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Meta-Analysis
. 2015 Dec 3;2015(12):CD007746.
doi: 10.1002/14651858.CD007746.pub2.

Mycophenolic acid versus azathioprine as primary immunosuppression for kidney transplant recipients

Martin Wagner  1 , Amy K Earley, Angela C Webster, Christopher H Schmid, Ethan M Balk, Katrin Uhlig
Affiliations
Meta-Analysis

Mycophenolic acid versus azathioprine as primary immunosuppression for kidney transplant recipients

Martin Wagner et al. Cochrane Database Syst Rev. .

Abstract

Background: Modern immunosuppressive regimens after kidney transplantation usually use a combination of two or three agents of different classes to prevent rejection and maintain graft function. Most frequently, calcineurin-inhibitors (CNI) are combined with corticosteroids and a proliferation-inhibitor, either azathioprine (AZA) or mycophenolic acid (MPA). MPA has largely replaced AZA as a first line agent in primary immunosuppression, as MPA is believed to be of stronger immunosuppressive potency than AZA. However, treatment with MPA is more costly, which calls for a comprehensive assessment of the comparative effects of the two drugs.

Objectives: This review of randomised controlled trials (RCTs) aimed to look at the benefits and harms of MPA versus AZA in primary immunosuppressive regimens after kidney transplantation. Both agents were compared regarding their efficacy for maintaining graft and patient survival, prevention of acute rejection, maintaining graft function, and their safety, including infections, malignancies and other adverse events. Furthermore, we investigated potential effect modifiers, such as transplantation era and the concomitant immunosuppressive regimen in detail.

Search methods: We searched Cochrane Kidney and Transplant's Specialised Register (to 21 September 2015) through contact with the Trials' Search Co-ordinator using search terms relevant to this review.

Selection criteria: All RCTs about MPA versus AZA in primary immunosuppression after kidney transplantation were included, without restriction on language or publication type.

Data collection and analysis: Two authors independently determined study eligibility, assessed risk of bias and extracted data from each study. Statistical analyses were performed using the random-effects model and the results were expressed as risk ratio (RR) for dichotomous outcomes and mean difference (MD) for continuous outcomes with 95% confidence intervals (CI).

Main results: We included 23 studies (94 reports) that involved 3301 participants. All studies tested mycophenolate mofetil (MMF), an MPA, and 22 studies reported at least one outcome relevant for this review. Assessment of methodological quality indicated that important information on factors used to judge susceptibility for bias was infrequently and inconsistently reported.MMF treatment reduced the risk for graft loss including death (RR 0.82, 95% CI 0.67 to 1.0) and for death-censored graft loss (RR 0.78, 95% CI 0.62 to 0.99, P < 0.05). No statistically significant difference for MMF versus AZA treatment was found for all-cause mortality (16 studies, 2987 participants: RR 0.95, 95% CI 0.70 to 1.29). The risk for any acute rejection (22 studies, 3301 participants: RR 0.65, 95% CI 0.57 to 0.73, P < 0.01), biopsy-proven acute rejection (12 studies, 2696 participants: RR 0.59, 95% CI 0.52 to 0.68) and antibody-treated acute rejection (15 studies, 2914 participants: RR 0.48, 95% CI 0.36 to 0.65, P < 0.01) were reduced in MMF treated patients. Meta-regression analyses suggested that the magnitude of risk reduction of acute rejection may be dependent on the control rate (relative risk reduction (RRR) 0.34, 95% CI 0.10 to 1.09, P = 0.08), AZA dose (RRR 1.01, 95% CI 1.00 to 1.01, P = 0.10) and the use of cyclosporin A micro-emulsion (RRR 1.27, 95% CI 0.98 to 1.65, P = 0.07). Pooled analyses failed to show a significant and meaningful difference between MMF and AZA in kidney function measures.Data on malignancies and infections were sparse, except for cytomegalovirus (CMV) infections. The risk for CMV viraemia/syndrome (13 studies, 2880 participants: RR 1.06, 95% CI 0.85 to 1.32) was not statistically significantly different between MMF and AZA treated patients, whereas the likelihood of tissue-invasive CMV disease was greater with MMF therapy (7 studies, 1510 participants: RR 1.70, 95% CI 1.10 to 2.61). Adverse event profiles varied: gastrointestinal symptoms were more likely in MMF treated patients and thrombocytopenia and elevated liver enzymes were more common in AZA treatment.

Authors' conclusions: MMF was superior to AZA for improvement of graft survival and prevention of acute rejection after kidney transplantation. These benefits must be weighed against potential harms such as tissue-invasive CMV disease. However, assessment of the evidence on safety outcomes was limited due to rare events in the observation periods of the studies (e.g. malignancies) and inconsistent reporting and definitions (e.g. infections, adverse events). Thus, balancing benefits and harms of the two drugs remains a major task of the transplant physician to decide which agent the individual patient should be started on.

PubMed Disclaimer

Conflict of interest statement

  1. In the past 5 years, MW received travel grants from Genzyme

  2. In the past 5 years, CS received grants from Blue Cross Blue Shield, TEVA Pharma and Glaxo Smith Kline

  3. AE, AW, EB and KU do not have any known conflicts of interest

Figures

1
1
Literature search and identification of studies
2
2
Risk of bias graph: review authors' judgements about each risk of bias item presented as percentages across all included studies.
3
3
Risk of bias summary: review authors' judgements about each risk of bias item for each included study.
4
4
Meta‐regression of logarithmic relative risk of death censored graft loss by MMF dose (panel A) and by control rate (panel B)
5
5
Meta‐regression of logarithmic relative risk of any acute rejection by year of transplantation (panel A), AZA‐dose (panel B), MMF‐dose (panel C) and by control rate (panel D)
6
6
Meta‐regression of mean difference in serum creatinine (mg/dL) by AZA dose (panel A), and by MMF dose (panel B)
7
7
Funnel plots of outcomes. Graft loss: censored for death (panel A, Analysis 1.3); acute rejection: total (panel B, Analysis 1.6); Infection: cytomegalovirus viraemia/syndrome (panel C, Analysis 1.11)
1.1
1.1. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 1 Death: all cause.
1.2
1.2. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 2 Graft loss: including death.
1.3
1.3. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 3 Graft loss: censored for death.
1.4
1.4. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 4 Primary non‐function.
1.5
1.5. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 5 Malignancy: longest duration of follow‐up.
1.6
1.6. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 6 Acute rejection: total.
1.7
1.7. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 7 Acute rejection: confirmed by biopsy.
1.8
1.8. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 8 Acute rejection: steroid resistant/antibody treated.
1.9
1.9. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 9 Chronic allograft nephropathy.
1.10
1.10. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 10 Infection: other (longest duration of follow‐up).
1.11
1.11. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 11 Infection: CMV viraemia/syndrome.
1.12
1.12. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 12 Infection: CMV tissue invasive.
1.13
1.13. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 13 Graft function: serum creatinine.
1.14
1.14. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 14 Graft function: CrCl/GFR.
1.15
1.15. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 15 Graft function: proteinuria.
1.16
1.16. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 16 Graft function: proteinuria.
1.17
1.17. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 17 Adverse events: gastrointestinal (longest duration of follow‐up).
1.18
1.18. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 18 Adverse events: other (longest duration of follow‐up).
1.19
1.19. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 19 Adverse events: haematological (longest duration of follow‐up).
1.20
1.20. Analysis
Comparison 1 Mycophenolate mofetil versus azathioprine, Outcome 20 Total cholesterol.
2.1
2.1. Analysis
Comparison 2 Subgroup analyses: RCT versus quasi‐RCT, Outcome 1 Graft loss: censored for death.
2.2
2.2. Analysis
Comparison 2 Subgroup analyses: RCT versus quasi‐RCT, Outcome 2 Acute rejection (total).
2.3
2.3. Analysis
Comparison 2 Subgroup analyses: RCT versus quasi‐RCT, Outcome 3 Infection: CMV viraemia/syndrome.
2.4
2.4. Analysis
Comparison 2 Subgroup analyses: RCT versus quasi‐RCT, Outcome 4 Graft function, serum creatinine.
3.1
3.1. Analysis
Comparison 3 Subgroup analyses: ITT analysis, Outcome 1 Graft loss: censored for death.
3.2
3.2. Analysis
Comparison 3 Subgroup analyses: ITT analysis, Outcome 2 Acute rejection: total.
3.3
3.3. Analysis
Comparison 3 Subgroup analyses: ITT analysis, Outcome 3 Infection: CMV viraemia/syndrome.
3.4
3.4. Analysis
Comparison 3 Subgroup analyses: ITT analysis, Outcome 4 Graft function: serum creatinine.
4.1
4.1. Analysis
Comparison 4 Subgroup analyses: adults only versus children included, Outcome 1 Graft loss: censored for death.
4.2
4.2. Analysis
Comparison 4 Subgroup analyses: adults only versus children included, Outcome 2 Acute rejection: total.
4.3
4.3. Analysis
Comparison 4 Subgroup analyses: adults only versus children included, Outcome 3 Infection: CMV viraemia/syndrome.
4.4
4.4. Analysis
Comparison 4 Subgroup analyses: adults only versus children included, Outcome 4 Graft function: serum creatinine.
5.1
5.1. Analysis
Comparison 5 Subgroup analyses: industry versus non‐industry funding, Outcome 1 Graft loss: censored for death.
5.2
5.2. Analysis
Comparison 5 Subgroup analyses: industry versus non‐industry funding, Outcome 2 Acute rejection: total.
5.3
5.3. Analysis
Comparison 5 Subgroup analyses: industry versus non‐industry funding, Outcome 3 Infection: CMV viraemia/syndrome.
5.4
5.4. Analysis
Comparison 5 Subgroup analyses: industry versus non‐industry funding, Outcome 4 Graft function: serum creatinine.
6.1
6.1. Analysis
Comparison 6 Subgroup analyses: publication type, Outcome 1 Graft loss: censored for death.
6.2
6.2. Analysis
Comparison 6 Subgroup analyses: publication type, Outcome 2 Acute rejection: total.
6.3
6.3. Analysis
Comparison 6 Subgroup analyses: publication type, Outcome 3 Infection: CMV viraemia/syndrome.
6.4
6.4. Analysis
Comparison 6 Subgroup analyses: publication type, Outcome 4 Graft function: serum creatinine.
See this image and copyright information in PMC

Update of

  • doi: 10.1002/14651858.CD007746

References

References to studies included in this review

Army Hospital 2002 {published data only}
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    1. Wlodarczyk Z, Glyda M, Paczek L, Ostrowski M, Marcinkowski W, Klinger M, et al. Long‐term results of steroid withdrawal following renal transplantation in tacrolimus‐based immunosuppression regimens ‐ results of multicenter study [abstract no: 25]. 3rd International Congress on Immunosuppression; 2004 Dec 8‐11; San Diego, CA. 2004. [CENTRAL: CN‐00550597]
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Egfjord 1999 {published data only}
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Folkmane 2001 {published data only}
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Isbel 1997 {published data only}
    1. Isbel NM, Smith KG, Leydon JA, Walker RG, Becker GJ. Mycophenolate mofetil suppresses the humoral response to influenza vaccination in renal transplant recipients [abstract no: P1014]. Nephrology 1997;3(Suppl 1):S327. [CENTRAL: CN‐00460991]
Ji 2001 {published data only}
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Joh 2005 {published data only}
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Johnson 2000 {published data only}
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    1. Gonwa T, Johnson C, Ahsan N, Alfrey EJ, Halloran P, Stegall M, et al. Randomized trial of tacrolimus + mycophenolate mofetil or azathioprine versus cyclosporine + mycophenolate mofetil after cadaveric kidney transplantation: results at three years. Transplantation 2003;75(12):2048‐53. [MEDLINE: ] - PubMed
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    1. Gonwa TA, FK506/MMF Study Trial Group. Two year follow‐up of a randomized trial of FK506 + MMF vs FK506 + AZA vs CyA + MMF [abstract]. XVIII International Congress of the Transplantation Society; 2000 Aug 27‐Sep 1; Rome, Italy. 2000. [CENTRAL: CN‐00433630]
Keven 2003 {published data only}
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Ling 1998 {published data only}
    1. Ling JY, Zhu Y, Shun FK. Combined use of MMF with low dosage of cyclosporine A in renal transplantation. Chinese Journal of Organ Transplantation 1998;19(3):175‐6.
Mendez 1998 {published data only}
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Merville 2004 {published data only}
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Miladipour 2002 {published data only}
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MMF TRI Study 1996 {published data only}
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MMF US Study 1995 {published data only}
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MYSS Study 2004 {published data only}
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Sadek 2002 {published data only}
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    1. Sadek S, Vogt B, Beauregard‐Zllinger L, Prestele H, Neoral Phase IV Study Group. Short‐term combination of mycophenolate mofetil with cyclosporine as a safe therapeutic option for renal transplant recipients [abstract]. Transplantation 2000;69(8 Suppl):S160. [CENTRAL: CN‐00447538] - PubMed
    1. Sadek SA, Vogt B, Beauregard‐Zollinger L, Neoral Phase IV Study Group. Short‐term mycophenolate mofetil combined with cyclosporine compared to standard maintenance regimens of cyclosporine with mycophenolate mofetil or azathioprine in kidney transplantation: interim analysis [abstract no: 927]. Transplantation 1999;67(7):S238. [CENTRAL: CN‐00766427]
    1. Vogt B, Sadek S, Phase IV Neonatal Study Group. Short‐term combination of mycophenolate mofetil with cyclosporine as a safe therapeutive option in renal transplantation [abstract]. XVIII International Congress of the Transplantation Society; 2000 Aug 27‐Sep 1; Rome, Italy. 2000. [CENTRAL: CN‐00448227]
Suhail 2000 {published data only}
    1. Suhail SM, Vathsala A, Lou HX, Woo KT. Safety and efficacy of mycophenolate mofetil for prophylaxis in Asian renal transplant recipients. Transplantation Proceedings 2000;32(7):1757‐8. [MEDLINE: ] - PubMed
    1. Vathsala A, Lou H, Suhail SM, Woo K. Does 6 months prophylaxis with mycophenolate mofetil reduce acute rejection in renal transplantation? [abstract]. Journal of the American Society of Nephrology 2000;11(Sept):711A. [CENTRAL: CN‐00583822]
Sun 2002b {published data only}
    1. Sun CC, Hao JW, Sun J, Yang DA. A comparison between therapeutic effects of mycophenolate mofetil and azathioprine in the management of patients after renal transplantation. Yiyao Dao Bao [Herald of Medicine] 2002;21(9):544‐6. [CENTRAL: CN‐00429261]
Tuncer 2002 {published data only}
    1. Tuncer M, Gurkan A, Erdogan O, Demirbas A, Suleymanlar G, Ersoy FF, et al. Mycophenolate mofetil in renal transplantation: five years experience. Transplantation Proceedings 2002;34(6):2087‐8. [MEDLINE: ] - PubMed
Weimer 2002 {published data only}
    1. Weimer R, Deisz S, Dietrich H, Renner F, Bodeker RH, Daniel V, et al. Impact of maintenance immunosuppressive regimens‐‐balance between graft protective suppression of immune functions and a near physiological immune response. Transplant International 2011;24(6):596‐609. [MEDLINE: ] - PubMed
    1. Weimer R, Deisz S, Dietrich H, Yildiz S, Staak A, Renner F, et al. Impact of maintenance immunosuppressive regimens on immunological parameters of graft outcome [abstract no: P101]. Transplant International 2007;20(Suppl 2):120.
    1. Weimer R, Deisz S, Renner F, Dietrich H, Daniel V, Kamali‐Ernst S, et al. Different impact of maintenance immunosuppressive regimens on the immune response of renal transplant recipients [abstract no: 112]. Transplantation 2008;86(2 Suppl):40. [CENTRAL: CN‐00671788]
    1. Weimer R, Deisz S, Renner F, Dietrich H, Suesal C, Kamali‐Ernst S, et al. Impact of steroid withdrawal on the immune response of renal transplant recipients [abstract no: O‐249]. Transplant International 2009;22(Suppl 2):66.
    1. Weimer R, Ettrich M, Renner F, Dietrich H, Susal C, Deisz S, et al. ATG induction in renal transplant recipients: Long‐term hazard of severe infection is associated with long‐term functional T cell impairment but not the ATG‐induced CD4 cell decline. Human Immunology 2014;75(6):561‐9. [MEDLINE: ] - PubMed

References to studies excluded from this review

Araujo 1999 {published data only}
    1. Araujo MR, Oliveira AC, Abensur H, Marcondes M, Romao JE, Zatz R, et al. Mycopheolate mofetil (MMF) in the treatment of chronic renal allograft rejection: a three‐year follow‐up [abstract]. Journal of the American Society of Nephrology 1999;10(Program & Abstracts):719A. [CENTRAL: CN‐00550469]
Asci 2002 {published data only}
    1. Asci G, Toz H, Ok E, Sezis M, Basci A. No benefit from mycophenolate mofetil in renal transplant recipients with chronic allograft nephropathy [abstract no: O56]. Nephrology Dialysis Transplantation 2002;17(Suppl 1):18. [MEDLINE: ]
Baek 2004 {published data only}
    1. Baek H, Huh W, Kim JA, Kim Y, Kim DJ, Oh H, et al. Efficacy of mycophenolate mofetil and azathiporine therapy in paired cadaveric renal transplantation: five‐year experience [abstract]. 41st Congress. European Renal Association. European Dialysis and Transplantation Association; 2004 May 15‐18; Lisbon, Portugal. 2004:402. [CENTRAL: CN‐00509077]
Bataille 2010 {published data only}
    1. Bataille S, Moal V, Gaudart J, Indreies M, Purgus R, Dussol B, et al. Cytomegalovirus risk factors in renal transplantation with modern immunosuppression. Transplant Infectious Disease 2010;12(6):480‐8. [MEDLINE: ] - PubMed
Benfield 1999 {published data only}
    1. Benfield MR, Herrin J, Feld L, Rose S, Stablein D, Tejani A. Safety of kidney biopsy in pediatric transplantation: a report of the Controlled Clinical Trials in Pediatric Transplantation Trial of Induction Therapy Study Group. Transplantation 1999;67(4):544‐7. [MEDLINE: ] - PubMed
    1. Benfield MR, Symons JM, Bynon S, Eckhoff D, Herrin J, Harmon W, et al. Mycophenolate mofetil in pediatric renal transplantation. Pediatric Transplantation 1999;3(1):33‐7. [MEDLINE: ] - PubMed
    1. Benfield MR, Tejani A, Harmon WE, McDonald R, Stablein DM, McIntosh M, et al. A randomized multicenter trial of OKT3 mAbs induction compared with intravenous cyclosporine in pediatric renal transplantation. Pediatric Transplantation 2005;9(3):282‐92. [MEDLINE: ] - PubMed
    1. Tejani A. A randomized prospective multicenter trial of T‐cell antibody induction therapy in pediatric renal transplantation [abstract]. XVIII International Congress of the Transplantation Society; 2000 Aug 27‐Sep 1; Rome, Italy. 2000.
    1. Tejani A, Harmon W, Benfield M, Elshihabi I, McDonald R, Stablein D, et al. A randomized prospective multicenter trial of T‐cell antibody induction therapy in pediatric renal transplantation [abstract]. Transplantation 2000;69(8 Suppl):S111. [CENTRAL: CN‐00402826]
Boletis 1999b {published data only}
    1. Boletis JN, Stamatiadis D, Markis F, Konstandinidou I, Theodosis I, Mansour M, et al. Mycophenolate mofetil in renal transplantation [abstract]. Nephrology Dialysis Transplantation 1999;14:2975. [CENTRAL: CN‐00278914]
Brennan 2005 {published data only}
    1. Agha IA, Hardinger KL, Bohl D, Ansari A, Dyk P, Koch M, et al. Preemptive withdrawal of AZA or MMF prevents progression of BK viremia to BK nephropathy: a prospective randomized controlled trial of BK virus infection after renal transplantation [abstract]. American Journal of Transplantation 2004;4(Suppl 8):200. [CENTRAL: CN‐00509045]
    1. Bohl DL, Storch GA, Ryschkewitsch C, Gaudreault‐Keener M, Schnitzler MA, Major EO, et al. Donor origin of BK virus in renal transplantation and role of HLA C7 in susceptibility to sustained BK viremia. American Journal of Transplantation 2005;5(9):2213‐21. [MEDLINE: ] - PubMed
    1. Brennan DC, Agha I, Bohl DL, Schnitzler MA, Hardinger KL, Lockwood M, et al. Incidence of BK with tacrolimus versus cyclosporine and impact of preemptive immunosuppression reduction.[erratum appears in Am J Transplant. 2005 Apr;5(4 Pt 1):839]. American Journal of Transplantation 2005;5(3):582‐94. [MEDLINE: ] - PubMed
    1. Brennan DC, Bohl DL, Storch GA, Major EO, Agha IA, Schnitzler MA. High donor antibody level and HLA C7 predict sustained BK‐polyoma viremia: results of a randomized prospective trial [abstract no: P817]. Transplantation 2004;78(2 Suppl):488. [CENTRAL: CN‐00644222]
    1. Hardinger KL, Bohl DL, Schnitzler MA, Lockwood M, Storch GA, Brennan DC. A randomized, prospective, pharmacoeconomic trial of tacrolimus versus cyclosporine in combination with thymoglobulin in renal transplant recipients. Transplantation 2005;80(1):41‐6. [MEDLINE: ] - PubMed
Cransberg 2007 {published data only}
    1. Cransberg K, Cornelissen M, Lilien M, Hoeck K, Davin JC, Nauta J. Maintenance immunosuppression with mycophenolate mofetil and corticosteroids in pediatric kidney transplantation: temporary benefit but not without risk. Transplantation 2007;83(8):1041‐7. [MEDLINE: ] - PubMed
El‐Agroudy 2009 {published data only}
    1. El‐Agroudy AE, El‐Dahshan KF, Wafa EW, Sheashaa HA, Gad ZA, Ismail AM, et al. Safe conversion of mycophenolate mofetil to azathioprine in kidney transplant recipients with sirolimus‐based immunosuppression. Nephrology 2009;14(2):255‐61. [MEDLINE: ] - PubMed
    1. El‐Dahshan K, El‐Agroudy A, Wafa E, Gad Z. Safe conversion of mycophenolate mofetil to azathioprine in kidney transplant recipients with sirolimus‐based immunosuppression [abstract no: Su711]. World Congress of Nephrology; 2009 May 22‐26; Milan, Italy. 2009. - PubMed
Ettenger 1995 {published data only}
    1. Ettenger R, Mentser BW, Potter D, Cohen A. Mycophenolate mofetil (MMF) in pediatric (PED) renal transplantation (TX): a report of the PED MMF study group [abstract]. Journal of the American Society of Nephrology 1995;6(3):1082. [CENTRAL: CN‐00483891]
Griffin 2003 {published data only}
    1. Griffin MD, Slezak JM, Kozel TK, Bergstralh EJ, Schwab TR, Gloor JM, et al. Renal function loss in chronic allograft nephropathy: results of a two‐year study of mycophenolate mofetil substitution for azathioprine [abstract]. American Journal of Transplantation 2003;3(Suppl 5):223. [CENTRAL: CN‐00445554]
Ha 2004 {published data only}
    1. Ha J, Yun IJ, Lee JH, Choi SJ, Kang JM, Kim SJ. Azathioprine combination therapy can stably reduce cyclosporine dose as mycophenolate mofetil combination therapy for the recipients showing stable renal function after renal transplantation [abstract no: P‐19]. 3rd International Congress on Immunosuppression; 2004 Dec 8‐11; San Diego (CA). 2004. [CENTRAL: CN‐00583458]
Hernandez 2007 {published data only}
    1. Hernandez D, Miquel R, Porrini E, Fernandez A, Gonzalez‐Posada JM, Hortal L, et al. Randomized controlled study comparing reduced calcineurin inhibitors exposure versus standard cyclosporine‐based immunosuppression. Transplantation 2007;84(6):706‐14. [MEDLINE: ] - PubMed
Jain 2001 {published data only}
    1. Jain S, Metcalfe M, White SA, Furness PN, Nicholson ML. Chronic allograft nephropathy: a prospective randomised trial of cyclosporin reduction with or without mycophenolate mofetil. Transplantation Proceedings 2001;33(3):2165‐6. [MEDLINE: ] - PubMed
    1. Jain S, Metcalfe M, White SA, Furness PN, Nicholson ML. Randomized trial comparing mycophenolate mofetil and azathioprine to allow cyclosporin reduction in chronic allograft nephropathy [abstract no: PO513W]. XVIII International Congress of the Transplantation Society; 2000 Aug 27‐Sep 1; Rome, Italy. 2000. [CENTRAL: CN‐00445890]
    1. Nicholson ML, Jain S, Metcalfe M, White SA, Furness PN. Chronic allograft nephropathy: a prospective randomised trial of cyclosporin reduction with or without mycophenolate mofetil [abstract no: 437]. Transplantation 2000;69(8 Suppl):S227. [CENTRAL: CN‐00446949] - PubMed
Jirasiritham 2000 {published data only}
    1. Jirasiritham S, Sumethkul V, Mavichak V, Chalermsanyakorn P. The treatment of chronic rejection with mycophenolate mofetil versus azathioprine in kidney transplantation. Transplantation Proceedings 2000;32(7):2040‐2. [MEDLINE: ] - PubMed
Kasiske 1997 {published data only}
    1. Kasiske BL, Johnson HJ, Heim‐Duthoy KL, Rao VK, Dahl DC, Jacobs DM, et al. Does mycophenolate mofetil improve already good results from cyclosporine induction early after renal transplantation? [abstract]. 16th Annual Meeting. American Society of Transplant Physicians (ASTP); 1997 May 10‐14; Chicago (ILL). 1997:236. [CENTRAL: CN‐00509263]
Khosroshahi 2006a {published data only}
    1. Khosroshahi HT, Asghari A, Estakhr R, Baiaz B, Ardalan MR, Shoja MM. Effects of azathioprine and mycophenolate mofetil‐immunosuppressive regimens on the erythropoietic system of renal transplant recipients. Transplantation Proceedings 2006;38(7):2077‐9. [MEDLINE: ] - PubMed
    1. Khosroshahi HT, Estakhri R, Shoja MM. Effects of azathioprine and mycophenolate mofetil based immunosuppressive regimen on the erthropoietic system of the renal transplant recipients [abstract no: SP735]. Nephrology Dialysis Transplantation 2006;21(Suppl 4):iv263. [CENTRAL: CN‐00626063] - PubMed
Kim 1999 {published data only}
    1. Kim JK, Shin YH, Park YG, Hur D, Kim MS, Lee SR. Clinical observation of mycophenolate mofetil for the prevention of acute rejection in renal transplantation [abstract]. Journal of the American Society of Nephrology 1999;10(Program & Abstracts):734A. [CENTRAL: CN‐00550544]
Langman 1996 {published data only}
    1. Langman LJ, LeGatt DF, Halloran PF, Yatscoff RW. Pharmacodynamic assessment of mycophenolic acid‐induced immunosuppression in renal transplant recipients. Transplantation 1996;62(5):666‐72. [MEDLINE: ] - PubMed
Lezaic 2005 {published data only}
    1. Lezaic V, Marinkovic J, Ristic S, Dokic Z, Radivojevic D, Blagojevic R, et al. Conversion of azathioprine to mycophenolate mofetil and chronic graft failure progression [abstract]. Transplantation 2004;78(2 Suppl):268. [CENTRAL: CN‐00509315] - PubMed
    1. Lezaic VD, Marinkovic J, Ristic S, Dokic ZM, Basta Jovanovic G, Radivojevic DM, et al. Conversion of azathioprine to mycophenolate mofetil and chronic graft failure progression. Transplantation Proceedings 2005;37(2):734‐6. [MEDLINE: ] - PubMed
Lison 2004 {published data only}
    1. Eilts V, Zantvoort F, Wullstein HG, Hillebrand GF, Gobmann J, Kachel HG, et al. Mycophenolate mofetil ‐ a solution for cyclosporine induced hypertension in kidney transplanted patients? [abstract no: T‐PO50008]. Nephrology 2005;10(Suppl 1):A209. [CENTRAL: CN‐00583349]
    1. Lison AE, Eilts V, Zantvoort F, Wullstein H. Mycophenolate mofetil‐ a solution for cyclosporine induced hypertension in kidney transplanted patients? [abstract]. Transplantation 2004;78(2 Suppl):659. [CENTRAL: CN‐00527138]
Makhdoomi 2005 {published data only}
    1. Makhdoomi K, Ahmadpoor P, Ghafari A, Yekta Z. Comparison of 1 year allograft function with mycofenolate mofetil versus azathioprine in renal transplant patients [abstract no: T‐PO50033]. Nephrology 2005;10(Suppl):A216.
Mandelbaum 1998 {published data only}
    1. Mandelbaum AP, Wiesel M, Ksoll‐Ruddek D, Zeier MG. Long‐term results of mycophenolate‐mofetil (MMF) as compared to azathioprine (AZA) in renal transplantation [abstract]. Journal of the American Society of Nephrology 1998;9(Program & Abstracts):686A. [CENTRAL: CN‐00446574]
Merion 2000 {published data only}
    1. Merion RM, Henry ML, Melzer JS, Sollinger HW, Sutherland DE, Taylor RJ. Randomized, prospective trial of mycophenolate mofetil versus azathioprine for prevention of acute renal allograft rejection after simultaneous kidney‐pancreas transplantation. Transplantation 2000;70(1):105‐11. [MEDLINE: ] - PubMed
Metcalfe 2002 {published data only}
    1. Brook NR, Metcalf MS, Jain S, Bicknell GR, Nicholson ML, Harper SJ. A randomised trial of mycophenolate mofetil versus azathioprine as calcineurin inhibitor sparing agents in the treatment of chronic allograft nephropathy [abstract no: P‐97]. 3rd International Congress on Immunosuppression; 2004 Dec 8‐11; San Diego (CA). 2004. [CENTRAL: CN‐00550372] - PubMed
    1. Brook NR, Metcalfe MS, Waller JR, Jain S, Hosgood SA, Nicholson ML. A prospective randomised trial of mycophenolate mofetil and azathioprine after calcineurin reduction in renal allografts with established chronic allograft nephropathy [abstract]. American Journal of Transplantation 2004;4(Suppl 8):485. [CENTRAL: CN‐00509106]
    1. Metcalfe MS, Jain S, Waller JR, Saunders RN, Bicknell GR, Nicholson ML. A randomized trial of mycophenolate mofetil versus azathioprine as calcineurin inhibitor sparing agents in the treatment of chronic allograft nephropathy. Transplantation Proceedings 2002;34(5):1812‐4. [MEDLINE: ] - PubMed
MMF 1998 {published data only}
    1. Mycophenolate mofetil for the treatment of a first acute renal allograft rejection: The Mycophenolate Mofetil Acute Renal Rejection Study Group.[erratum appears in Transplantation 1998 Apr 15;65(7):followi]. Transplantation 1998;65(2):235‐41. [MEDLINE: ] - PubMed
    1. Mycophenolate Mofetil Acute Renal Rejection Study Group. Mycophenolate mofetil for the treatment of a first acute renal allograft rejection: three‐year follow‐up. The Mycophenolate Mofetil Acute Renal Rejection Study Group. Transplantation 2001 Apr 27;71(8):1091‐7. [MEDLINE: ] - PubMed
    1. Pescovitz MD. Mycophenolate mofetil for the treatment of renal transplant rejection: 3 years of follow‐up [abstract no: 929]. Transplantation 1999;67(7):S239. [CENTRAL: CN‐00765711]
    1. Pirsch J, Best JH, 1912 Renal Transplant Mycophenolate Mofetil Study Group. An economic evaluation of mycophenolate mofetil (MMF) versus azathioprine (AZA) as adjunctive treatment for acute renal allograft rejection [abstract]. 16th Annual Meeting. American Society of Transplant Physicians (ASTP); 1997 May 10‐14; Chicago (IL). 1997:239. [CENTRAL: CN‐00509418]
    1. Pirsch JD, Pescovitz MD, Ferguson R, Deierhoi M, Hooftman L, Navarro M. Mycophenolate mofetil for the treatment of first acute renal allograft rejection [abstract]. 16th Annual Meeting. American Society of Transplant Physicians (ASTP); 1997 May 10‐14; Chicago (IL). 1997:261. [CENTRAL: CN‐00509419]
MO2ART Study 2003 {published data only}
    1. Balshaw R, Marra C, Nashan B, Hagenmeyer EG, Kalo Z, Keown P. Two‐hour post‐dose cyclosporine levels in renal transplantation: a cost‐effective strategy for reducing graft rejection [abstract no: 3316]. XIXth International Congress of the Transplantation Society; 2002 Aug 25‐30; Miami (FL). 2002. [CENTRAL: CN‐00415222]
    1. Buchler M, Chadban S, Cole E, Midtvedt K, Thervet E, Prestele H, et al. Evolution of the absorption profile of cyclosporine A in renal transplant recipients: a longitudinal study of the de novo and maintenance phases. Nephrology Dialysis Transplantation 2006;21(1):197‐202. [MEDLINE: ] - PubMed
    1. Buchler M, Chadban S, Jost L, Rodriguez A, Beauregard L, Balshaw R. Excellent renal tolerability of neoral C‐2h monitoring in de novo kidney transplantation: initial results of the MO2ART trial [abstract no: 1038]. American Journal of Transplantation 2002;2(Suppl 3):399. [CENTRAL: CN‐00550435]
    1. Chadban S, Pilmore H, Goodman D, Hutchison B, MO2ART SG. Minimal rejection and excellent graft function by neoral C2 monitoring in renal transplantation: interim results of MO2ART [abstract]. Transplantation Society of Australia & New Zealand (TSANZ). 21st Annual Scientific Meeting; 2003 Apr 9‐11; Canberra, Australia. 2003:65. [CENTRAL: CN‐00444732]
    1. Chadban S, Pilmore H, Goodman D, Jose M, Hutchison B, Cole E. Optimal C2 targets after month 3 for renal transplant recipients receiving cyclosporin‐microemulsion based triple therapy ‐ the MO2ART trial [abstract no: 93]. Transplantation Society of Australia & New Zealand (TSANZ). 22nd Annual Scientific Meeting; 2004 Mar 31‐Apr 2; Canberra, Australia. 2004:83. [CENTRAL: CN‐00583658]
Nowacka‐Cieciur 2000 {published data only}
    1. Nowacka‐Cieciura E, Kaminska B, Cieciura T, Gradowska L, Pazik J, Lao M, et al. Randomised open clinical trial of conversion from mycophenolate mofetil to azathioprine in cadaveric renal transplantation. Transplant International 2000;13(Suppl 1):S68‐72. [MEDLINE: ] - PubMed
Oliveira 1999 {published data only}
    1. Oliveira JG, Ramos JP, Xavier P, Sampaio S, Magalhaees M, Mandes A, et al. Lymphocyte subsets in peripheral blood and inside the allograft in renal tx treated with AZA versus MMF: CD3DR andICAM‐1 down regulation with MMF [abstract]. Nephrology Dialysis Transplantation 1999;14(9):A276. [CENTRAL: CN‐00583426]
Schurter 1997 {published data only}
    1. Schurter G, Glicklich D, Greenstein SM, Schreiber T, Mallis M, Clemetson S, et al. Mycophenolate mofetil (MMF) therapy for chronic rejection in renal transplant recipients [abstract]. 16th Annual Meeting. American Society of Transplant Physicians (ASTP); 1997 May 10‐14; Chicago (IL). 1997:133. [CENTRAL: CN‐00509469]
Smak Gregoor 2000 {published data only}
    1. Smak Gregoor PJ, Gelder T, Besouw NM, mast P, kuiper P, Ijzermans JN, et al. Long‐term follow‐up of a prospective, randomised study on minimising immunosuppressive medication from one year after kidney transplantation [abstract no: 0016]. XIXth International Congress of the Transplantation Society; 2002 Aug 25‐30; Miami (FL). 2002. [CENTRAL: CN‐00416672]
    1. Smak Gregoor PJ, Gelder T, Besouw NM, Mast BJ, IJzermans JN, Weimar W. Randomized study on the conversion of treatment with cyclosporine to azathioprine or mycophenolate mofetil followed by dose reduction. Transplantation 2000;70(1):143‐8. [MEDLINE: ] - PubMed
    1. Smak Gregoor PJ, Gelder T, Besouw NM, Mast BJ, Kuiper P, IJzermans JN, et al. Five‐year follow‐up of a prospective, randomised study on minimising immunosuppressive medication from one year after kidney transplantation [abstract no: 1276]. American Journal of Transplantation 2003;3(Suppl 5):479. [CENTRAL: CN‐00447778]
    1. Gelder T, Kuiper P, Besouw NM, Mast B, Smak Gregoor PJ, Ijzermans JN, et al. Randomised trial comparing conversion of maintenance treatment with ciclosporine and prednisone to azathioprine or mycophenolate mofetil with prednisone one year after kidney transplantation [abstract no: 248]. Transplantation 1998;65(12):S64. [CENTRAL: CN‐00583809]
Touchard 2005 {published data only}
    1. Touchard G, Bridoux F, Etienne I, Toupance O, Lavaud S, Hurault de Ligny B, et al. Efficacy and safety of maintenance neoral monotherapy compared to bitherapy neoral+MMF or neoral+AZA in renal transplantation [abstract no: 1198]. American Journal of Transplantation 2005;5(Suppl 11):462. [CENTRAL: CN‐00793401]
Tsinalis 2000 {published data only}
    1. Tsinalis D, Binet I, Dickenmann M, Steiger J, Brunner F, Thiel G. Cost of medical care after renal transplantation comparing cyclosporine‐mycophenolate to tacrolimus‐azathioprine ‐ a randomised controlled study [abstract]. XVIII International Congress of the Transplantation Society; 2000 Aug 27‐Sep 1; Rome, Italy. 2000.
Vacher‐Coponat 2006 {published data only}
    1. Al‐Massarani G, Vacher‐Coponat H, Paul P, Widemann A, Arnaud L, Loundou A, et al. Impact of immunosuppressive treatment on endothelial biomarkers after kidney transplantation. American Journal of Transplantation 2008;8(11):2360‐7. [MEDLINE: ] - PubMed
    1. Legris T, Picard C, Moal V, Burtey S, Loundou A, Purgus R, et al. Humoral immunity after kidney transplantation: impact of two randomized immunosuppressive protocols. Annals of Transplantation 2013;18:622‐34. [MEDLINE: ] - PubMed
    1. Vacher‐Coponat H, Brunet C, Moal V, Loundou A, Bonnet E, Lyonnet L, et al. Tacrolimus/mycophenolate mofetil improved natural killer lymphocyte reconstitution one year after kidney transplant by reference to cyclosporine/azathioprine. Transplantation 2006;82(4):558‐66. [MEDLINE: ] - PubMed
    1. Vacher‐Coponat H, Indreies M, Moal V, Purgus R, Moussi JF, Dussol B, et al. Cost effectiveness comparison for two immunosuppressive regimens in kidney transplantation [abstract no: 1634]. Transplantation 2008;86(2 Suppl):541. [CENTRAL: CN‐00679019]
    1. Vacher‐Coponat H, Moal V, Indreies M, Purgus R, Loundou A, Burtey S, et al. A randomized trial with steroids and antithymocyte globulins comparing cyclosporine/azathioprine versus tacrolimus/mycophenolate mofetil (CATM2) in renal transplantation. Transplantation 2012;93(4):437‐43. [MEDLINE: ] - PubMed
van der Mast 2000 {published data only}
    1. Mast BJ, Besouw NM, Kuiper P, Vaessen LM, Ijzermans JN, Gelder T, et al. A longitudinal study of TGF‐beta1 protein levels in renal allograft recipients converted from CsA to MMF or AZA. Clinical Transplantation 2000;14(1):66‐9. [MEDLINE: ] - PubMed
Vanrenterghem 1998 {published data only}
    1. Forsythe J. Tacrolimus and mycophenolate mofetil in cadaveric renal transplant recipients. The European Multicentre Tacrolimus/MMF Study Group. Transplantation Proceedings 1999;31(7A):69S‐71S. [MEDLINE: ] - PubMed
    1. Morales JM, Andres A, Morales E, Herrero JC, Cubas A, Praga M, et al. Tacrolimus, mycophenolate mofetil and corticosteroids as primary immunosuppression after renal transplantation at the Hospital 12 de Octubre, Madrid. Transplantation Proceedings 1999;31(7A):75S‐77S. [MEDLINE: ] - PubMed
    1. Squifflet JP, Backman L, Claesson K, Dietl KH, Ekberg H, Forsythe JL, et al. Dose optimization of mycophenolate mofetil when administered with a low dose of tacrolimus in cadaveric renal transplant recipients. Transplantation 2001;72(1):63‐9. [MEDLINE: ] - PubMed
    1. Squifflet JP, Hooff JP, Vanrenterghem Y. The Benelux experience with the combination of tacrolimus and mycophenolate mofetil. Transplantation Proceedings 1999;31(7A):72S‐74S. [MEDLINE: ] - PubMed
    1. Vanrenterghem Y, Squifflet JP, Forsythe J, Heeman U, Backman L, Taube D, et al. Co‐administration of tacrolimus and mycophenolate mofetil in cadaveric renal transplant recipients. Transplantation Proceedings 1998;30(4):1290‐1. [MEDLINE: ] - PubMed
Woeste 2002 {published data only}
    1. 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. Transplantation Proceedings 2002;34(5):1920‐1. [MEDLINE: ] - PubMed
    1. Woeste G, Wullstein C, Pridohl O, Dette K, Bechstein WO. Five year results of a randomized study comparing FK506/MMF and ciclosporin A/azathioprine after simultaneous pancreas and kidney transplantation [abstract]. 5th International Conference on New Trends in Clinical and Experimental Immunosuppression; 2002 Feb 7‐10; Geneva, Switzerland. 2002. [CENTRAL: CN‐00817724]
Wuthrich 2000 {published data only}
    1. Binswanger U, Ambuehl P, Cicvara Muzar S, Knoflach A. Randomized conversion from Mycophenolate to Azathioprine: follow‐up after 2 years. [abstract no: 1592]. A Transplant Odyssey; 2001 Aug 20‐23; Istanbul, Turkey. 2001. [CENTRAL: CN‐00602119]
    1. Inderbitzin M, Muzar SC, Ambuhl PM, Knoflach A, Binswanger U. Randomized conversion from mycophenolate mofetil to azathioprine: follow‐up after 2 years [abstract]. Journal of the American Society of Nephrology 2001;12(Program & Abstracts):896A. [CENTRAL: CN‐00602120]
    1. Wuthrich RP, Cicvara S, Ambuhl PM, Binswanger U. Randomized trial of conversion from mycophenolate mofetil to azathioprine 6 months after renal allograft transplantation. Nephrology Dialysis Transplantation 2000;15(8):1228‐31. [MEDLINE: ] - PubMed

References to studies awaiting assessment

Do 2001a {published data only}
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References to ongoing studies

ATHENA Study 2012 {published data only}
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References to other published versions of this review

Wagner 2009a
    1. Wagner M, Balk EM, Webster AC, Raman G, Trikalinos TA, Schmid CH, et al. Mycophenolic acid versus azathioprine as primary immunosuppression for kidney transplant recipients. Cochrane Database of Systematic Reviews 2009, Issue 2. [DOI: 10.1002/14651858.CD007746] - DOI - PMC - PubMed

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