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Extensive clinical use has confirmed that tacrolimus (Prograf®) is a key option for immunosuppression after transplantation. In large, prospective, randomised, multicentre trials in adults and children receiving solid organ transplants, tacrolimus was at least as effective or provided better efficacy than cyclosporin microemulsion in terms of patient and graft survival, treatment failure rates and the incidence of biopsy-proven acute and corticosteroid-resistant rejection episodes. Notably, the lower incidence of rejection episodes after renal transplantation in tacrolimus recipients was reflected in improved cost effectiveness. In bone marrow transplant (BMT) recipients, the incidence of tacrolimus grade II–IV graft-versus-host disease was significantly lower with tacrolimus than cyclosporin treatment. Efficacy was maintained in renal and liver transplant recipients after total withdrawal of corticosteroid therapy from tacrolimus-based immunosuppression, with the incidence of acute rejection episodes at up to 2 years’ follow-up being similar with or without corticosteroids.
Tacrolimus provided effective rescue therapy in transplant recipients with persistent acute or chronic allograft rejection or drug-related toxicity associated with cyclosporin treatment. Typically, conversion to tacrolimus reversed rejection episodes and/or improved the tolerability profile, particularly in terms of reduced hyperlipidaemia. In lung transplant recipients with obliterative bronchiolitis, conversion to tacrolimus reduced the decline in and/or improved lung function in terms of forced expiratory volume in 1 second.
Tolerability issues may be a factor when choosing a calcineurin inhibitor. Cyclosporin tends to be associated with a higher incidence of significant hypertension, hyperlipidaemia, hirsutism, gingivitis and gum hyperplasia, whereas the incidence of some types of neurotoxicity, disturbances in glucose metabolism, diarrhoea, pruritus and alopecia may be higher with tacrolimus treatment. Renal function, as assessed by serum creatinine levels and glomerular filtration rates, was better in tacrolimus than cyclosporin recipients at up to 5 years’ follow-up.
Conclusion: Recent well designed trials have consolidated the place of tacrolimus as an important choice for primary immunosuppression in solid organ transplantation and in BMT. Notably, in adults and children receiving transplants, tacrolimus-based primary immunosuppression was at least as effective or provided better efficacy than cyclosporin microemulsion treatment in terms of patient and graft survival, treatment failure and the incidence of acute and corticosteroid-resistant rejection episodes. The reduced incidence of rejection episodes in renal transplant recipients receiving tacrolimus translated into a better cost effectiveness relative to cyclosporin microemulsion treatment. The optimal immunosuppression regimen is ultimately dependent on balancing such factors as the efficacy of the individual drugs, their tolerability, potential for drug interactions and pharmacoeconomic issues.
Overview of Pharmacodynamic Properties
Tacrolimus modulates cell-mediated and humoral immune responses associated with allograft rejection in several ways. The pivotal mechanism of action involves inhibition of the signal transduction pathway leading to T-cell activation via complex formation of the drug with the immunophilin FK506 binding protein 12, thus blocking the phosphotase activity of calcineurin and subsequent production of interleukin (IL)-2. Although cyclosporin also inhibits calcineurin through complex formation with a separate immunophilin, in vitro and in vivo studies demonstrate that tacrolimus is 10–100 times more effective than cyclosporin in its ability to exert immunosuppressive actions. Tacrolimus may also inhibit cellular activities such as nitric oxide synthetase activation and apoptosis, and may potentiate the action of corticosteroids in these processes.
Overview of Pharmacokinetic Properties
Tacrolimus treatment is associated with several other well established effects including nephrotoxic, diabetogenic, neurological and cardiovascular effects, with several cellular and immunological mechanisms potentially involved. Many of these effects appear to be mechanistically related through inhibition of calcineurin and thus, are also associated with cyclosporin treatment. Tacrolimus may be less atherogenic than cyclosporin, in terms of its lipogenic potential. Like cyclosporin, pharmacokinetic parameters of tacrolimus show high inter- and intraindividual variability and both drugs have a narrow therapeutic index, necessitating therapeutic whole-blood drug monitoring to optimise treatment. Absorption and oral bioavailability (≈25%) of tacrolimus is poor, with the rate and extent of absorption reduced in the presence of food. Tacrolimus is rapidly, albeit incompletely, absorbed in the gastrointestinal tract, with peak tacrolimus concentrations in whole blood (Cmax) attained approximately 1–2 hours after oral administration. In adult renal and liver transplant recipients receiving oral tacrolimus 0.3 mg/kg/day, respective Cmax values were 24.2 and 68.5 ng/mL, with corresponding area under the concentration-time curve values of 288 and 519 ng · h/mL.
Tacrolimus is extensively bound to erythrocytes, with blood: plasma ratios showing wide variation (mean 35). Plasma protein binding may be as high as 99%, with the majority of the drug bound to α1-acid glycoprotein and albumin. The drug is widely distributed into most tissues. In renal and liver transplant recipients receiving intravenous tacrolimus, the volume of distribution was 1.41 and 0.85 L/kg. Tacrolimus crosses the placenta, with umbilical cord plasma concentrations approximately one-third of those in maternal plasma, and is present in breast milk at similar levels to those reported in the plasma.
Tacrolimus is almost completely metabolised prior to elimination. Metabolism is via cytochrome P450 (CYP) 3A4 isoenzymes in the liver and, to a lesser extent, CYP3A4 isoenzymes and P-glycoprotein in the intestinal mucosa. Several metabolites are formed and, although at least one of these shows some immunosuppressive activity, the immunosuppressive activity of tacrolimus is chiefly due to the parent drug. The elimination half-life of the drug ranged from 12–19 hours in adult transplant recipients, with less than 1% of the dose excreted as parent drug in the urine. The main route of elimination is via the biliary tract and excretion in faeces.
Poor bioavailability is observed in a higher percentage of non-Caucasian (African-American, Hispanics) than Caucasian patients, with a study in renal transplant recipients showing that African-American recipients required higher dosages of tacrolimus on a milligram per kilogram basis. Clearance of tacrolimus appears to be higher in children than adults; therefore children require higher dosages on a milligram per kilogram basis than adults. Clearance of the drug is reduced in adults with severe hepatic impairment (mean Child Pugh >10) compared with healthy adult volunteers.
Like cyclosporin, tacrolimus is subject to a number of pharmacokinetic drug interactions of potential clinical significance, including those involving other drugs metabolised by the CYP enzyme system. The main CYP3A4 inhibitors that may potentially increase whole-blood tacrolimus concentrations are various calcium antagonists (diltiazem, nicardipine, nifedipine and verapamil), imidazole antifungal agents (clotrimazole, fluconazole, itraconazole and ketoconazole), macrolide antibacterial agents (clarithromycin and erythromycin), prokinetic agents (cisapride and metoclopramide), and other drugs (bromocriptine, cimetidine, corticosteroids, cyclosporin, danazol and protease inhibitors) and grapefruit juice. Enzyme inducers that may decrease tacrolimus concentrations include certain anticonvulsants (carbamazepine, phenobarbital and phenytoin), as well as rifabutin and rifampicin (rifampin).
Tacrolimus is an established agent for primary immunosuppression and rescue therapy in solid organ transplant and bone marrow transplant (BMT) recipients. Typically, protocols for tacrolimus-based primary immunosuppression initially included corticosteroids and, in general, azathioprine or mycophenolate mofetil, with some patients also receiving adjunctive antilymphocyte antibody therapy. Rescue therapy with tacrolimus involved conversion from cyclosporin to tacrolimus, generally without modification of concomitant drug therapy. Unless stated otherwise, all analyses were intent-to-treat and clinical trials (n > 100 patients per trial) evaluating primary immunosuppression were prospective, randomised, nonblind and multicentre in design.
Renal transplantation: At 5 years’ follow-up, tacrolimus provided better efficacy than cyclosporin microemulsion in intent-to-treat analyses, in terms of graft survival (79% vs 54%; p < 0.0001), the number of patients who switched to the other calcineurin inhibitor (5% vs 27% of cyclosporin microemulsion recipients; p < 0.001) and in terms of treatment failure (21% vs 56%; p < 0.001). At earlier timepoints (12–36 months post-transplantation), patient- and graft-survival rates were similar in both treatment groups in three recent trials. Notably, at 6 months’ follow-up, the incidence of biopsy-proven acute rejection episodes was significantly lower with tacrolimus-based treatment than with cyclosporin microemulsion therapy (19.6% vs 37.3%; p < 0.001) in the largest trial. Tacrolimus recipients also showed better renal function than cyclosporin microemulsion recipients at up to 5 years’ follow-up, as assessed by serum creatinine levels and glomerular filtration rates.
Dual therapy with tacrolimus-based immunosuppression provided equivalent efficacy to tacrolimus-based triple therapy at up to 36 months’ follow-up in adult renal transplant recipients. In two other trials, corticosteroid therapy could effectively be withdrawn from tacrolimus-based immunosuppression. Preliminary data from prospective trials (n = 104–266 evaluable patients) indicated that tacrolimus in combination with sirolimus and a corticosteroid provided effective immunosuppression therapy in renal transplant recipients. A reduced dosage of tacrolimus in combination with sirolimus and a corticosteroid was as effective as the same regimen with standard dosages of tacrolimus in one of these trials.
Tacrolimus-based rescue therapy is effective in adult patients with persistent acute or chronic rejection or drug-related toxicity during cyclosporin microemulsion treatment after renal transplant, typically improving serum lipid profiles and reversing chronic rejection.
In general, the efficacy of tacrolimus-based primary immunosuppression and rescue therapy for children and adolescents who received renal transplants was similar to that reported in adults. Notably, tacrolimus recipients showed better efficacy in terms of the incidence of biopsy-proven acute and corticosteroid-resistant rejection episodes at 6 months’ follow-up than cyclosporin microemulsion treatment when used for primary immunosuppression.
Two large nonrandomised, single-centre studies in adult renal transplant recipients indicated that tacrolimus-based immunosuppressive regimens improved disease-specific quality of life (QOL) compared with cyclosporin-based regimens.
Liver transplantation: At 12 months’ follow-up, tacrolimus-based immunosuppression provided better efficacy than cyclosporin microemulsion in terms of patient survival in a prospective, multicentre trial in 606 liver transplant recipients. There were also significantly fewer retransplantations (4% vs 10% of patients; p < 0.05) and treatment failures for immunological reasons (2% vs 4%; p < 0.05) with tacrolimus treatment than with cyclosporin microemulsion therapy, with a significantly greater proportion of tacrolimus recipients achieving the primary outcome at this timepoint (freedom from death, retransplantation or treatment failure for immunological reasons) [21% vs 32%, p = 0.001; time-to-event analysis log-rank test p = 0.002]. Furthermore, graft survival favoured tacrolimus recipients although this difference was not statistically significant (80% vs 66% in the cyclosporin microemulsion group). In a retrospective trial and two single-centre trials, tacrolimus rescue therapy was effective in adult liver transplant recipients experiencing acute cellular or chronic rejections, or drug-related toxicity during cyclosporin microemulsion treatment.
In children and adolescent liver transplant recipients receiving tacrolimus-based primary immunosuppression, patient (93.4% vs 92.2%) and graft survival (92.3% vs 85.4%) rates were similar to those in the cyclosporin microemulsion group at 12 months. However, biopsy-proven acute rejection (44.5% vs 59.8%; p < 0.05) and corticosteroid-resistant rejection (6% vs 29.6%; p < 0.001) rates were significantly lower with tacrolimus treatment. The efficacy of tacrolimus rescue therapy in children and adolescent liver transplant patients was similar to that observed in adults.
Heart transplantation: Recent trials have shown that tacrolimus-based regimens provided effective primary immunosuppression in adult heart transplant recipients, with similar patient survival rates at 22–36 months (76–97%) to those achieved with cyclosporin microemulsion-based therapy (72–95%). All analyses were on-treatment. In general, fewer recipients of tacrolimus-based immunosuppression experienced acute rejection episodes than cyclosporin recipients, although this difference was not always statistically significant. Tacrolimus-based primary immunosuppression provided statistically significant and clinically relevant improvements in health-related QOL from baseline, with improvements generally occurring earlier and to a greater extent in the tacrolimus group than in the cyclosporin group (standard formulation).
In several small studies in adult heart transplant recipients, tacrolimus-based rescue therapy was effective in the vast majority of patients at up to 3 years of follow-up, with patients showing marked improvements in systolic and diastolic blood pressure, total serum cholesterol levels and triglyceride levels. Furthermore, tacrolimus rescue therapy stabilised lung function at up to 1-year follow-up in recipients with bronchiolitis obliterans syndrome at the time of conversion from cyclosporin.
Lung transplantation: In prospective trials, tacrolimus-based primary immunosuppression was at least as effective as cyclosporin-based regimens (formulation not specified) in adult lung transplant recipients. Patient survival at 12 months was ≥73% in the tacrolimus groups versus >-72% with cyclosporin-based immunosuppression. Although in one trial, the incidence of acute rejection episodes per 100 patient-days was appreciably lower in tacrolimus than cyclosporin recipients, in the larger trial there was no between-group difference in this parameter. Also, significantly fewer tacrolimus than cyclosporin recipients required crossover to the alternative immunosuppressant because of rejection or other reasons in this latter trial (9% vs 33% of recipients; p = 0.0004). Tacrolimus-based immunosuppression also proved effective as rescue therapy in adult lung transplant recipients in small nonrandomised studies and a large retrospective study. In the latter study, there was a marked reduction in the mean number of histologically and clinically diagnosed rejection episodes after conversion. Moreover, all studies suggested that the rate of decline in pulmonary function (based on forced expiratory volume in 1 second) may have decreased or lung function may even be improved with tacrolimus rescue therapy in patients who developed bronchiolitis obliterans syndrome while receiving cyclosporin-based immunosuppression.
Simultaneous pancreas and kidney transplantation: Tacrolimus-based immunosuppression was at least as effective as cyclosporin microemulsion therapy in adult simultaneous pancreas and kidney (SPK) transplant recipients in a recent large, randomised trial. Pancreas graft survival was significantly better at 1 year in the tacrolimus group than the cyclosporin group (91.2% vs 73.9%; p < 0.001), although there was no between-group difference in patient or kidney graft survival. Tacrolimus recipients also experienced better efficacy in terms of biopsy-proven rejection episodes of grades 2 and 3, and in the duration of the initial hospital stay. In two single-centre studies, the majority of SPK recipients receiving tacrolimus-based immunosuppression were effectively withdrawn from corticosteroid treatment at some point post-transplantation.
Bone marrow transplantation: At 2–2.5 years’ follow-up, the incidence of grade II–IV acute graft-versus-host disease (GVHD) was consistently lower with tacrolimus-than cyclosporin-based immunosuppression after allogenic BMT in two trials. Kaplan-Meier estimates for the probability of survival were not significantly different between treatment groups. Furthermore, the severity of acute GVHD across all grades was markedly reduced in the tacrolimus group compared with the cyclosporin group. In general, tacrolimus rescue therapy proved effective in patients who developed acute or chronic GVHD, or drug-related toxicity during cyclosporin primary immunosuppression.
Commonly reported treatment-emergent adverse events associated with tacrolimus-based immunosuppression included nephrotoxicity, neurotoxicity, diarrhoea and other GI disturbances, increased risk of infections (viral, bacterial and fungal) and malignancies, hypertension and disturbances in glucose metabolism. All of these adverse events also occurred with cyclosporin-based immunosuppression. Furthermore, tacrolimus recipients showed better renal function than cyclosporin microemulsion recipients at up to 5 years’ follow-up, as assessed by serum creatinine levels and glomerular filtration rates.
Tacrolimus is associated with a lower incidence of hypertension and hypercholesterolaemia than cyclosporin, but a higher incidence of diarrhoea, disturbances in glucose metabolism and some types of neurotoxicity. In addition, tacrolimus is only rarely associated with the cyclosporin-specific adverse effects hirsutism, gum hyperplasia and gingivitis, but it may cause alopecia and pruritus. Virtually all patients receiving a calcineurin inhibitor experienced at least one treatment-emergent adverse event. Many adverse events are dose dependent and respond to dosage reduction.
Post-transplant diabetes mellitus (PTDM) is one of the more serious metabolic disorders associated with calcineurin inhibitor treatment. In general, recent large clinical trials have revealed no between-group difference in the incidence of PTDM with tacrolimus treatment and cyclosporin microemulsion treatment.
Several studies have demonstrated that serum lipid profiles and the cardiovascular risk profile were affected less by tacrolimus than by cyclosporin, with tacrolimus recipients experiencing lower serum total cholesterol and triglyceride levels, and higher high density lipoprotein cholesterol levels. Mild to moderate hypertension has been documented in up to 50% of transplant recipients receiving tacrolimus-based immunosuppression and has usually been managed effectively with antihypertensive agents.
All immunosuppressive agents also increase the risk of developing malignancy, particularly lymphoma and malignancy of the skin. The incidence of Epstein-Barr virus-related post-transplant lymphoproliferative disorder (PTLD) in adult transplant recipients receiving tacrolimus therapy is typically less than 2% and appears to be similar to that in cyclosporin recipients, although the incidence in paediatric liver transplant recipients may be higher with tacrolimus treatment than with cyclosporin therapy. However, this finding may have been a result of the significantly higher mortality rate at 3 years post-transplantation in the cyclosporin than in the tacrolimus group (32% vs 15%; p < 0.05).
The risks of tacrolimus treatment during pregnancy appear to be no greater than those associated with cyclosporin microemulsion treatment.
Pharmacoeconomic studies post-transplantation demonstrated a cost advantage for tacrolimus-based immunosuppression compared with cyclosporin microemulsion-based immunosuppression as a result of a lower rate of acute rejection in patients treated with tacrolimus.
In renal transplant recipients, intent-to-treat cost-effectiveness analyses of direct medical costs, from a randomised prospective trial over a period of 2.7 years and in two retrospective analyses of 6-month data, demonstrated that tacrolimus-based therapy was more cost effective than cyclosporin-based therapy. In all analyses, the higher acquisition cost of tacrolimus was more than offset by the costs associated with the higher rate of acute rejection in the cyclosporin groups. For example, in the randomised study the rate of acute rejection was 13% in the tacrolimus group and 24% in the cyclosporin group. Although the total average cost per patient was higher with tacrolimus treatment, better clinical outcomes associated with tacrolimus led to more favourable cost effectiveness compared with cyclosporin in terms of cost per survivor (£20 033 vs £20 374), cost per patient with a functioning graft (£21 555 vs £22 670) and cost per patient with a rejection-free graft (£29 359 vs £34 246). Year of costings was not reported.
A cost-minimisation analysis of a 6-month study demonstrated cost differences between the two treatment groups in favour of tacrolimus for total cost per patient (€1776), cost per survivor with a functioning graft (€2305) and cost per survivor (€1892). In a sensitivity analysis, the cost advantage for tacrolimus over cyclosporin was maintained when the unit costs of the main cost drivers were varied (e.g. hospitalisation and study drug by ±50% and concomitant medication by ±25%). These costs were based on an Italian hospital perspective, with the year of costings not reported.
In liver transplant recipients, a 6-month cost analysis demonstrated a lower total cost of rejection and drugs in the tacrolimus group compared with the cyclosporin group ($US434 300 vs $US1 305 300 for every 100 patients).
Dosage and Administration
Tacrolimus is indicated for primary immunosuppressive therapy following kidney and liver transplantation in greater than 60 countries and for heart transplantation in some of these countries; it is also approved as rescue therapy for a variety of solid solid organ transplants in more than 60 countries.
Tacrolimus should be taken orally in two divided doses at intervals of 12 hours. Administration via continuous intravenous infusion carries the risk of anaphylaxis, but may be used in the short term if oral therapy is not possible. When switching from intravenous to oral therapy, the first oral dose should be administered 8–12 hours after discontinuing the infusion.
The first dose of tacrolimus should be given no sooner than 6 hours after liver transplantation and within 24 hours of kidney transplantation. The recommended starting dosage of oral tacrolimus in adults ranges from approximately 0.1–0.3 mg/kg/day. The dose may be reduced during maintenance therapy, and should be titrated based on clinical assessments of rejection and tolerability for each patient.
Children generally require higher doses (on a milligram per kilogram basis) than adults to achieve similar whole-blood concentrations of tacrolimus. Low dosages are recommended in patients with renal or hepatic dysfunction. Tacrolimus may be given as rescue therapy, but should not be initiated until approximately 24 hours after the discontinuation of cyclosporin.
It is recommended that tacrolimus be taken on an empty stomach to maximise absorption. Trough whole-blood tacrolimus concentrations should be monitored and, generally, should be maintained below 20 μg/L.
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