrology 2/2016 Go to the issue