The importance of different immunosuppressive regimens in the development of posttransplant diabetes mellitus

Pediatric Diabetes

Volumn 13, Issue 1, 2012, Pages 81-91

  Prokai, A ^a   Fekete, A ^a   Pasti, K ^a   Rusai, K ^a   Banki, N F ^a   Reusz, G ^a   Szabo, A J ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Aza; CAMP; CV; CyA; DM; FKBP; FPG; HNF; HOMA R; IFG; IGT; IL; Immunosuppressants; IMPDH; MMF; MODY; MTOR; NFATc; OGTT; PTDM; Sir; Tac; Transplantation

Indexed keywords

AZATHIOPRINE; BASILIXIMAB; CALCINEURIN; CALCINEURIN INHIBITOR; CHLORAMPHENICOL ACETYLTRANSFERASE; CYCLOSPORIN A; FK 506 BINDING PROTEIN; GLUCOSE TRANSPORTER 1; GLYCOGEN SYNTHASE; HEPATOCYTE NUCLEAR FACTOR 4; INSULIN; INTERLEUKIN 2; MAMMALIAN TARGET OF RAPAMYCIN; METHYLPREDNISOLONE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; POLYAMINE; PREDNISOLONE; RAPAMYCIN; S6 KINASE; STEROID; TACROLIMUS; TRANSCRIPTION FACTOR NFAT;

ACUTE GRAFT REJECTION; CORTICOSTEROID THERAPY; DIABETES MELLITUS; DIABETOGENESIS; DISEASE ASSOCIATION; DOSE RESPONSE; DRUG DOSE REDUCTION; DRUG MECHANISM; DRUG MEGADOSE; DRUG PULSE THERAPY; DRUG SAFETY; DRUG SUBSTITUTION; DRUG WITHDRAWAL; GINGIVA HYPERPLASIA; GLUCOSE INTOLERANCE; GRAFT SURVIVAL; HEART TRANSPLANTATION; HIRSUTISM; HUMAN; HYPERLIPIDEMIA; HYPERTENSION; IMMUNOSUPPRESSIVE TREATMENT; IMPAIRED GLUCOSE TOLERANCE; INSULIN RELEASE; INSULIN RESISTANCE; INSULIN SENSITIVITY; KIDNEY TRANSPLANTATION; LIVER TRANSPLANTATION; LOW DRUG DOSE; LUNG TRANSPLANTATION; MAINTENANCE DRUG DOSE; MULTICENTER STUDY (TOPIC); NEPHROTOXICITY; NONHUMAN; PANCREAS ISLET BETA CELL; POSTTRANSPLANT DIABETES MELLITUS; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; RISK FACTOR; TRANSCRIPTION REGULATION;

CHILD; DIABETES MELLITUS; HUMANS; IMMUNOSUPPRESSION; IMMUNOSUPPRESSIVE AGENTS; MODELS, BIOLOGICAL; ORGAN TRANSPLANTATION; POSTOPERATIVE COMPLICATIONS; RISK FACTORS; TRANSPLANTATION CONDITIONING;

EID: 84856370688     PISSN: 1399543X     EISSN: 13995448     Source Type: Journal    
DOI: 10.1111/j.1399-5448.2011.00782.x     Document Type: Review

References (88)

1. Hariharan S, Johnson CP, Bresnahan BA, Taranto SE, McIntosh MJ, Stablein D. Improved graft survival after renal transplantation in the United States, 1988 to 1996. N Engl J Med 2000: 342: 605-612.
2. Briganti EM, Russ GR, McNeil JJ, Atkins RC, Chadban SJ. Risk of renal allograft loss from recurrent glomerulonephritis. N Engl J Med 2002: 347: 103-109.
3. Kasiske BL, Snyder JJ, Gilbertson D, Matas AJ. Diabetes mellitus after kidney transplantation in the United States. Am J Transplant 2003: 3: 178-185.
4. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2004: 27: 5-10.
5. Heisel O, Heisel R, Balshaw R, Keown P. New onset diabetes mellitus in patients receiving calcineurin inhibitors: a systematic review and meta-analysis. Am J Transplant 2004: 4: 583-595.
6. Davidson J, Wilkinson A, Dantal J et al. International Expert Panel. New-onset diabetes after transplantation: 2003 International consensus guidelines. Proceedings of an international expert panel meeting. Barcelona, Spain, 19 February 2003. Transplantation 2003: 75: 3-24.
7. Montori VM, Basu A, Erwin PJ, Velosa JA, Gabriel SE, Kudva YC. Post-transplantation diabetes: a systematic review of the literature. Diabetes Care 2002: 25: 583-592.
8. Sezer S, Akgul A, Altinoglu A, Arat Z, Ozdemir FN, Haberal M. Posttransplant diabetes mellitus: impact of good blood glucose regulation on renal transplant recipient outcome. Transplant Proc 2006: 38: 533-536.
9. Matas AJ, Gillingham KJ, Humar A et al. Posttransplant diabetes mellitus and acute rejection: impact on kidney transplant outcome. Transplantation 2008: 85: 338-343.
10. Helanterä I, Ortiz F, Räisänen-Sokolowski A, Koskinen P. Impact of glucose metabolism abnormalities on histopathological changes in kidney transplant protocol biopsies. Transpl Int 2010: 23: 374-381.
11. Greenspan LC, Gitelman SE, Leung MA, Glidden DV, Mathias RS. Increased incidence in post-transplant diabetes mellitus in children: a case-control analysis. Pediatr Nephrol 2002: 17: 1-5.
12. Al-Uzri A, Stablein DM, Cohn RA. Post-transplant diabetes mellitus in pediatric renal transplant recipients: a report of the North American Pediatric Renal Transplant Cooperative Study (NAPRTCS). Transplantation 2001: 72: 1020-1024.
13. Burroughs TE, Swindle JP, Salvalaggio PR et al. Increasing incidence of new-onset diabetes after transplant among pediatric renal transplant patients. Transplantation 2009: 88: 367-373.
14. Jain AB, Fung JJ, Tzakis AG et al. Comparative study of cyclosporine and FK 506 dosage requirements in adult and pediatric orthotropic liver transplant patients. Transplant Proc 1991: 23: 2763-2766.
15. Deierhoi MH, Haug M III. Review of select transplant subpopulations at high risk of failure from standard immunosuppressive therapy. Clin Transplant 2000: 14: 439-448.
16. Starzl TE, Todo S, Fung J, Demetris AJ, Venkataramman R, Jain A. FK 506 for liver, kidney, and pancreas transplantation. Lancet 1989: 2: 1000-1004.
17. Webster AC, Woodroffe RC, Taylor RS, Chapman JR, Craig JC. Tacrolimus versus cyclosporine as primary immunosuppression for kidney transplant recipients: meta-analysis and meta-regression of randomized trial data. BMJ 2005: 331: 810.
18. 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.
19. Oetjen E, Baun D, Beimesche S et al. Inhibition of human insulin gene transcription by the immunosuppressive drugs cyclosporine A and tacrolimus in primary, mature islets of transgenic mice. Mol Pharmacol 2003: 63: 1289-1295.
20. Redmon JB, Olson LK, Armstrong MB, Greene MJ, Robertson RP. Effects of tacrolimus (FK506) on human insulin gene expression, insulin mRNA levels, and insulin secretion in HIT-T15 cells. J Clin Invest 1996: 98: 2786-2793.
21. Radu RG, Fujimoto S, Mukai E et al. Tacrolimus suppresses glucose-induced insulin release from pancreatic islets by reducing glucokinase activity. Am J Physiol Endocrinol Metab 2005: 288: 365-371.
22. van Hooff JP, Christiaans MH, van Duijnhoven EM. Evaluating mechanisms of post-transplant diabetes mellitus. Nephrol Dial Transplant 2004: 19: 8-12.
23. Boots JM, van Duijnhoven EM, Christiaans MH, Wolffenbuttel BH, van Hooff JP. Glucose metabolism in renal transplant recipients on tacrolimus: the effect of steroid withdrawal and tacrolimus trough level reduction. J Am Soc Nephrol 2002: 13: 221-227.
24. Rodrigo E, Piñera C, de Cos MA et al. Evolution of tacrolimus blood levels and concentration-dose ratios in patients who develop new onset diabetes mellitus after kidney transplantation. Transpl Int 2005: 18: 1152-1157.
25. Filler G, Webb NJ, Milford DV et al. Four-year data after pediatric renal transplantation: a randomized trial of tacrolimus vs. cyclosporine micro emulsion. Pediatr Transplant 2005: 9: 498-503.
26. Hathout E, Alonso E, Anand R et al. SPLIT study group. Post-transplant diabetes mellitus in pediatric liver transplantation. Pediatr Transplant 2009: 13: 599-605.
27. Hathout EH, Chinnock RE, Johnston JK et al. Pediatric post-transplant diabetes: data from a large cohort of pediatric heart-transplant recipients. Am J Transplant 2003: 3: 994-998.
28. Prokai A, Fekete A, Kis E et al. Post-transplant diabetes mellitus in children following renal transplantation. Pediatr Transplant 2008: 12: 643-649.
29. Kuo HT, Poommipanit N, Sampaio M, Reddy P, Cho YW, Bunnapradist S. Risk factors for development of new-onset diabetes mellitus in pediatric renal transplant recipients: an analysis of the OPTN/UNOS database. Transplantation 2010: 89: 434-439.
30. Filler G, Neuschulz I, Vollmer I, Amendt P, Hocher B. Tacrolimus reversibly reduces insulin secretion in paediatric renal transplant recipients. Nephrol Dial Transplant 2000: 15: 867-871.
31. Butani L, Makker SP. Conversion from tacrolimus to neoral for post-renal transplant diabetes. Pediatr Nephrol 2000: 15: 176-178.
32. Borel JF, Feurer C, Gubler HU, Stähelin H. Biological effects of cyclosporine A: a new antilymphocytic agent. Agents Actions 1976: 6: 468-475.
33. Robertson RP, Franklin G, Nelson L. Intravenous glucose tolerance and pancreatic islet beta-cell function in patients with multiple sclerosis during 2-yr treatment with cyclosporine. Diabetes 1989: 38: 58-64.
34. Esmatjes E, Ricart MJ, Ferrer JP, Oppenhaimer F, Vilardell J, Casamitjana R. Cyclosporine's effect on insulin secretion in patients with kidney transplants. Transplantation 1991: 52: 500-503.
35. Sjöholm A. Inhibitory effects of cyclosporine A on rat insulinoma cell proliferation, polyamine content and insulin secretion. Mol Cell Endocrinol 1994: 99: 21-24.
36. Borlak J, Niehof M. HNF4alpha and HNF1alpha dysfunction as a molecular rational for cyclosporine induced post-transplantation diabetes mellitus. PLoS One 2009: 4: 4662.
37. Yale JF, Roy RD, Grose M, Seemayer TA, Murphy GF, Marliss EB. Effects of cyclosporine on glucose tolerance in the rat. Diabetes 1985: 34: 1309-1313.
38. Hahn HJ, Laube R, Klöting I. Is the cyclosporine A toxicity on rat pancreatic B-cells modulated by the MHC? Exp Clin Endocrinol 1989: 93: 203-207.
39. Bouchta NB, Ghisdal L, Abramowicz D et al. Conversion from tacrolimus to cyclosporine is associated with a significant improvement of glucose metabolism in patients with new-onset diabetes mellitus after renal transplantation. Transplant Proc 2005: 37: 1857-1860.
40. Ramos-Cebrián M, Torregrosa JV, Gutiérrez-Dalmau A, Oppenheimer F, Campistol JM. Conversion from tacrolimus to cyclosporine could improve control of post-transplant diabetes mellitus after renal transplantation. Transplant Proc 2007: 39: 2251-2253.
41. Romagnoli J, Citterio F, Violi P, Nanni G, Castagneto M. Post-transplant diabetes mellitus after kidney transplantation with different immunosuppressive agents. Transplant Proc 2004: 36: 690-691.
42. Luan FL, Zhang H, Schaubel DE et al. Comparative risk of impaired glucose metabolism associated with cyclosporine versus tacrolimus in the late post-transplant period. Am J Transplant 2008: 8: 1871-1877.
43. Vincenti F, Friman S, Scheuermann E et al.; DIRECT (Diabetes Incidence after Renal Transplantation: Neoral C Monitoring Versus Tacrolimus) Investigators. Results of an international, randomized trial comparing glucose metabolism disorders and outcome with cyclosporine versus tacrolimus. Am J Transplant 2007: 7: 1506-1514.
44. Shishido S, Sato H, Asanuma H et al. Unexpectedly high prevalence of pre-transplant abnormal glucose tolerance in pediatric kidney transplant recipients. Pediatr Transplant 2006: 10: 67-73.
45. Sehgal SN. Rapamune (Sirolimus, rapamycin): an overview and mechanism of action. Ther Drug Monit 1995: 17: 660-665.
46. Syed NA, Khandelwal RL. Reciprocal regulation of glycogen phosphorylase and glycogen synthase by insulin involving phosphatidylinositol-3 kinase and protein phosphatase-1 in HepG2 cells. Mol Cell Biochem 2000: 211: 123-136.
47. Liu Z, Wu Y, Nicklas EW, Jahn LA, Price WJ, Barrett EJ. Unlike insulin, amino acids stimulate p70S6K but not GSK-3 or glycogen synthase in human skeletal muscle. Am J Physiol Endocrinol Metab 2004: 286: 523-528.
48. Taha C, Liu Z, Jin J, Al-Hasani H, Sonenberg N, Klip A. Opposite translational control of GLUT1 and GLUT4 glucose transporter mRNAs in response to insulin. Role of mammalian target of rapamycin, protein kinase b, and phosphatidylinositol 3-kinase in GLUT1 mRNA translation. J Biol Chem 1999: 274: 33085-33091.
49. Harrington LS, Findlay GM, Lamb RF. Restraining PI3K: mTOR signaling goes back to the membrane. Trends Biochem Sci 2005: 30: 35-42.
50. Teutonico A, Schena PF, Di Paulo S. Glucose metabolism in renal transplant recipients: effect of calcineurin-inhibitor withdrawal and conversion to sirolimus. J Am Soc Nephrol 2005: 16: 3128-3135.
51. Ciancio G, Burke GW, Gaynor JJ et al. A randomized long-term trial of tacrolimus/sirolimus versus tacrolimus/mycophenolate versus cyclosporine/sirolimus in renal transplantation: three-year analysis. Transplantation 2006: 81: 845-852.
52. Andoh TF, Lindsley J, Franceschini N, Bennett WM. Synergistic effects of cyclosporine and rapamycin in a chronic nephrotoxicity model. Transplantation 1996: 62: 311-316.
53. Romagnoli J, Citterio F, Nanni G et al. Incidence of post-transplant diabetes mellitus in kidney transplant recipients immunosuppressed with sirolimus in combination with cyclosporine. Transplant Proc 2006: 38: 1034-1036.
54. Halim MA, Al-Otaibi T, Johny KV et al. Long-term follow-up of 100 high-risk renal transplant recipients converted from calcineurin inhibitors to sirolimus: a single center experience. Transplant Proc 2009: 41: 1666-1670.
55. Garcia CD, Bittencourt VB, Alves AB et al. Conversion to sirolimus in pediatric renal transplantation recipients. Transplant Proc 2006: 38: 1901-1903.
56. Hymes LC, Warshaw BL, Amaral SG, Greenbaum LA. Tacrolimus withdrawal and conversion to sirolimus at three months post-pediatric renal transplantation. Pediatr Transplant 2008: 12: 773-777.
57. Hymes LC, Warshaw BL. Sirolimus in pediatric patients: results in the first 6 months post-renal transplant. Pediatr Transplant 2005: 9: 520-522.
58. Long CN, Katzin B, Fry EG. The adrenal cortex and carbohydrate metabolism. Endocrinology 1940: 26: 309-344.
59. Olefsky JM, Kimmerling G. Effects of glucocorticoids on carbohydrate metabolism. Am J Med Sci 1976: 271: 202-210.
60. Hjelmesaeth J, Midtvedt K, Jenssen T, Hartmann A. Insulin resistance after renal transplantation: impact of immunosuppressive and antihypertensive therapy. Diabetes Care 2001: 24: 2121-2126.
61. Hjelmesaeth J, Hartmann A, Kofstad J et al. Glucose intolerance after renal transplantation depends upon prednisolone dose and recipient age. Transplantation 1997: 64: 979-983.
62. Midtvedt K, Hjelmesaeth J, Hartmann A et al. Insulin resistance after renal transplantation: the effect of steroid dose reduction and withdrawal. J Am Soc Nephrol 2004: 15: 3233-3239.
63. Augustine JJ, Hricik DE. Minimization of immunosuppression in kidney transplantation. Curr Opin Nephrol Hypertens 2007: 16: 535-541.
64. Rostaing L, Cantarovich D, Mourad G et al. CARMEN Study Group. Corticosteroid-free immunosuppression with tacrolimus, mycophenolate mofetil, and daclizumab induction in renal transplantation. Transplantation 2005: 79: 807-814.
65. Almawi WY, Melemedjian OK, Rieder MJ. An alternate mechanism of glucocorticoid anti-proliferative effect: promotion of a Th2 cytokine-secreting profile. Clin Transplant 1999: 13: 365-374.
66. Schulak JA, Mayes JT, Moritz CE, Hricik DE. A prospective randomized trial of prednisone versus no prednisone maintenance therapy in cyclosporine-treated and azathioprine-treated renal transplant patients. Transplantation 1990: 49: 327-332.
67. Vanrenterghem Y, van Hooff JP, Squifflet JP et al; European Tacrolimus/MMF Renal Transplantation Study Group. Minimization of immunosuppressive therapy after renal transplantation: results of a randomized controlled trial. Am J Transplant 2005: 5: 87-95.
68. Kasiske BL, Chakkera HA, Louis TA, Ma JZ. A meta-analysis of immunosuppression withdrawal trials in renal transplantation. J Am Soc Nephrol 2000: 11: 1910-1917.
69. Pascual J, Quereda C, Zamora J, Hernández D; Spanish Group for Evidence-Based Medicine in Renal Transplantation. Steroid withdrawal in renal transplant patients on triple therapy with a calcineurin inhibitor and mycophenolate mofetil: a meta-analysis of randomized, controlled trials. Transplantation 2004: 78: 1548-1556.
70. Woodle ES, First MR, Pirsch J, Shihab F, Gaber AO, Van Veldhuisen P, Astellas Corticosteroid Withdrawal Study Group. A prospective, randomized, double-blind, placebo-controlled multicenter trial comparing early (7 day) corticosteroid cessation versus long-term, low-dose corticosteroid therapy. Ann Surg 2008: 248: 564-577.
71. Li L, Chang A, Naesens M et al. Steroid-free immunosuppression since 1999: 129 pediatric renal transplants with sustained graft and patient benefits. Am J Transplant 2009: 9: 1362-1372.
72. Paolillo JA, Boyle GJ, Law YM et al. Post-transplant diabetes mellitus in pediatric thoracic organ recipients receiving tacrolimus-based immunosuppression. Transplantation 2001: 71: 252-256.
73. Chapman TM, Keating GM. Basiliximab: a review of its use as induction therapy in renal transplantation. Drugs 2003: 63: 2803-2835.
74. Setoguchi R, Hori S, Takahashi T, Sakaguchi S. Homeostatic maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J Exp Med 2005: 201: 723-735.
75. Bayés B, Pastor MC, Lauzurica R, Granada ML, Salinas I, Romero R. Do anti-CD25 monoclonal antibodies potentiate post-transplant diabetes mellitus? Transplant Proc 2007: 39: 2248-2250.
76. Offner G, Toenshoff B, Höcker B et al. Efficacy and safety of Basiliximab in pediatric renal transplant patients receiving cyclosporine, mycophenolate mofetil, and steroids. Transplantation 2008: 86: 1241-1248.
77. Swiatecka-Urban A, Garcia C, Feuerstein D et al. Basiliximab induction improves the outcome of renal transplants in children and adolescents. Pediatr Nephrol 2001: 16: 693-696.
78. Elion GB. The purine path to chemotherapy. Science 1989: 244: 41-47.
79. Gheith OA, Bakr MA, Fouda MA, Shokeir AA, Sobh M, Ghoneim M. Prospective randomized study of azathioprine vs cyclosporine based therapy in primary haplo-identical living-donor kidney transplantation: 20-year experience. Clin Exp Nephrol 2007: 11: 151-155.
80. Allison AC, Eugui EM. Purine metabolism and immunosuppressive effects of mycophenolate mofetil (MMF). Clin Transplant 1996: 10: 77-84.
81. Jaber JJ, Feustel PJ, Elbahloul O, Conti AD, Gallichio MH, Conti DJ. Early steroid withdrawal therapy in renal transplant recipients: a steroid-free sirolimus and CellCept-based calcineurin inhibitor-minimization protocol. Clin Transplant 2007: 21: 101-109.
82. Karie-Guigues S, Janus N, Saliba F et al. Long-term renal function in liver transplant recipients and impact of immunosuppressive regimens (calcineurin inhibitors alone or in combination with mycophenolate mofetil): the TRY study. Liver Transpl 2009: 15: 1083-1091.
83. Duijnhoven EM, Boots JM, Christiaans MH, Wolffenbuttel BH, 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.
84. Jeffcoate W. Growth hormone therapy and its relationship to insulin resistance, glucose intolerance and diabetes mellitus: a review of recent evidence. Drug Saf 2002: 25: 199-212.
85. Starkman H, Das S. Cystic fibrosis presenting as new onset diabetes mellitus in adolescent twins. Pediatr Diabetes 2004: 5: 99-101.
86. Stoffel M, Duncan SA. The maturity-onset diabetes of the young (MODY1) transcription factor HNF4alpha regulates expression of genes required for glucose transport and metabolism. Proc Natl Acad Sci U S A 1997: 94: 13209-13214.
87. Kolatsi-Joannou M, Bingham C, Ellard S et al. Hepatocyte nuclear factor-1beta: a new kindred with renal cysts and diabetes and gene expression in normal human development. J Am Soc Nephrol 2001: 12: 2175-2180.
88. Richter S, Shih DQ, Pearson ER et al. Regulation of apolipoprotein M gene expression by MODY3 gene hepatocyte nuclear factor-1alpha: haploinsufficiency is associated with reduced serum apolipoprotein M levels. Diabetes 2003: 52: 2989-2995.