Non-linear Relationship between Tacrolimus Blood Concentration and Acute Rejection After Kidney Transplantation: A Systematic Review and Dose-Response Meta-Analysis of Cohort Studies

Author(s): Saifu Yin, Turun Song, Xingxing Li, Hanyue Xu, Xueling Zhang, Yamei Jiang, Tao Lin*.

Journal Name: Current Pharmaceutical Design

Volume 25 , Issue 21 , 2019


Abstract:

Background: Maintaining the exposure of tacrolimus (Tac) after kidney transplantation (KT) must be necessary to prevent acute rejection (AR) and improve graft survival,but there is still no clear consensus on the optimal Tac target blood concentration and concentration-effect relationship is poorly defined.

Methods: We conducted a dose-response meta-analysis to quantitatively assess the association between Tac blood concentration and (AR) or adverse effects after KT. A comprehensive search of PubMed, Embase and Cochrane library databases was conducted to find eligible studies up to 10th September 2018. Unpublished data from patients receiving KT in West China Hospital (Sichuan University, China) were also collected. Both twostage dose-response and one-stage dose-response meta-analysis models were used to improve the statistical power.

Results: A total of 4967 individuals from 10 original studies and 1453 individuals from West China Hospital were eligible for the ultimate analysis. In the two-stage dose-response meta-analysis model, we observed a significant non-linear relationship between Tac blood concentration and AR (P < 0.001) with moderate heterogeneity (I2 = 46.0%, P = 0.08). Tac blood concentration at 8ng/ml was associated with the lowest risk of AR (RR: 0.26, 95%CI: 0.13 - 0.54) by reference to 2ng/ml. Tac concentration at 7.0 - 11.0 ng/ml reduced the risk of AR by at least 70%, 5-14 ng/ml by at least 60%, and 4.5 – 14 ng/ml at least 50%. In the one-stage dose-response model, we also found a strong non-linear relationship between Tac and AR (P < 0.001) with moderate heterogeneity (I2 = 41.2%, P = 0.10). Tac concentration of 7.5 ng/ml was associated with the lowest risk of AR (RR: 0.35, 95%CI: 0.16 - 0.77). The blood concentration at 5.5 - 9.5 ng/ml was associated with the reduced AR by at least 60% and 4.5 - 10.5 ng/ml by at least 50% by reference to 2 ng/ml.

Conclusion: Maintaining Tac blood concentration at 5 - 9.5 ng/ml within the first year may prevent AR most effectively.

Keywords: Tacrolimus, kidney transplantation, acute rejection, dose-response meta-analysis, systematic review, immunosuppressive drug.

[1]
Tonelli M, Wiebe N, Knoll G, et al. Systematic review: Kidney transplantation compared with dialysis in clinically relevant outcomes. Am J Transplant 2011; 11(10): 2093-109.
[http://dx.doi.org/10.1111/j.1600-6143.2011.03686.x] [PMID: 21883901]
[2]
Dharnidharka VR, Fiorina P, Harmon WE. Kidney transplantation in children. N Engl J Med 2014; 371(6): 549-58.
[http://dx.doi.org/10.1056/NEJMra1314376] [PMID: 25099579]
[3]
Guirado L, Cantarell C, Franco A, et al. Efficacy and safety of conversion from twice-daily to once-daily tacrolimus in a large cohort of stable kidney transplant recipients. Am J Transplant 2011; 11(9): 1965-71.
[http://dx.doi.org/10.1111/j.1600-6143.2011.03571.x] [PMID: 21668633]
[4]
Scholten EM, Cremers SCLM, Schoemaker RC, et al. AUC-guided dosing of tacrolimus prevents progressive systemic overexposure in renal transplant recipients. Kidney Int 2005; 67(6): 2440-7.
[http://dx.doi.org/10.1111/j.1523-1755.2005.00352.x] [PMID: 15882290]
[5]
Gatault P, Kamar N. Reduction of extended-release tacrolimus dose in low immunological risk kidney transplant recipients increases risk of rejection and appearance of DSA - a randomized study. Am J Transplant 2016; 17(5): 1370-9.
[http://dx.doi.org/10.1111/ajt.14109] [PMID: 27862923]
[6]
David-Neto E, Romano P, Kamada Triboni AH, et al. longitudinal pharmacokinetics of tacrolimus in elderly compared with younger recipients in the first 6 months after renal transplantation. Transplantation 2017; 101(6): 1365-72.
[http://dx.doi.org/10.1097/TP.0000000000001369] [PMID: 27482958]
[7]
Tanriover B, Jaikaransingh V, MacConmara MP, et al. Acute rejection rates and graft outcomes according to induction regimen among recipients of kidneys from deceased donors treated with tacrolimus and mycophenolate. Clin J Am Soc Nephrol 2016; 11(9): 1650-61.
[http://dx.doi.org/10.2215/CJN.13171215] [PMID: 27364616]
[8]
Rostaing L, Bunnapradist S, Grinyó JM, et al. Novel once-daily extended-release tacrolimus versus twice-daily tacrolimus in de novo kidney transplant recipients: two-year results of phase 3, double-blind, randomized trial. Am J Kidney Dis 2016; 67(4): 648-59.
[http://dx.doi.org/10.1053/j.ajkd.2015.10.024] [PMID: 26717860]
[9]
Ensor CR, Iasella CJ, Harrigan KM, et al. Increasing tacrolimus time-in-therapeutic range is associated with superior one-year outcomes in lung transplant recipients. Am J Transplant 2018; 18(6): 1527-33.
[http://dx.doi.org/10.1111/ajt.14723] [PMID: 29513387]
[10]
Kahan BD, Keown P, Levy GA, Johnston A. Therapeutic drug monitoring of immunosuppressant drugs in clinical practice. Clin Ther 2002; 24(3): 330-50.
[http://dx.doi.org/10.1016/S0149-2918(02)85038-X] [PMID: 11952020]
[11]
Pascual M, Theruvath T, Kawai T, Tolkoff-Rubin N, Cosimi AB. Strategies to improve long-term outcomes after renal transplantation. N Engl J Med 2002; 346(8): 580-90.
[http://dx.doi.org/10.1056/NEJMra011295] [PMID: 11856798]
[12]
Ekberg H, Tedesco-Silva H, Demirbas A, et al. Reduced exposure to calcineurin inhibitors in renal transplantation. N Engl J Med 2007; 357(25): 2562-75.
[http://dx.doi.org/10.1056/NEJMoa067411] [PMID: 18094377]
[13]
Lim WH, Eris J, Kanellis J, et al. A systematic review of conversion from calcineurin inhibitor to mammalian target of rapamycin inhibitors for maintenance immunosuppression in kidney transplant recipients. Am J Transplant 2014; 14(9): 2106-19.
[http://dx.doi.org/10.1111/ajt.12795] [PMID: 25088685]
[14]
Kang JS, Lee MH. Overview of therapeutic drug monitoring. Korean J Intern Med (Korean Assoc Intern Med) 2009; 24(1): 1-10.
[http://dx.doi.org/10.3904/kjim.2009.24.1.1] [PMID: 19270474]
[15]
Naesens M, Kuypers DRJ, Sarwal M. Calcineurin inhibitor nephrotoxicity. Clin J Am Soc Nephrol 2009; 4(2): 481-508.
[http://dx.doi.org/10.2215/CJN.04800908] [PMID: 19218475]
[16]
McMaster P, Mirza DF, Ismail T, Vennarecci G, Patapis P, Mayer AD. Therapeutic drug monitoring of tacrolimus in clinical transplantation. Ther Drug Monit 1995; 17(6): 602-5.
[http://dx.doi.org/10.1097/00007691-199512000-00010] [PMID: 8588228]
[17]
Gatault P, Kamar N. Reduction of extended-release tacrolimus dose in low immunological risk kidney transplant recipients increases risk of rejection and appearance of DSA - a randomized study. Am J Transplant 2016; 17(5): 1370-9.
[http://dx.doi.org/10.1111/ajt.14109] [PMID: 27862923]
[18]
Sapir-Pichhadze R, Wang Y, Famure O, Li Y, Kim SJ. Time-dependent variability in tacrolimus trough blood levels is a risk factor for late kidney transplant failure. Kidney Int 2014; 85(6): 1404-11.
[http://dx.doi.org/10.1038/ki.2013.465] [PMID: 24336032]
[19]
Kasiske BL, Zeier MG, Chapman JR, et al. KDIGO clinical practice guideline for the care of kidney transplant recipients: a summary. Kidney Int 2010; 77(4): 299-311.
[http://dx.doi.org/10.1038/ki.2009.377] [PMID: 19847156]
[20]
Laskow DA, Vincenti F, Neylan JF, Mendez R, Matas AJ. An open-label, concentration-ranging trial of FK506 in primary kidney transplantation: a report of the United States Multicenter FK506 Kidney Transplant Group. Transplantation 1996; 62(7): 900-5.
[http://dx.doi.org/10.1097/00007890-199610150-00005] [PMID: 8878381]
[21]
Staatz CE, Tett SE. Clinical pharmacokinetics and pharmacodynamics of tacrolimus in solid organ transplantation. Clin Pharmacokinet 2004; 43(10): 623-53.
[http://dx.doi.org/10.2165/00003088-200443100-00001] [PMID: 15244495]
[22]
Christians U, Jacobsen W, Benet LZ, Lampen A. Mechanisms of clinically relevant drug interactions associated with tacrolimus. Clin Pharmacokinet 2002; 41(11): 813-51.
[http://dx.doi.org/10.2165/00003088-200241110-00003] [PMID: 12190331]
[23]
Davis S, Gralla J, Klem P, et al. Lower tacrolimus exposure and time in therapeutic range increase the risk of de novo donor-specific antibodies in the first year of kidney transplantation. Am J Transplant 2018; 18(4): 907-15.
[http://dx.doi.org/10.1111/ajt.14504] [PMID: 28925597]
[24]
Richards KR, Hager D, Muth B, Astor BC, Kaufman D, Djamali A. Tacrolimus trough level at discharge predicts acute rejection in moderately sensitized renal transplant recipients. Transplantation 2014; 97(10): 986-91.
[http://dx.doi.org/10.1097/TP.0000000000000149] [PMID: 24784360]
[25]
Bouamar R, Shuker N, Hesselink DA, et al. Tacrolimus predose concentrations do not predict the risk of acute rejection after renal transplantation: a pooled analysis from three randomized-controlled clinical trials.(†) Am J Transplant 2013; 13(5): 1253-61.
[http://dx.doi.org/10.1111/ajt.12191] [PMID: 23480233]
[26]
USRDS 2008 Annual Data Report: Atlas of End-Stage Renal Disease in the United States. Bethesda, MD: National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases 2008.
[27]
Ledinh H, Weekers L, Bonvoisin C, et al. Results of kidney transplantation from controlled donors after cardio-circulatory death: a single center experience. Transpl Int 2012; 25(2): 201-9.
[http://dx.doi.org/10.1111/j.1432-2277.2011.01402.x] [PMID: 22220676]
[28]
Farrugia D, Mahboob S, Cheshire J, et al. Malignancy-related mortality following kidney transplantation is common. Kidney Int 2014; 85(6): 1395-403.
[http://dx.doi.org/10.1038/ki.2013.458] [PMID: 24257690]
[29]
Liao WC, Tu YK, Wu MS, et al. Blood glucose concentration and risk of pancreatic cancer: systematic review and dose-response meta-analysis. BMJ 2015; 350: g7371.
[http://dx.doi.org/10.1136/bmj.g7371]
[30]
Orsini N, Li R, Wolk A, Khudyakov P, Spiegelman D. Meta-analysis for linear and nonlinear dose-response relations: examples, an evaluation of approximations, and software. Am J Epidemiol 2012; 175(1): 66-73.
[http://dx.doi.org/10.1093/aje/kwr265] [PMID: 22135359]
[31]
Shim SR, Lee J. Dose-response meta-analysis: Application and practice using the R software. Epidemiol Health 2019; 41e2019006
[http://dx.doi.org/10.4178/epih.e2019006] [PMID: 30999740]
[32]
Langford O, Aronson JK, van Valkenhoef G, Stevens RJ. Methods for meta-analysis of pharmacodynamic dose-response data with application to multi-arm studies of alogliptin. Stat Methods Med Res 2018; 27(2): 564-78.
[http://dx.doi.org/10.1177/0962280216637093] [PMID: 26994216]
[33]
Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 2000; 283(15): 2008-12.
[http://dx.doi.org/10.1001/jama.283.15.2008] [PMID: 10789670]
[34]
Choi EK, Park HB, Lee KH, et al. Body mass index and 20-specific cancers: re-analyses of dose-response meta-analyses of observational studies. Ann Oncol 2017; 29(3): 749-57.
[http://dx.doi.org/10.1093/annonc/mdx819] [PMID: 29300814]
[35]
Song T, Fu L, Rao Z, et al. Kidneys from older living donors provide excellent short and intermediate outcomes--a single china center’s experience. Transplantation 2015; 99(8): e81-8.
[http://dx.doi.org/10.1097/TP.0000000000000580] [PMID: 26308304]
[36]
Jiang Y, Song T, Qiu Y, et al. Outcomes of single kidney transplantation from pediatric donors: A single-center experience. Pediatr Transplant 2018; 22(5)e13196
[http://dx.doi.org/10.1111/petr.13196] [PMID: 29696741]
[37]
Wells GA, Shea B, O’Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses.
[38]
Liao WC, Tu YK, Wu MS, et al. Blood glucose concentration and risk of pancreatic cancer: Systematic review and dose-response meta-analysis 2015.
[http://dx.doi.org/10.1136/bmj.g7371]
[39]
Aune D, Keum N, Giovannucci E, et al. Whole grain consumption and risk of cardiovascular disease, cancer, and all cause and cause specific mortality: systematic review and dose-response meta-analysis of prospective studies. BMJ 2016; 353: i2716.
[http://dx.doi.org/10.1136/bmj.i2716] [PMID: 27301975]
[40]
Zhong S, Yan X, Wu Y, et al. Body mass index and mortality in prostate cancer patients: a dose-response meta-analysis. Prostate Cancer Prostatic Dis 2016; 19(2): 122-31.
[http://dx.doi.org/10.1038/pcan.2015.64] [PMID: 26754262]
[41]
Fletcher J. What is heterogeneity and is it important? BMJ 2007; 334(7584): 94-6.
[http://dx.doi.org/10.1136/bmj.39057.406644.68] [PMID: 17218716]
[42]
Larsson SC, Drca N, Wolk A. Alcohol consumption and risk of atrial fibrillation: A prospective study and dose-response meta-analysis. J Am Coll Cardiol 2014; 64(3): 281-9.
[http://dx.doi.org/10.1016/j.jacc.2014.03.048] [PMID: 25034065]
[43]
Rong Y, Chen L, Zhu T, et al. Egg consumption and risk of coronary heart disease and stroke: dose-response meta-analysis of prospective cohort studies. BMJ 2013; 346e8539
[http://dx.doi.org/10.1136/bmj.e8539] [PMID: 23295181]
[44]
Discacciati A, Orsini N, Wolk A. Coffee consumption and risk of nonaggressive, aggressive and fatal prostate cancer--a dose-response meta-analysis. Ann Oncol 2014; 25(3): 584-91.
[http://dx.doi.org/10.1093/annonc/mdt420] [PMID: 24276028]
[45]
Orsini N, Li R, Wolk A, Khudyakov P, Spiegelman D. Meta-analysis for linear and nonlinear dose-response relations: examples, an evaluation of approximations, and software. Am J Epidemiol 2012; 175(1): 66-73.
[http://dx.doi.org/10.1093/aje/kwr265] [PMID: 22135359]
[46]
Crippa A, Discacciati A, Bottai M, Spiegelman D, Orsini N. One-stage dose-response meta-analysis for aggregated data. Stat Methods Med Res 2019; 28(5): 1579-96.
[http://dx.doi.org/10.1177/0962280218773122] [PMID: 29742975]
[47]
Xu C, Doi SAR. The robust error meta-regression method for dose-response meta-analysis. Int J Evid-Based Healthc 2018; 16(3): 138-44.
[PMID: 29251651]
[48]
Cosio FG, Amer H, Grande JP, Larson TS, Stegall MD, Griffin MD. Comparison of low versus high tacrolimus levels in kidney transplantation: assessment of efficacy by protocol biopsies. Transplantation 2007; 83(4): 411-6.
[http://dx.doi.org/10.1097/01.tp.0000251807.72246.7d] [PMID: 17318073]
[49]
Langone A, Doria C, Greenstein S, et al. Does reduction in mycophenolic acid dose compromise efficacy regardless of tacrolimus exposure level? An analysis of prospective data from the Mycophenolic Renal Transplant (MORE) Registry. Clin Transplant 2013; 27(1): 15-24.
[http://dx.doi.org/10.1111/j.1399-0012.2012.01694.x] [PMID: 22861144]
[50]
Shihab FS, Olyaei A, Wiland A, McCague K, Norman DJ. Tacrolimus exposure in the real world: an analysis from the Mycophenolic acid Observational REnal transplant study. Clin Transplant 2014; 28(7): 768-75.
[http://dx.doi.org/10.1111/ctr.12377] [PMID: 24754603]
[51]
Arreola-Guerra JM, Serrano M, Morales-Buenrostro LE, Vilatobá M, Alberú J. Tacrolimus trough levels as a risk factor for acute rejection in renal transplant patients. Ann Transplant 2016; 21: 105-14.
[http://dx.doi.org/10.12659/AOT.895104] [PMID: 26879833]
[52]
Aktürk S, Erdoğmuş Ş, Kumru G, et al. Average tacrolimus trough level in the first month after transplantation may predict acute rejection. Transplant Proc 2017; 49(3): 430-5.
[http://dx.doi.org/10.1016/j.transproceed.2017.02.011] [PMID: 28340806]
[53]
Tang JT, Yan L, Wang LL, et al. A low fixed tacrolimus starting dose is effective and safe in chinese renal transplantation recipients. Ann Transplant 2018; 23: 300-9.
[http://dx.doi.org/10.12659/AOT.907666]
[54]
Gaynor JJ, Ciancio G, Guerra G, et al. Lower tacrolimus trough levels are associated with subsequently higher acute rejection risk during the first 12 months after kidney transplantation. Transpl Int 2016; 29(2): 216-26.
[http://dx.doi.org/10.1111/tri.12699] [PMID: 26442829]
[55]
Naesens M, Kuypers DRJ, Sarwal M. Calcineurin inhibitor nephrotoxicity. Clin J Am Soc Nephrol 2009; 4(2): 481-508.
[http://dx.doi.org/10.2215/CJN.04800908] [PMID: 19218475]
[56]
Ekberg H, Tedesco-Silva H, Demirbas A, et al. Reduced exposure to calcineurin inhibitors in renal transplantation. N Engl J Med 2007; 357(25): 2562-75.
[http://dx.doi.org/10.1056/NEJMoa067411] [PMID: 18094377]
[57]
Lim WH, Eris J, Kanellis J, et al. A systematic review of conversion from calcineurin inhibitor to mammalian target of rapamycin inhibitors for maintenance immunosuppression in kidney transplant recipients. Am J Transplant 2014; 14(9): 2106-19.
[http://dx.doi.org/10.1111/ajt.12795] [PMID: 25088685]
[58]
Sawinski D, Trofe-Clark J, Leas B, et al. Calcineurin inhibitor minimization, conversion, withdrawal, and avoidance strategies in renal transplantation: a systematic review and meta- analysis. Am J Transplant 2016; 16(7): 2117-38.
[http://dx.doi.org/10.1111/ajt.13710] [PMID: 26990455]
[59]
Zahir H, McCaughan G, Gleeson M, Nand RA, McLachlan AJ. Factors affecting variability in distribution of tacrolimus in liver transplant recipients. Br J Clin Pharmacol 2004; 57(3): 298-309.
[http://dx.doi.org/10.1046/j.1365-2125.2003.02008.x] [PMID: 14998426]
[60]
Starzl TE, Murase N, Abu-Elmagd K, et al. Tolerogenic immunosuppression for organ transplantation. Lancet 2003; 361(9368): 1502-10.
[http://dx.doi.org/10.1016/S0140-6736(03)13175-3] [PMID: 12737859]
[61]
Moreau A, Alliot-Licht B, Cuturi MC, Blancho G. Tolerogenic dendritic cell therapy in organ transplantation. Transpl Int 2017; 30(8): 754-64.
[http://dx.doi.org/10.1111/tri.12889] [PMID: 27864897]
[62]
Adams DH, Sanchez-Fueyo A, Samuel D. From immunosuppression to tolerance. J Hepatol 2015; 62(1)(Suppl.): S170-85.
[http://dx.doi.org/10.1016/j.jhep.2015.02.042] [PMID: 25920086]
[63]
Kinnunen S. Secular trends in infection-related mortality after kidney transplantation. Clin J Am Soc Nephrol, 2018. CJN.11511017.
[64]
Howard RJ, Patton PR, Reed AI, et al. The changing causes of graft loss and death after kidney transplantation. Transplantation 2002; 73(12): 1923-8.
[http://dx.doi.org/10.1097/00007890-200206270-00013] [PMID: 12131689]
[65]
Pruthi R, Steenkamp R, Feest T. UK Renal Registry 16th annual report: Chapter 8 survival and cause of death of UK adult patients on renal replacement therapy in 2012: national and centre-specific analyses. Nephron Clin Pract 2013; 125(1-4): 139-69.
[http://dx.doi.org/10.1159/000360027] [PMID: 24662172]
[66]
Sarnak MJ, Jaber BL. Mortality caused by sepsis in patients with end-stage renal disease compared with the general population. Kidney Int 2000; 58(4): 1758-64.
[http://dx.doi.org/10.1111/j.1523-1755.2000.00337.x] [PMID: 11012910]
[67]
Sarnak MJ, Jaber BL. Pulmonary infectious mortality among patients with end-stage renal disease. Chest 2001; 120(6): 1883-7.
[http://dx.doi.org/10.1378/chest.120.6.1883] [PMID: 11742917]
[68]
Farrugia D, Cheshire J, Begaj I, Khosla S, Ray D, Sharif A. Death within the first year after kidney transplantation--an observational cohort study. Transpl Int 2014; 27(3): 262-70.
[http://dx.doi.org/10.1111/tri.12218] [PMID: 24138318]
[69]
Arend SM, Mallat MJ, Westendorp RJ, van der Woude FJ, van Es LA. Patient survival after renal transplantation; more than 25 years follow-up. Nephrol Dial Transplant 1997; 12(8): 1672-9.
[http://dx.doi.org/10.1093/ndt/12.8.1672] [PMID: 9269647]
[70]
Briggs JD. Causes of death after renal transplantation. Nephrol Dial Transplant 2001; 16(8): 1545-9.
[http://dx.doi.org/10.1093/ndt/16.8.1545] [PMID: 11477152]
[71]
Vogelzang JL, van Stralen KJ, Noordzij M, et al. Mortality from infections and malignancies in patients treated with renal replacement therapy: data from the ERA-EDTA registry. Nephrol Dial Transplant 2015; 30(6): 1028-37.
[http://dx.doi.org/10.1093/ndt/gfv007] [PMID: 25637641]
[72]
Meier-Kriesche HU, Schold JD, Srinivas TR, Kaplan B. Lack of improvement in renal allograft survival despite a marked decrease in acute rejection rates over the most recent era. Am J Transplant 2004; 4(3): 378-83.
[http://dx.doi.org/10.1111/j.1600-6143.2004.00332.x] [PMID: 14961990]
[73]
Chhabra D, Alvarado A, Dalal P, et al. Impact of calcineurin-inhibitor conversion to mTOR inhibitor on renal allograft function in a prednisone-free regimen. Am J Transplant 2013; 13(11): 2902-11.
[http://dx.doi.org/10.1111/ajt.12437] [PMID: 24007570]
[74]
Qazi Y, Shaffer D, Kaplan B, et al. Efficacy and safety of everolimus plus low-dose tacrolimus versus mycophenolate mofetil plus standard-dose tacrolimus in de novo renal transplant recipients: 12-month data. Am J Transplant 2017; 17(5): 1358-69.
[http://dx.doi.org/10.1111/ajt.14090] [PMID: 27775865]
[75]
Gatault P, Kamar N. Reduction of extended-release tacrolimus dose in low immunological risk kidney transplant recipients increases risk of rejection and appearance of DSA - a randomized study. Am J Transplant 2017; 17(5): 1370-9.
[http://dx.doi.org/10.1111/ajt.14109] [PMID: 27862923]
[76]
Naesens M, Kuypers DR, Sarwal M. Calcineurin inhibitor nephrotoxicity. Clin J Am Soc Nephrol 2009; 4(2): 481-508.
[http://dx.doi.org/10.2215/CJN.04800908] [PMID: 19218475]
[77]
Marcén R. Immunosuppressive drugs in kidney transplantation: impact on patient survival, and incidence of cardiovascular disease, malignancy and infection. Drugs 2009; 69(16): 2227-43.
[http://dx.doi.org/10.2165/11319260-000000000-00000] [PMID: 19852526]
[78]
Nankivell BJ, Borrows RJ, Fung CL, O’Connell PJ, Chapman JR, Allen RD. Calcineurin inhibitor nephrotoxicity: longitudinal assessment by protocol histology. Transplantation 2004; 78(4): 557-65.
[http://dx.doi.org/10.1097/01.TP.0000128636.70499.6E] [PMID: 15446315]
[79]
Moore J, Middleton L, Cockwell P, et al. Calcineurin inhibitor sparing with mycophenolate in kidney transplantation: a systematic review and meta-analysis. Transplantation 2009; 87(4): 591-605.
[http://dx.doi.org/10.1097/TP.0b013e318195a421] [PMID: 19307799]
[80]
Ekberg H, Tedesco-Silva H, Demirbas A, et al. Reduced exposure to calcineurin inhibitors in renal transplantation. N Engl J Med 2007; 357(25): 2562-75.
[http://dx.doi.org/10.1056/NEJMoa067411] [PMID: 18094377]
[81]
Moers C, Smits JM, Maathuis MHJ, et al. Machine perfusion or cold storage in deceased-donor kidney transplantation. N Engl J Med 2009; 360(1): 7-19.
[http://dx.doi.org/10.1056/NEJMoa0802289] [PMID: 19118301]
[82]
Macrae J, Friedman AL, Friedman EA, Eggers P. Live and deceased donor kidney transplantation in patients aged 75 years and older in the United States. Int Urol Nephrol 2005; 37(3): 641-8.
[http://dx.doi.org/10.1007/s11255-004-0010-6] [PMID: 16307355]
[83]
Lim WH, Gray NA, Chadban SJ, Pilmore H, Wong G. Graft and patient outcomes of zero-human leucocyte-antigen-mismatched deceased and live donor kidney transplant recipients. Transpl Int 2015; 28(5): 610-8.
[http://dx.doi.org/10.1111/tri.12542] [PMID: 25689280]
[84]
Albano L, Banas B, Klempnauer JL, Glyda M, Viklicky O, Kamar N. OSAKA trial: a randomized, controlled trial comparing tacrolimus QD and BD in kidney transplantation. Transplantation 2013; 96(10): 897-903.
[http://dx.doi.org/10.1097/TP.0b013e3182a203bd] [PMID: 23982340]
[85]
Stifft F, Stolk LML, Undre N, van Hooff JP, Christiaans MH. Lower variability in 24-hour exposure during once-daily compared to twice-daily tacrolimus formulation in kidney transplantation. Transplantation 2014; 97(7): 775-80.
[PMID: 24686426]
[86]
Tacrolimus once daily (ADVAGRAF) versus twice daily (PROGRAF) in de novo renal transplantation: a randomized phase III study. Am J Transplant 2010; 10: 2632.
[87]
Crespo M, Mir M, Marin M, et al. De novo kidney transplant recipients need higher doses of Advagraf compared with Prograf to get therapeutic levels. Transplant Proc 2009; 41(6): 2115-7.
[http://dx.doi.org/10.1016/j.transproceed.2009.05.014] [PMID: 19715848]
[88]
Andrés A, Delgado-Arranz M, Morales E, et al. Extended-release tacrolimus therapy in de novo kidney transplant recipients: single-center experience. Transplant Proc 2010; 42(8): 3034-7.
[http://dx.doi.org/10.1016/j.transproceed.2010.07.044] [PMID: 20970602]
[89]
Jelassi ML, Lefeuvre S, Karras A, Moulonguet L, Billaud EM. Therapeutic drug monitoring in de novo kidney transplant receiving the modified-release once-daily tacrolimus. Transplant Proc 2011; 43(2): 491-4.
[http://dx.doi.org/10.1016/j.transproceed.2011.01.043] [PMID: 21440742]
[90]
Shi X, Liu R, Xie X, et al. Effect of human leukocyte antigen mismatching on the outcomes of pediatric kidney transplantation: a systematic review and meta-analysis. Nephrol Dial Transplant 2017; 32(11): 1939-48.
[http://dx.doi.org/10.1093/ndt/gfx259] [PMID: 28992320]
[91]
Shi X, Lv J, Han W, et al. What is the impact of human leukocyte antigen mismatching on graft survival and mortality in renal transplantation? A meta-analysis of 23 cohort studies involving 486,608 recipients. BMC Nephrol 2018; 19(1): 116.
[http://dx.doi.org/10.1186/s12882-018-0908-3] [PMID: 29776389]
[92]
Ko EJ, Yu JH, Yang CW, Chung BH. Clinical outcomes of ABO- and HLA-incompatible kidney transplantation: a nationwide cohort study. Transpl Int 2017; 30(12): 1215-25.
[http://dx.doi.org/10.1111/tri.12979] [PMID: 28493630]
[93]
Singh D, Kiberd BA, West KA, et al. Importance of peak PRA in predicting the kidney transplant survival in highly sensitized patients. Transplant Proc 2003; 35(7): 2395-7.
[http://dx.doi.org/10.1016/j.transproceed.2003.08.007]
[94]
Lim WH, Chapman JR, Wong G. Peak panel reactive antibody, cancer, graft, and patient outcomes in kidney transplant recipients. Transplantation 2015; 99(5): 1043-50.
[http://dx.doi.org/10.1097/TP.0000000000000469] [PMID: 25539466]


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VOLUME: 25
ISSUE: 21
Year: 2019
Page: [2394 - 2403]
Pages: 10
DOI: 10.2174/1381612825666190717101941
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