Posttransplantation anemia: Mechanisms and management

Clinical Journal of the American Society of Nephrology

Volumn 6, Issue 7, 2011, Pages 1794-1801

  Yabu, Julie M ^a   Winkelmayer, Wolfgang C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN RECEPTOR ANTAGONIST; ANTIANEMIC AGENT; AZATHIOPRINE; CALCINEURIN INHIBITOR; CYCLOSPORIN; DAPSONE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ERYTHROPOIETIN; EVEROLIMUS; GANCICLOVIR; MYCOPHENOLIC ACID; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; RAPAMYCIN; SULFAMETHOXAZOLE; TACROLIMUS; TRIMETHOPRIM; VALGANCICLOVIR;

ADVERSE OUTCOME; ANEMIA; BK VIRUS; CARDIOVASCULAR DISEASE; CHRONIC KIDNEY DISEASE; CLINICAL STUDY; CYTOMEGALOVIRUS INFECTION; DRUG EFFICACY; DRUG SAFETY; EPSTEIN BARR VIRUS INFECTION; ERYTHEMA INFECTIOSUM; ERYTHROPOIESIS; GRAFT DYSFUNCTION; GRAFT RECIPIENT; HEMOLYSIS; HEPATITIS B; HEPATITIS C; HERPES VIRUS INFECTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOSUPPRESSIVE TREATMENT; IRON DEFICIENCY; KIDNEY ALLOGRAFT REJECTION; KIDNEY DONOR; KIDNEY GRAFT; KIDNEY TRANSPLANTATION; MORTALITY; PATHOGENESIS; POSTOPERATIVE COMPLICATION; POSTTRANSPLANTATION ANEMIA; PREVALENCE; REVIEW; RISK; SCREENING; TREATMENT OUTCOME;

ANEMIA; HEMATINICS; HUMANS; KIDNEY TRANSPLANTATION; PATIENT SELECTION; RISK ASSESSMENT; RISK FACTORS; TREATMENT OUTCOME;

EID: 79960333102     PISSN: 15559041     EISSN: 1555905X     Source Type: Journal    
DOI: 10.2215/CJN.01190211     Document Type: Review

References (69)

1. Karthikeyan V, Karpinski J, Nair RC, Knoll G: The burden of chronic kidney disease in renal transplant recipients. Am J Transplant 4: 262-269, 2004
2. McClellan WM, Flanders WD, Langston RD, Jurkovitz C, Presley R: Anemia and renal insufficiency are independent risk factors for death among patients with congestive heart failure admitted to community hospitals: A population-based study. J Am Soc Nephrol 13: 1928-1936, 2002
3. Sarnak MJ, Coronado BE, Greene T, Wang SR, Kusek JW, Beck GJ, Levey AS: Cardiovascular disease risk factors in chronic renal insufficiency. Clin Nephrol 57: 327-335, 2002
4. Locatelli F, Pisoni RL, Combe C, Bommer J, Andreucci VE, Piera L, Greenwood R, Feldman HI, Port FK, Held PJ: Anaemia in haemodialysis patients of five European countries: Association with morbidity and mortality in the Dialysis Outcomes and Practice Patterns Study (DOPPS). Nephrol Dial Transplant 19: 121-132, 2004
5. Winearls CG, Oliver DO, Pippard MJ, Reid C, Downing MR, Cotes PM: Effect of human erythropoietin derived from recombinant DNA on the anaemia of patients maintained by chronic haemodialysis. Lancet 2: 1175-1178, 1986
6. Kasiske BL: Cardiovascular disease after renal transplantation. Semin Nephrol 20: 176-187, 2000
7. Djamali A, Samaniego M, Muth B, Muehrer R, Hofmann RM, Pirsch J, Howard A, Mourad G, Becker BN: Medical care of kidney transplant recipients after the first posttransplant year. Clin J Am Soc Nephrol 1: 623-640, 2006
8. Imoagene-Oyedeji AE, Rosas SE, Doyle AM, Goral S, Bloom RD: Posttransplantation anemia at 12 months in kidney recipients treated with mycophenolate mofetil: Risk factors and implications for mortality. J Am Soc Nephrol 17: 3240-3247, 2006
9. Molnar MZ, Czira M, Ambrus C, Szeifert L, Szentkiralyi A, Beko G, Rosivall L, Remport A, Novak M, Mucsi I: Anemia is associated with mortality in kidney-transplanted patients: A prospective cohort study. Am J Transplant 7: 818-824, 2007
10. Lorenz M, Kletzmayr J, Perschl A, Furrer A, Horl WH, Sunder-Plassmann G: Anemia and iron deficiencies among long-term renal transplant recipients. J Am Soc Nephrol 13: 794-797, 2002
11. Yorgin PD, Scandling JD, Belson A, Sanchez J, Alexander SR, Andreoni KA: Late post-transplant anemia in adult renal transplant recipients: An under-recognized problem? Am J Transplant 2: 429-435, 2002
12. Vanrenterghem Y, Ponticelli C, Morales JM, Abramowicz D, Baboolal K, Eklund B, Kliem V, Legendre C, Morais Sarmento AL, Vincenti F: Prevalence and management of anemia in renal transplant recipients: A European survey. Am J Transplant 3: 835-845, 2003
13. Kasiske BL, Vazquez MA, Harmon WE, Brown RS, Danovitch GM, Gaston RS, Roth D, Scandling JD, Singer GG: Recommendations for the outpatient surveillance of renal transplant recipients. American Society of Transplantation. J Am Soc Nephrol 11[Suppl 15]: S1-S86, 2000
14. NKF-K/DOQI clinical practice guidelines and clinical practice recommendations for anemia in chronic kidney disease: 2007 update of hemoglobin target. Am J Kidney Dis 50: 471-530, 2007
15. Sun CH, Ward HJ, Paul WL, Koyle MA, Yanagawa N, Lee DB: Serum erythropoietin levels after renal transplantation. N Engl J Med 321: 151-157, 1989
16. Mix TC, Kazmi W, Khan S, Ruthazer R, Rohrer R, Pereira BJ, Kausz AT: Anemia: A continuing problem following kidney transplantation. Am J Transplant 3: 1426-1433, 2003
17. Molnar MZ, Mucsi I, Macdougall IC, Marsh JE, Yaqoob M, Main J, Courtney AE, Fogarty D, Mikhail A, Choukroun G, Short CD, Covic A, Goldsmith DJ: Prevalence and management of anaemia in renal transplant recipients: Data from ten European centres. Nephron Clin Pract 117: c127-c134, 2010
18. Gill JS, Abichandani R, Khan S, Kausz AT, Pereira BJ: Opportunities to improve the care of patients with kidney transplant failure. Kidney Int 61: 2193-2200, 2002
19. Miles AM, Markell MS, Daskalakis P, Sumrani NB, Hong J, Sommer BG, Friedman EA: Anemia following renal transplantation: Erythropoietin response and iron deficiency. Clin Transplant 11: 313-315, 1997
20. Zheng S, Coyne DW, Joist H, Schuessler R, Godboldo-Brooks A, Ercole P, Brennan DC: Iron deficiency anemia and iron losses after renal transplantation. Transpl Int 22: 434-440, 2009
21. Shah N, Al-Khoury S, Afzali B, Covic A, Roche A, Marsh J, Macdougall IC, Goldsmith DJ: Posttransplantation anemia in adult renal allograft recipients: Prevalence and predictors. Transplantation 81: 1112-1118, 2006
22. Winkelmayer WC, Kewalramani R, Rutstein M, Gabardi S, Vonvisger T, Chandraker A: Pharmacoepidemiology of anemia in kidney transplant recipients. J Am Soc Nephrol 15: 1347-1352, 2004
23. Jacobson PA, Schladt D, Oetting WS, Leduc R, Guan W, Matas AJ, Lamba V, Mannon RB, Julian BA, Israni A: Genetic determinants of mycophenolate-related anemia and leukopenia after transplantation. Transplantation 91: 309-316, 2011
24. Fishbane S, Cohen DJ, Coyne DW, Djamali A, Singh AK, Wish JB: Posttransplant anemia: The role of sirolimus. Kidney Int 76: 376-382, 2009
25. Friend P, Russ G, Oberbauer R, Murgia MG, Tufveson G, Chapman J, Blancho G, Mota A, Grandaliano G, Campistol JM, Brault Y, Burke JT: Incidence of anemia in sirolimustreated renal transplant recipients: The importance of preserving renal function. Transpl Int 20: 754-760, 2007
26. Kim MJ, Mayr M, Pechula M, Steiger J, Dickenmann M: Marked erythrocyte microcytosis under primary immunosuppression with sirolimus. Transpl Int 19: 12-18, 2006
27. Webster AC, Lee VW, Chapman JR, Craig JC: Target of rapa-mycin inhibitors (Sirolimus and Everolimus) for primary immunosuppression of kidney transplant recipients: A systematic review and meta-analysis of randomized trials. Transplantation 81: 1234-1248, 2006
28. Sofroniadou S, Kassimatis T, Goldsmith D: Anaemia, microcytosis and sirolimus: Is iron the missing link? Nephrol Dial Transplant 25: 1667-1675, 2010
29. Grinyo JM, Cruzado JM: Mycophenolate mofetil and sirolimus combination in renal transplantation. Am J Transplant 6: 1991-1999, 2006
30. Alonso-Santor JE, Gutierrez-Zufiaurre JL, Perez-Castrillon JL: Microangiopathic hemolytic anemia secondary to cyclosporine. Ann Pharmacother 38: 903, 2004
31. Reynolds JC, Agodoa LY, Yuan CM, Abbott KC: Thrombotic microangiopathy after renal transplantation in the United States. Am J Kidney Dis 42: 1058-1068, 2003
32. Udupa KB, Crabtree HM, Lipschitz DA: In vitro culture of proerythroblasts: Characterization of proliferative response to erythropoietin and steroids. Br J Haematol 62: 705-714, 1986
33. Golde DW, Bersch N, Cline MJ: Potentiation of erythropoiesis in vitro by dexamethasone. J Clin Invest 57: 57-62, 1976
34. Naik PM, Lyon GM 3rd, Ramirez A, Lawrence EC, Neujahr DC, Force S, Pelaez A: Dapsone-induced hemolytic anemia in lung allograft recipients. J Heart Lung Transplant 27: 1198-1202, 2008
35. Balfour HH Jr: Antiviral drugs. N Engl J Med 340: 1255-1268, 1999
36. Kim HC, Park SB, Han SY, Whang EA: Anemia following renal transplantation. Transplant Proc 35: 302-303, 2003
37. Moudgil A, Shidban H, Nast CC, Bagga A, Aswad S, Graham SL, Mendez R, Jordan SC: Parvovirus B19 infection-related complications in renal transplant recipients: Treatment with intravenous immunoglobulin. Transplantation 64: 1847-1850, 1997
38. Moffatt S, Yaegashi N, Tada K, Tanaka N, Sugamura K: Human parvovirus B19 nonstructural (NS1) protein induces apoptosis in erythroid lineage cells. J Virol 72: 3018-3028, 1998
39. Moffatt S, Tanaka N, Tada K, Nose M, Nakamura M, Muraoka O, Hirano T, Sugamura K: A cytotoxic nonstructural protein, NS1, of human parvovirus B19 induces activation of interleukin-6 gene expression. J Virol 70: 8485-8491, 1996
40. Baranski B, Armstrong G, Truman JT, Quinnan GV Jr, Straus SE, Young NS: Epstein-Barr virus in the bone marrow of patients with aplastic anemia. Ann Intern Med 109: 695-704, 1988
41. Apperley JF, Dowding C, Hibbin J, Buiter J, Matutes E, Sissons PJ, Gordon M, Goldman JM: The effect of cytomegalovirus on hemopoiesis: In vitro evidence for selective infection of marrow stromal cells. Exp Hematol 17: 38-45, 1989
42. Weiss G, Goodnough LT: Anemia of chronic disease. N Engl J Med 352: 1011-1023, 2005
43. Besarab A, Caro J, Jarrell BE, Francos G, Erslev AJ: Dynamics of erythropoiesis following renal transplantation. Kidney Int 32: 526-536, 1987
44. Wilflingseder J, Kainz A, Perco P, Korbely R, Mayer B, Oberbauer R: Molecular predictors for anaemia after kidney transplantation. Nephrol Dial Transplant 24: 1015-1023, 2009
45. Chua MS, Barry C, Chen X, Salvatierra O, Sarwal MM: Molecular profiling of anemia in acute renal allograft rejection using DNA microarrays. Am J Transplant 3: 17-22, 2003
46. Nicolas G, Chauvet C, Viatte L, Danan JL, Bigard X, Devaux I, Beaumont C, Kahn A, Vaulont S: The gene encoding the iron regulatory peptide hepcidin is regulated by anemia, hypoxia, and inflammation. J Clin Invest 110: 1037-1044, 2002
47. Malyszko J, Malyszko JS, Mysliwiec M: A possible role of hepcidin in the pathogenesis of anemia among kidney allograft recipients. Transplant Proc 41: 3056-3059, 2009
48. Ainsworth CD, Crowther MA, Treleaven D, Evanovitch D, Webert KE, Blajchman MA: Severe hemolytic anemia postrenal transplantation produced by donor anti-D passenger lymphocytes: Case report and literature review. Transfus Med Rev 23: 155-159, 2009
49. Kahwaji J, Barker E, Pepkowitz S, Klapper E, Villicana R, Peng A, Chang R, Jordan SC, Vo AA: Acute hemolysis after high-dose intravenous immunoglobulin therapy in highly HLA sensitized patients. Clin J Am Soc Nephrol 4: 1993-1997, 2009
50. Brunner B, Kropshofer G, Ellemunter H, Brunner A, Mueller T, Margreiter R, Tzankov A: Severe cold agglutinin disease caused by recurrent monomorphic Epstein-Barr virus (EBV)-associated post-transplant lymphoproliferative disorder (PTLD), clonally related to an EBV-negative plasmacytic hyperplasia in a pediatric multivisceral organ transplant recipient. Pediatr Transplant 11: 547-551, 2007
51. Bia M, Adey DB, Bloom RD, Chan L, Kulkarni S, Tomlanovich S: KDOQI US commentary on the 2009 KDIGO clinical practice guideline for the care of kidney transplant recipients. Am J Kidney Dis 56: 189-218, 2010
52. 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 14: 462-468, 2003
53. Rigatto C, Parfrey P, Foley R, Negrijn C, Tribula C, Jeffery J: Congestive heart failure in renal transplant recipients: Risk factors, outcomes, and relationship with ischemic heart disease. J Am Soc Nephrol 13: 1084-1090, 2002
54. Djamali A, Becker YT, Simmons WD, Johnson CA, Premasathian N, Becker BN: Increasing hematocrit reduces early posttransplant cardiovascular risk in diabetic transplant recipients. Transplantation 76: 816-820, 2003
55. 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 21: 3559-3566, 2006
56. Winkelmayer WC, Lorenz M, Kramar R, Horl WH, Sunder-Plassmann G: Percentage of hypochromic red blood cells is an independent risk factor for mortality in kidney transplant recipients. Am J Transplant 4: 2075-2081, 2004
57. Van Loo A, Vanholder R, Bernaert P, De Roose J, Lameire N: Recombinant human erythropoietin corrects anaemia during the first weeks after renal transplantation: A randomized prospective study. Nephrol Dial Transplant 11: 1815-1821, 1996
58. Choukroun G, Martinez F: Benefits of erythropoietin in renal transplantation. Transplantation 79: S49-S50, 2005
59. Choukroun GK, Dussol B, Etienne I, Cassuto-Viguier E, Toupance O, Glowacki F, Moulin B, Lebronchu Y, Touchard G, Le Meur Y, Martinez F: The complete correction of posttransplant anemia reduces the rate of progression of chronic allograft nephropathy. Am J Transplant 10 [Suppl S4]: 141, 2010
60. Choukroun GK, Dussol B, Etienne I, Al Najjar A, Lang P, Thierry A: The complete correction of post-transplant anemia improves graft survival: Results of a multicentre randomized study. J Am Soc Nephrol 21 [Suppl]: 803A, 2010
61. Martinez F, Kamar N, Pallet N, Lang P, Durrbach A, Lebranchu Y, Adem A, Barbier S, Cassuto-Viguier E, Glowaki F, Le Meur Y, Rostaing L, Legendre C, Hermine O, Choukroun G: High dose epoetin beta in the first weeks following renal transplantation and delayed graft function: Results of the Neo-PDGF study. Am J Transplant 10: 1695-1700, 2010
62. Heinze G, Kainz A, Horl WH, Oberbauer R: Mortality in renal transplant recipients given erythropoietins to increase haemoglobin concentration: Cohort study. BMJ 339: b4018, 2009
63. Pfeffer MA, Burdmann EA, Chen CY, Cooper ME, de Zeeuw D, Eckardt KU, Feyzi JM, Ivanovich P, Kewalramani R, Levey AS, Lewis EF, McGill JB, McMurray JJ, Parfrey P, Parving HH, Remuzzi G, Singh AK, Solomon SD, Toto R: A trial of darbepoetin alfa in type 2 diabetes and chronic kidney disease. N Engl J Med 361: 2019-2032, 2009
64. Singh AK, Szczech L, Tang KL, Barnhart H, Sapp S, Wolfson M, Reddan D: Correction of anemia with epoetin alfa in chronic kidney disease. N Engl J Med 355: 2085-2098, 2006
65. Drueke TB, Locatelli F, Clyne N, Eckardt KU, Macdougall IC, Tsakiris D, Burger HU, Scherhag A: Normalization of hemoglobin level in patients with chronic kidney disease and anemia. N Engl J Med 355: 2071-2084, 2006
66. Muirhead N, Cattran DC, Zaltzman J, Jindal K, First MR, Boucher A, Keown PA, Munch LC, Wong C: Safety and efficacy of recombinant human erythropoietin in correcting the anemia of patients with chronic renal allograft dysfunction. J Am Soc Nephrol 5: 1216-1222, 1994
67. Yoshimura N, Oka T, Ohmori Y, Aikawa I: Effects of recombinant human erythropoietin on the anemia of renal transplant recipients with chronic rejection. Transplantation 48: 527-529, 1989
68. Becker BN, Becker YT, Leverson GE, Heisey DM: Erythropoietin therapy may retard progression in chronic renal transplant dysfunction. Nephrol Dial Transplant 17: 1667-1673, 2002
69. National Kidney Foundation: K/DOQI clinical practice guidelines for chronic kidney disease: Evaluation, classification and stratification. Am J Kidney Dis 39[Suppl 1]: S1-S266, 2002