New Onset Diabetes Mellitus in Patients Receiving Calcineurin Inhibitors: A Systematic Review and Meta-Analysis

American Journal of Transplantation

Volumn 4, Issue 4, 2004, Pages 583-595

  Heisel, Olaf ^a,c   Heisel, Rochelle ^c   Balshaw, Robert ^b,c   Keown, Paul ^a,c  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b SIMON FRASER UNIVERSITY   (Canada)

^c Syreon Corporation   (Canada)

Author keywords

Cyclosporine; Diabetes mellitus; Heart; Kidney; Liver; Lung; Tacrolimus; Transplantation

Indexed keywords

AZATHIOPRINE; CALCINEURIN INHIBITOR; CORTICOSTEROID; CYCLOSPORIN A; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; RAPAMYCIN; STEROID; TACROLIMUS;

CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DATA BASE; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; INCIDENCE; INSULIN DEPENDENT DIABETES MELLITUS; META ANALYSIS; ORGAN TRANSPLANTATION; PRIORITY JOURNAL; PROSPECTIVE STUDY; QUANTITATIVE ANALYSIS; RANDOMIZED CONTROLLED TRIAL; REVIEW;

CALCINEURIN; CYCLOSPORINE; DIABETES MELLITUS; DIABETES MELLITUS, TYPE 1; HUMANS; IMMUNOSUPPRESSIVE AGENTS; ORGAN TRANSPLANTATION; PROSPECTIVE STUDIES; RETROSPECTIVE STUDIES; TACROLIMUS; TIME FACTORS;

EID: 1942502245     PISSN: 16006135     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1600-6143.2003.00372.x     Document Type: Review

References (100)

1. Anonymous. A comparison of tacrolimus (FK 506) and cyclosporine for immunosuppression in liver transplantation. The U.S. Multicenter FK506 Liver Study Group. N Engl J Med 1994; 331: 1110-1115.
2. Anonymous. Randomised trial comparing tacrolimus (FK506) and cyclosporin in prevention of liver allograft rejection. European FK506 Multicentre Liver Study Group. Lancet 1994; 344: 423-428.
3. Plosker GL, Foster RH. Tacrolimus: a further update of its pharmacology and therapeutic use in the management of organ transplantation. Drugs 2000; 59: 323-389.
4. Lazzaro C, McKechnie T, McKenna M. Tacrolimus versus cyclosporin in renal transplantation in Italy: cost-minimisation and cost-effectiveness analyses. J Nephrol 2002; 15: 580-588.
5. Vincenti F, Jensik SC, Filo RS, Miller J, Pirsch J. A long-term comparison of tacrolimus (FK506) and cyclosporine in kidney transplantation: evidence for improved allograft survival at five years. Transplantation 2002; 73: 775-782. [erratum appears in Transplantation 2002 April 27; 73 (8): 1370].
6. Vincenti F, Jensik SC, Filo RS, Miller J, Pirsch J. A long-term comparison of tacrolimus (FK506) and cyclosporine in kidney transplantation: evidence for improved allograft survival at five years. Transplantation 2002; 73: 775-782. [erratum appears in Transplantation 2002 April 27; 73 (8): 1370].
7. Ahsan N, Johnson C, Gonwa T et al. Randomized trial of tacrolimus plus mycophenolate mefetil or azathioprine versus cyclosporine oral solution (modified) plus mycophenolate mofetil after cadaveric kidney transplantation: results at 2 years. Transplantation 2001; 72: 245-250.
8. Taylor DO, Barr ML, Radovancevic B et al. A randomized, multicenter comparison of tacrolimus and cyclosporine immunosuppressive regimens in cardiac transplantation: decreased hyperlipidemia and hypertension with tacrolimus. J Heart Lung Transplant 1999; 18: 336-345.
9. Pirsch JD. Randomized multicenter trial with traditional formulation of cyclosporine. Presented at Transplant 2000; Chicago; Illinois, May 13-17, 2000.
10. Henry ML. Cyclosporine and tacrolimus (FK506): a comparison of efficacy and safety profiles. Clin Transplant 1999; 13: 209-220.
11. Ligtenberg G, Hene RJ, Blankestijn PJ, Koomans HA. Cardiovascular risk factors in renal transplant patients: cyclosporin A versus tacrolimus. J Am Soc Nephrol 2001; 12: 368-373.
12. Pham SM, Kormos RL, Hattler BG et al. A prospective trial of tacrolimus (FK 506) in clinical heart transplantation: intermediate-term results. J Thorac Cardiovasc Surg 1996; 111: 764-772.
13. Reichart B, Meiser B, Vigano M et al. European Multicenter Tacrolimus (FK506) Heart Pilot Study: one-year results - European Tacrolimus Multicenter Heart Study Group. J Heart Lung Transplant 1998; 17: 775-781.
14. Rinaldi M, Pellegrini C, Martinelli L et al. FK506 effectiveness in reducing acute rejection after heart transplantation: a prospective randomized study. J Heart Lung Transplant 1997; 16: 1001-1010.
15. Taylor DO, Barr ML, Radovancevic B et al. A randomized, multicenter comparison of tacrolimus and cyclosporine immunosuppressive regimens in cardiac transplantation: decreased hyperlipidemia and hypertension with tacrolimus. J Heart Lung Transplant 1999; 18: 336-345.
16. Woodward RS, Schnitzler MA, Baty J et al. Incidence and cost of new onset diabetes mellitus among U.S. wait-listed and transplanted renal allograft recipients. Am J Transplant 2003; 3: 590.
17. Sumrani NB, Delaney V, Ding ZK et al. Diabetes mellitus after renal transplantation in the cyclosporine era - an analysis of risk factors. Transplantation 1991; 51: 343-347.
18. Weir MR, Fink JC. Risk for posttransplant Diabetes mellitus with current immunosuppressive medications. Am J Kidney Dis 1999; 34: 1-13.
19. Roth D, Milgrom M, Esquenazi V, Fuller L, Burke G, Miller J. Posttransplant hyperglycemia. Increased incidence in cyclosporine-treated renal allograft recipients. Transplantation 1989; 47: 278-281.
20. Miles AM, Sumrani N, Horowitz R et al. Diabetes mellitus after renal transplantation: as deleterious as non-transplant-associated diabetes? Transplantation 1998; 65: 380-384.
21. Hricik DE, Almawi WY, Strom TB. Trends in the use of glucocorticoids in renal transplantation. Transplantation 1994; 57: 979-989.
22. Yoshimura N, Nakai I, Ohmori Y et al. Effect of cyclosporine on the endocrine and exocrine pancreas in kidney transplant recipients. Am J Kidney Dis 1988; 12: 11-17.
23. Rao M, Jacob CK, Shastry JC. Post-renal transplant diabetes mellitus-a retrospective study. Nephrol Dial Transplant 1992; 7: 1039-1042.
24. von Kiparski A, Frei D, Uhlschmid G, Largiader F, Binswanger U. Post-transplant diabetes mellitus in renal allograft recipients: a matched-pair control study. Nephrol Dial Transplant 1990; 5: 220-225.
25. Hricik DE, MAOT. Schulak JA, Herson J. Steroid-free immunosuppression in cyclosporine-treated renal transplant recipients: a meta-analysis. J Am Soc Nephrol 1993; 4: 1300-1305.
26. Peters DH, Fitton A, Plosker GL, Faulds D, Tacrolimus. A review of its pharmacology, and therapeutic potential in hepatic and renal transplantation. Drugs 1993; 46: 746-794.
27. Spencer CM, Goa KL, Gillis JC, Tacrolimus. An update of its pharmacology and clinical efficacy in the management of organ transplantation. Drugs 1997; 54: 925-975.
28. Pirsch JD, Miller J, Deierhoi MH, Vincenti F, Filo RS. A comparison of tacrolimus (FK506) and cyclosporine for immunosuppression after cadaveric renal transplantation. FK506 Kidney Transplant Study Group. Transplantation 1997; 63: 977-983.
29. Jadad AR, Moore RA, Carroll D et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials 1996; 17: 1-12.
30. Markell M, Salifu M, Stratilatova M et al. Comparison of risk for post-transplant diabetes (PTDM) in age-stratifies cyclosporine and tacrolimus-treated patients, American Transplant Congress, Abstract 208, 2002.
31. Jevnikar AM, Cole E, Zaltzman JS et al. A retrospective analysis of the clinical indications and efficacy of tacrolimus in non-study renal transplant patients in Ontario, Canada. The 2nd International Congress on Immunosuppression, Abstract P-96 2001, 135.
32. Sperschneider H. A large, multicentre trial to compare the efficacy and safety of tacrolimus with cyclosporine microemulsion following renal transplantation. Transplant Proc 2001; 33: 1279-1281.
33. van Duijnhoven EM, Christiaans MH, Boots JM, Nieman FH, Wolffenbuttel BH, van Hooff JP. Glucose metabolism in the first 3 years after renal transplantation in patients receiving tacrolimus versus cyclosporine-based immunosuppression. J Am Soc Nephrol 2002; 13: 213-220.
34. Johnson C, Ahsan N, Gonwa T et al. Randomized trial of tacrolimus (Prograf) in combination with azathioprine or mycophenolate mofetil versus cyclosporine (Neoral) with mycophenolate mofetil after cadaveric kidney transplantation. Transplantation 2000; 69: 834-841.
35. Morris-Stiff G, Ostrowski K, Balaji V et al. Prospective randomised study comparing tacrolimus (Prograf) and cyclosporin (Neoral) as primary immunosuppression in cadaveric renal transplants at a single institution: interim report of the first 80 cases. Transplant Int 1998; 11: S334-S336.
36. Neylan JF. Racial differences in renal transplantation after immunosuppression with tacrolimus versus cyclosporine. FK506 Kidney Transplant Study Group. Transplantation 1998; 65: 515-523.
37. Mayer AD, Dmitrewski J, Squifflet JP et al Multicenter randomized trial comparing tacrolimus (FK506) and cyclosporine in the prevention of renal allograft rejection: a report of the European Tacrolimus Multicenter Renal Study Group. Transplantation 1997; 64: 436-443.
38. Vincenti F, Laskow DA, Neylan JF, Mendez R, Matas AJ. One-year follow-up of an open-label trial of FK506 for primary kidney transplantation. A report of the U.S. Multicenter FK506 Kidney Transplant Group. Transplantation 1996; 61: 1576-1581.
39. Senninger N, Golling M, Datsis K, Sido B, Herfarth C, Otto G. Glucose metabolism following liver transplantation and immunosuppression with cyclosporine A or FK 506. Transplant Proc 1995; 27: 1127-1128.
40. Meiser BM, Uberfuhr P, Fuchs A et al. Single-center randomized trial comparing tacrolimus (FK506) and cyclosporine in the prevention of acute myocardial rejection. J Heart Lung Transplant 1998; 17: 782-788.
41. Depczynski B, Daly B, Campbell LV, Chisholm DJ, Keogh A. Predicting the occurrence of diabetes mellitus in recipients of heart transplants. Diabet Med 2000; 17: 15-19.
42. Reichenspurner H, Kur F, Treede H et al. Optimization of the immunosuppressive protocol after lung transplantation. Transplantation 1999; 68: 67-71.
43. Kur F, Reichenspurner H, Meiser BM et al. Tacrolimus (FK506) as primary immunosuppressant after lung transplantation. Thorac Cardiovasc Surg 1999; 47: 174-178.
44. Bismuth H. Comparison of FK 506- and cyclosporine-based immunosuppression: FK 506 therapy significantly reduces the incidence of acute, steroid-resistant, refractory, and chronic rejection whilst possessing a comparable safety profile. European FK 506 Multicenter Liver Study Group. Transplant Proc 1995; 27: 45-49.
45. Lohmann T, List C, Lamesch P et al. Diabetes mellitus and islet cell specific autoimmunity as adverse effects of immunsuppressive therapy by FK506/tacrolimus. Exp Clin Endocrinol Diabetes 2000; 108: 347-352.
46. Stegall MD, Wachs ME, Everson G et al. Prednisone withdrawal 14 days after liver transplantation with mycophenolate: a prospective trial of cyclosporine and tacrolimus. Transplantation 1997; 64: 1755-1760.
47. Steinmuller TM, Graf KJ, Schleicher J et al. The effect of FK506 versus cyclosporine on glucose and lipid metabolism - a randomized trial. Transplantation 1994; 58: 669-674.
48. Groetzner J, Meiser BM, Schirmer J et al. Tacrolimus or cyclosporine for immunosuppression after cardiac transplantation: which treatment reveals more side effects during long-term follow-up? Transplant Proc 2001; 33: 1461-1464.
49. Kasiske BL, Snyder JJ, Gilbertson D, Matas AJ. Diabetes mellitus after kidney transplantation in the United States. Am J Transplant 2003; 3: 178-185.
50. Villamil F, Ericzon BG, Risaliti A et al. Efficacy and safety of cyclosporine microemulsion with C2 monitoring versus tacrolimus in de novo liver transplant recipients. Presented at 2003 International Liver Transplant Society Meeting. Barcelona, Spain, 2003.
51. Jang HJ, Kim SC, Han DJ. Comparison of pancreas transplantation outcome between the cyclosporine and tacrolimus eras. Transplant Proc 2000; 32: 2470-2471.
52. Land W, Malaise J, Sandberg J, Langrehr J. Tacrolimus versus cyclosporine in primary simultaneous pancreas-kidney transplantation: preliminary results at 1 year of a large multicenter trial. Transplant Proc 2002; 34: 1911-1912.
53. Woeste G, Wullstein C, Dette K, Pridohl O, Lubke P, Bechstein WO. Tacrolimus/mycophenolate mofetil vs cyclosporine A/Azathioprine after simultaneous pancreas and kidney transplantation: five-year results of a randomized study. Transplant Proc 2002; 34: 1920-1921.
54. Hahn HJ, Laube F, Lucke S, Kloting I, Kohnert KD, Warzock R. Toxic effects of cyclosporine on the endocrine pancreas of Wistar rats. Transplantation 1986; 41: 44-47.
55. Wahlstrom HE, Akimoto R, Endres D, Kolterman O, Moossa AR. Recovery and hypersecretion of insulin and reversal of insulin resistance after withdrawal of short-term cyclosporine treatment. Transplantation 1992; 53: 1190-1195.
56. Nielsen JH, Mandrup-Poulsen T, Nerup J. Direct effects of cyclosporin A on human pancreatic beta-cells. Diabetes 1986; 35: 1049-1052.
57. Strasser S, Alejandro R, Shapiro ET, Ricordi C, Todo S, Mintz DH. Effect of FK506 on insulin secretion in normal dogs. Metabolism 1992; 41: 64-67.
58. Ricordi C, Zeng YJ, Alejandro R et al. In vivo effect of FK506 on human pancreatic islets. Transplantation 1991; 52: 519-522.
59. Hirano Y, Fujihira S, Ohara K, Katsuki S, Noguchi H. Morphological and functional changes of islets of Langerhans in FK506-treated rats. Transplantation 1992; 53: 889-894.
60. Hahn HJ, Dunger A, Laube F et al. Reversibility of the acute toxic effect of cyclosporin A on pancreatic B cells of Wistar rats. Diabetologia 1986; 29: 489-494.
61. Krentz AJ, Dousset B, Mayer D et al. Metabolic effects of cyclosporin A and FK 506 in liver transplant recipients. Diabetes 1993; 42: 1753-1759.
62. Ekstrand AV, Eriksson JG, Gronhagen-Riska C, Ahonen PJ, Groop LC. Insulin resistance and insulin deficiency in the pathogenesis of posttransplantation diabetes in man. Transplantation 1992; 53: 563-569.
63. Marks WH, Harding MW, Handschumacher R, Marks C, Lorber MI. The immunochemical distribution of cyclophilin in normal mammalian tissues. Transplantation 1991; 52: 340-345.
64. Tamura K, Fujimura T, Tsutsumi T et al. Transcriptional inhibition of insulin by FK506 and possible involvement of FK506 binding protein-12 in pancreatic beta-cell. Transplantation 1995; 59: 1606-1613.
65. Emre S, Genyk Y, Schluger LK et al. Treatment of tacrolimus-related adverse effects by conversion to cyclosporine in liver transplant recipients. Transpl Int 2000; 13: 73-78.
66. Mor E, Sheiner PA, Schwartz ME, Emre S, Guy S, Miller CM. Reversal of severe FK506 side effects by conversion to cyclosporine-based immunosuppression. Transplantation 1994; 58: 380-382.
67. Tabasco-Minguillan J, Mieles L, Carroll P, Gavaler J, Van Thiel DH, Starzl TE. Long-term insulin requirement after liver transplantation with FK 506 in American veterans. Transplant Proc 1993; 25: 677-678.
68. Baid S, Rubin N, Delmonico FL et al. Tacrolimus-associated posttransplant diabetes in renal transplant reciepients: an analysis of risk factors and role of hepatitis C infection. American Transplant Congress, Abstract 57, 2002.
69. Bloom RD, Rao V, Weng F, Grossman RA, Cohen D, Mange KC. Association of hepatitis C with posttransplant diabetes in renal transplant patients on tacrolimus. J Am Soc Nephrol 2002; 13: 1374-1380.
70. First MR, Gerber DA, Hariharan S, Kaufman DB, Shapiro R. Posttransplant diabetes mellitus in kidney allograft recipients: incidence, risk factors, and management. Transplantation 2002; 73: 379-386.
71. Johny KV, Nampoory MRN, Costandi JN et al. High incidence of post-transplant diabetes mellitus in Kuwait. Diabetes Res Clin Pract 2002; 55: 123-130.
72. Mysore S, Kumar A, Fa K et al. Steroid avoidance (SA) in kidney transplant recipients treated with simulect (Bmab), Neoral (CsA) and cellcept (MMF) - a randomized prospective controlled clinical trial. American Transplant Congress, Abstract 1012, 2002.
73. Panz VRBR, Raal FJ, Maher H, Hsu HC, Joffe BI. Diabetogenic effect of tacrolimus in South African patients undergoing kidney transplantation. Transplantation 2002; 73: 587-590.
74. Boots JM, van Duijnhoven EM, Christiaans MH, Nieman FH, van Suylen RJ, van Hooff JP. Single-center experience with tacrolimus versus cyclosporine-Neoral in renal transplant recipients. Transpl Int 2001; 14: 370-383.
75. Busque S, Boucher A, Zaltzman JS et al. A prospective evaluation of tacrolimus-based immunosuppressive therapy in highly sensitized renal allograft recipients. International Congress on Immunosuppression, Abstract P-92, 2001, 134.
76. Cosio FG, Pesavento TE, Osei K, Henry ML, Ferguson RM. Posttransplant diabetes mellitus: increasing incidence in renal allograft recipients transplanted in recent years. Kidney Int 2001; 59: 732-737.
77. Van Duijnhoven EM, Boots JMM, Christiaans MHL, Wolffenbuttel BHR, Van Hooff JP. Influence of tacrolimus on glucose metabolism before and after renal transplantation: a prospective study. J Am Soc Nephrol 2001; 12: 583-588.
78. Hjelmesaeth J, Hartmann A, Kofstad J, Egeland T, Stenstrom J, Fauchald P. Tapering off prednisolone and cyclosporin the first year after renal transplantation: the effect on glucose tolerance. Nephrol Dial Transplant 2001; 16: 829-835.
79. Maes BD, Kuypers D, Messiaen T et al. Posttransplantation diabetes mellitus in FK-506-treated renal transplant recipients: analysis of incidence and risk factors. Transplantation 2001; 72: 1655-1661.
80. Mourad G, Garrigue V, Squifflet JP et al. Induction versus non-induction in renal transplant recipients with tacrolimus-based immunosuppression. Transplantation 2001; 72: 1050-1055.
81. Nam JH, Mun JI, Kim SI et al. beta-Cell dysfunction rather than insulin resistance is the main contributing factor for the development of postrenal transplantation diabetes mellitus. Transplantation 2001; 71: 1417-1423.
82. Revanur VK, Jardine AG, Kingsmore DB, Jaques BC, Hamilton DH, Jindal RM. Influence of diabetes mellitus on patient and graft survival in recipients of kidney transplantation. Clin Transplant 2001; 15: 89-94.
83. Jawad F, Rizvi SA. Posttransplant diabetes mellitus in live-related renal transplantation. Transplant Proc 2000; 32: 1888.
84. Khoury N, Kriaa F, Hiesse C et al. Posttransplant diabetes mellitus in kidney transplant recipients under tacrolimus immunosuppression. Transplant Proc 2000; 32: 2763-2764.
85. Miller J, Mendez R, Pirsch JD, Jensik SC. Safety and efficacy of tacrolimus in combination with mycophenolate mofetil (MMF) in cadaveric renal transplant recipients. FK506/MMF Dose-Ranging Kidney Transplant Study Group. Transplantation 2000; 69: 875-880.
86. Park K, Ahn C, Bang BK et al. Efficacy of tacrolimus in primary kidney transplant patients: multicenter, open-label prospective study. Transplant Proc 2000; 32: 1705-1708.
87. Segoloni G, Bonomini V, Maresca MC et al. Tacrolimus is highly effective in both dual and triple therapy regimens following renal transplantation. Spanish and Italian Tacrolimus Study Group. Transpl Int 2000; 13: S336-S340.
88. Silva F, Queiros J, Vargas G, Henriques A, Sarmento A, Guimaraes S. Risk factors for posttransplant diabetes mellitus and impact of this complication after renal transplantation. Transplant Proc 2000; 32: 2609-2610.
89. Mancilla UE, Martinez NB, Alberu J, Diliz H. Primary immunosuppression with tacrolimus in renal transplantation: a multicenter, open-label study. Adv Ther 1999; 16: 210-218.
90. Shapiro R, Jordan ML, Scantlebury VP et al. A prospective, randomized trial of tacrolimus/prednisone versus tacrolimus/prednisone/mycophenolate mofetil in renal transplant recipients. Transplantation 1999; 67: 411-415.
91. Tanabe K, Ishikawa N, Tokumoto T et al. Long-term results of living kidney transplantation under tacrolimus immunosuppression: a single-center experience. Transplant Proc 1998; 30: 1224-1226.
92. Saxena S, Dash SC, Guleria S et al. Post transplant diabetes mellitus in live related renal allograft recipients: a single centre experience. J Assoc Physicians India 1996; 44: 477-479.
93. AlDosary AA, Ramji AS, Elliott TG et al. Post-liver transplantation diabetes mellitus: An association with hepatitis C. Liver Transplant 2002; 8: 356-361.
94. Lerut JP, Ciccarelli O, Mauel E et al. Adult liver transplantation and steroidazathioprine withdrawal in cyclosporine (Sandimmun) -based immunosuppression 5 year results of a prospective study. Transpl Int 2001; 14: 420-428.
95. Washburn K, Speeg KV, Esterl R et al. Steroid elimination 24 hours after liver transplantation using daclizumab, tacrolimus, and mycophenolate mofetil. Transplantation 2001; 72: 1675-1679.
96. Belli LS, De Carlis L, Rondinara G et al. Early cyclosporine monotherapy in liver transplantation: a 5-year follow-up of a prospective, randomized trial. Hepatology 1998; 27: 1524-1529.
97. Cai TH, Esterl RM Jr, Nichols L, Cigarroa F, Speeg KV, Halff GA. Improved immunosuppression with combination tacrolimus (FK506) and mycophenolic acid in orthotopic liver transplantation. Transplant Proc 1998; 30: 1413-1414.
98. Jain ARJ, Kashyap R, Rohal S et al. Liver transplantation under tacrolimus in infants, children, adults, and seniors: long-term results, survival, and adverse events in 1000 consecutive patients. Tranplant Proc 1998; 30: 1403-1404.
99. Margarit C, Rimola A, Gonzalez-Pinto I et al. Efficacy and safety of oral low-dose tacrolimus treatment in liver transplantation. Transpl Int 1998; 11: S260-S266.
100. Jindal RM, Popescu I, Schwartz ME, Emre S, Boccagni P, Miller CM. Diabetogenicity of FK506 versus cyclosporine in liver transplant recipients. Transplantation 1994; 58: 370-372.