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Saudi Journal of Kidney Diseases and Transplantation
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ORIGINAL ARTICLE  
Year : 2014  |  Volume : 25  |  Issue : 4  |  Page : 741-749
Steroid maintenance in repeat kidney transplantation: Influence of induction agents on outcomes


Division of Nephrology and Hypertension, Department of Medicine, Allegheny General Hospital, Pittsburgh, PA, USA

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Date of Web Publication24-Jun-2014
 

   Abstract 

The influence of steroid maintenance on the outcomes of repeat kidney transplant (RKT) recipients with respect to induction type is unclear. Using the Organ Procurement and Transplant Network/United Network of Organ Sharing (OPTN/UNOS) database, we identified patients (≥18 years) who underwent deceased donor RKT from January 2000 to December 2008 after receiving induction with rabbit-antithymocyte globulin (r-ATG), alemtuzumab or an IL-2 receptor blocker (IL-2B) and were discharged on a calcineurin inhibitor/mycophenolate mofetil regimen with or without steroids. Of 5634 patients, 3643 received r-ATG (steroid = 3157, no-steroid = 486), 448 alemtuzumab (steroid = 196, no-steroid = 252) and 1543 an IL-2B (steroid = 1465, no-steroid = 78). Unadjusted graft survivals were similar for the no-steroid versus steroid groups for induction with r-ATG [hazard ratio (HR) 0.85 and 95% confidence interval (95% CI) 0.70-1.03, P = 0.10], alemtuzumab (HR 0.76, 95% CI 0.51-1.14, P = 0.18) and IL-2B (HR 0.77, 95% CI 0.56-1.70, P = 0.23). In the adjusted model, steroid use improved graft survival in alem­tuzumab (HR 0.44, 95% CI 0.25-0.76, P = 0.003) but not in the r-ATG (HR 0.86, 95% CI 0.68-1.09, P = 0.21) or IL-2B (HR 0.98, 95% CI 0.56-1.70, P = 0.94) groups. Steroid use was asso­ciated with inferior patient survival in unadjusted (HR 1.30, 95% CI 1.17-1.44, P <0.001) and adjusted (HR 1.29, 95% CI 1.14-1.45, P <0.001) models for r-ATG induction, whereas this was not observed with alemtuzumab (unadjusted HR 1.11, 95% CI 0.89-1.37, P = 0.36; adjusted HR 0.90, 95% CI 0.68-1.20, P = 0.49) or IL-2B (unadjusted HR 1.01, 95% CI 0.87-1.18, P = 0.87; adjusted HR 1.15, 95% CI 0.97-1.38, P = 0.12) inductions. Our study showed a graft survival benefit in the alemtuzumab- and patient death risk in the r-ATG-induced RKT recipients discharged on steroids.

How to cite this article:
Sureshkumar KK, Hussain SM, Nashar K, Marcus RJ. Steroid maintenance in repeat kidney transplantation: Influence of induction agents on outcomes. Saudi J Kidney Dis Transpl 2014;25:741-9

How to cite this URL:
Sureshkumar KK, Hussain SM, Nashar K, Marcus RJ. Steroid maintenance in repeat kidney transplantation: Influence of induction agents on outcomes. Saudi J Kidney Dis Transpl [serial online] 2014 [cited 2020 May 29];25:741-9. Available from: http://www.sjkdt.org/text.asp?2014/25/4/741/134954

Presented in part as a poster at the American Society of Nephrology Kidney Week, November 2011, Philadelphia, PA


   Introduction Top


Despite impressive reductions in acute re­jection (AR) rates and improvement in short-term graft survival, long-term graft survival has not improved correspondingly in renal transplantation. [1],[2],[3] Approximately 50% of grafts fail within 10 years of transplantation. Many patients with failed allografts will undergo re­peat kidney transplantation (RKT). During the last decade, there has been a steady growth in re-listed and RKT patients. As of 2008, in the US, 18% of wait-listed and 13% of kidney transplant patients have received previous transplantation. [4] An analysis of the Canadian Organ Replacement Register has shown a 50% reduction in mortality for patients who failed their first renal allograft and went on to receive a repeat transplant as compared with conti­nuing dialysis. [5]

Steroid avoidance protocols have been in­creasingly used in recent years in patients undergoing kidney transplantation. RKT reci­pients are generally considered higher immu-nologic risk related to factors such as sensi-tization from prior transplant and transplant nephrectomy. It is intuitive to think that higher degrees of immunosuppression, including in­tensive induction therapy, and maintenance steroids would be beneficial in RKT reci­pients. On the other hand, RKT recipients could be more vulnerable to complications of cumulative immunosuppression that begins with prior transplants. Over the last decade, greater than 70% of kidney transplant reci­pients in the United States have received peri-operative induction therapy. Induction immuno-suppression improved graft and patient out­comes for most organ transplants. [6] The most commonly used induction agents in the recent era can be divided into either depleting or non-depleting. The depleting agents used include either the polyclonal rabbit-antithymocyte glo­bulin (r-ATG) or monoclonal alemtuzumab antibodies. The non-depleting agents used for induction are the interleukin-2 receptor bloc-kers (IL-2B, either basiliximab or daclizu-mab). The marketing authorization of daclizu-mab was withdrawn as of January 2009 and the product has been discontinued completely. It is unclear whether there are any graft or patient survival benefits for using maintenance steroids in RKT recipients with respect to the induction agents they received. Using the Organ Procurement and Transplant Network/ United Network of Organ Sharing (OPTN/ UNOS) database, we aimed to evaluate the influence of maintenance steroids on the outcomes of deceased donor RKT recipients stratified by induction type.


   Materials and Methods Top


This study was approved by the Institutional Review Board and was performed in accor­dance with the ethical standards laid down by the Declaration of Helsinki as well as Decla­ration of Istanbul. Using the OPTN/UNOS database, we identified patients ≥18 years who underwent deceased donor RKT between January 1 2000 and December 31 2008 and received induction therapy with r-ATG, alem-tuzumab or an IL-2B agent (basiliximab or daclizumab) and were discharged on a calci-neurin inhibitor (CNI)/mycophenolate mofetil (MMF)-based maintenance immunosuppres-sion regimen with or without steroids. A trans­plant was considered as a RKT if there was a history of previous kidney transplant for the patient in the database. For each induction type, patients were divided into two groups: Those who underwent early steroid withdrawal before the hospital discharge (ESW group) and those who were discharged on steroid mainte­nance. We designated the latter as the chronic steroid maintenance (CSM) group. Patients who received live donor kidney or multi-organ transplants, no induction, more than one induction or induction therapy with a different agent were excluded from the analysis.

Demographic variables for the different in­duction groups were collected. Graft was con­sidered failed when one of the following occurred: Need for maintenance dialysis, re-transplantation or patient death. An intention to treat method was used in the analysis. Graft and patient survivals were compared between the ESW and CSM groups for each induction type before and after adjusting for pre-spe-cified variables. The co-variates known to have an adverse impact on the graft outcome and included in the model were donor-related factors: Age, gender, expanded criteria donor (ECD) kidney, donation after cardiac death (DCD) kidney, death from cerebrovascular accident; recipient-related factors: Age, African American race, diabetes mellitus, dialysis du­ration, peak panel reactive antibody (PRA) titer, number of human leukocyte antigen (HLA) mismatches; and transplant-related fac­tors: Cold ischemia time (CIT), delayed graft function (DGF, defined as the need for dialysis within the first week after transplantation), 12-month AR and transplant year. Treated rejec­tion rates at 12 months post-transplantation were compared for the ESW versus CSM groups stratified by the induction type.


   Statistical Analysis Top


Comparisons among groups were made using the two-tailed t-test for continuous variables and chi square test for categorical variables. Values were expressed as mean ± standard deviation and median with range or percen­tage. When there were missing data for dif­ferent variables/risk factors, we assumed the absence of the risk factor for the purpose of analysis. Less than 2% of the data were mis­sing for different variables (except for treated AR where 20-25% of data were missing) used in the analysis. Both unadjusted (univariate) and adjusted (multivariate, after correcting for the confounding variables listed above) overall graft and patient survivals were calculated and were compared between the CSM versus the ESW groups within each induction type using a Cox regression model. Hazard ratio (HR) and 95% confidence interval (CI) were calcu­lated. A P-value of <0.05 was considered statistically significant. Statistical analysis was performed using SPSS software version 14.


   Results Top


The median follow-up for the entire group was 29.6 months (range 10.7-60.1 months). Trends in the use of induction agents in de­ceased donor RKT recipients from 2000 to 2008 are shown in [Figure 1]A and B. Alemtu-zumab was first used as an induction agent in 2003, with a gradual increase in its use over the subsequent years in the ESW group [Figure 1]A. The use of alemtuzumab was fairly stable from 2003 to 2008 in the CSM group [Figure 1]B. There was a gradual increase in the use of r-ATG in the CSM group with a corresponding decrease in the use of the IL-2 B agent from 2000 to 2008. In the CSM group, roughly 75% received r-ATG, 10% alemtuzumab and 15% an IL-2B agent in the year 2008. During the same year, about 55% of patients received r-ATG induction, 40% alemtuzumab and 5% an IL-B agent in the ESW group.
Figure 1: Trends in the use of induction agents from 2000 to 2008 in the steroid withdrawal (A) and steroid maintenance (B) groups.

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There were a total of 5634 patients who underwent deceased donor RKT during the study period and received induction with r-ATG, alemtuzumab or an IL-2B agent and discharged on a CNI/MMF-based maintenance immunosuppression with or without steroids. Among these patients, 3643 received r-ATG induction (CSM = 3157, ESW = 486), 448 alemtuzumab (CSM = 196, ESW = 252) and 1543 an IL-2 B agent (CSM = 1465, ESW = 78). Demographic characteristics of the CSM versus ESW groups by induction type are shown in [Table 1]. Among the patients who received r-ATG induction, the peak PRA titer was higher, with a higher prevalence of African Americans in the CSM group while in the ESW group, the recipient age was higher with a higher prevalence of ECD kidney use along with longer CIT and higher HLA mis­matches. In the alemtuzumab induction group, recipient diabetes and DCD kidney use was higher in the CSM versus ESW groups. In patients who received an IL-2B induction, peak PRA was higher and more patients were on pre-transplant dialysis in the CSM group, whereas recipient age was higher with in­creased use of DCD kidneys in the ESW group. Almost all patients were on tacrolimus as their CNI agent.
Table 1: Demographic features of patient groups by induction type.

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Graft survival

When compared with ESW, unadjusted graft survivals were similar in the CSM group in patients who received induction with r-ATG (HR 0.85, 95% CI 0.70-1.03, P = 0.10), alemtu-zumab (HR 0.76, 95% CI 0.51-1.14, P = 0.18) and IL-2B agent (HR 0.77, 95% CI 0.56-1.70, P = 0.23). After adjustment for confounding variables, CSM was associated with signifi­cantly improved graft survival compared with ESW in the alemtuzumab group (HR 0.44, 95% CI 0.25-0.76, P = 0.003), but neither in the r-ATG (HR 0.86, 95% CI 0.68-1.09, P = 0.21) nor in the IL-2B (HR 0.98, 95% CI 0.56-1.70, P = 0.94) group [Figure 2]. Factors that emerged as significant predictors of graft failure for each induction type in the multi-variate model are shown in [Table 2]. Only de­layed graft function (DGF consistently pre­dicted adverse graft outcome among all in­duction types.
Figure 2: Adjusted graft survival for maintenance steroid vs. no maintenance steroid groups in patients who received induction with r-ATG (A), alemtuzumab (B) and IL-2B (C).

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Table 2: Predictors of graft failure by induction type.

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Patient survival

In the unadjusted model, patient survival was inferior for the CSM (HR 1.30, 95% CI 1.17- 1.44, P <0.001) compared with the ESW group in patients who received r-ATG induction, and this finding persisted in the adjusted model (HR 1.29, 95% CI 1.14-1.45, P <0.001) [Figure 3]A. Unadjusted patient survivals were similar for the CSM versus ESW groups with alemtu-zumab (HR 1.11, 95% CI 0.89-1.37, P = 0.36) and IL-2B (HR 1.01, 95% CI 0.87-1.18, P = 0.87) inductions. After adjustment for con­founding variables, patient survivals remained similar in the CSM versus ESW groups for both alemtuzumab (HR 0.90, 95% CI 0.68- 1.20, P = 0.49) and IL-2B (HR 1.15, 95% CI 0.97-1.38, P = 0.12) inductions [Figure 3]B and C. Factors that emerged as significant pre­dictors of patient death in the multivariate model stratified by induction type are shown in [Table 3]. Recipient age, DGF, recipient diabetes and pre-transplant dialysis duration strongly predicted patient death for all induc­tion types. Maintenance steroid use was a risk factor for death only in patients who received induction with r-ATG.
Figure 3: Adjusted patient survival for maintenance steroid vs. no maintenance steroid groups in patients who received induction with r-ATG (A), alemtuzumab (B) and IL-2B (C).

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Table 3: Predictors of patient death by induction type.

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Acute rejection Interpretation of data regarding treated rejection was limited due to missing data in up to 20-25% of the transplants. Taking this limi­tation into consideration, the reported treated rejection rates for the CSM versus ESW groups at 12 months were similar in patients who re­ceived induction with r-ATG (10.6% vs. 10.9%, P = 0.85), alemtuzumab (13.3% vs. 10.7%, P = 0.41) and IL-2B agent (10.1% vs. 6.4%, P = 0.29).


   Discussion Top


Our study showed improved graft survival with steroid maintenance versus ESW in de­ceased donor RKT recipients undergoing in­duction therapy with alemtuzumab and dis­charged on a CNI/MMF-based regimen. This benefit was not apparent with r-ATG and IL-2B induction in such patients. Steroid mainte­nance was associated with decreased patient survival in patients who received r-ATG but not alemtuzumab or IL-2 B inductions.

Several studies have looked at the safety and effectiveness of steroid withdrawal in kidney transplantation with promising results. [7],[8],[9],[10] A randomized double-blind trial with five-year follow-up was reported by Woodle et al. [11] In this trial, 191 patients were randomized to ste­roid withdrawal at seven days after transplant and 195 patients to low-dose maintenance ste­roid (5 mg/day after 6 months post-transplant). All patients received induction therapy and were maintained on tacrolimus/MMF. There was an increase in Banff 1A biopsy-confirmed AR in the early steroid withdrawal group but similar patient, graft and death-censored graft survival at five years between the groups. The early steroid withdrawal group had a favorable effect on serum triglycerides, new-onset dia­betes and weight gain. A meta-analysis invol­ving 34 studies and 5637 patients showed in­creased AR risk but similar patient and graft survival with steroid avoidance or withdrawal when compared with maintenance steroids. [12] Cardiovascular risk factors including the inci­dence of hypertension, new-onset diabetes mellitus and hypercholesterolemia were re­duced significantly by steroid avoidance or withdrawal. The 10-year outcome of rapid ste­roid withdrawal involving 1241 adult primary kidney transplants was recently reported from the University of Minnesota. [13] Compared with a historical control group of patients on main­tenance steroids, patient, graft, death-censored graft and AR-free survivals were similar in the live donor (n = 791) and superior in the deceased donor (n = 450) transplant recipients. Rapid steroid withdrawal was associated with favorable effects on complications such as new-onset diabetes mellitus, cataracts, avas-cular necrosis and cytomegalovirus infections. Most of these studies primarily involved first transplant recipients who generally are at lower risk thus limiting their application in repeat transplant recipients. RKT was found to be a risk factor for AR in the group of patients undergoing early steroid withdrawal. [14] Risk for new initiation of steroids in deceased donor kidney transplant recipients initially discharged without maintenance steroids was higher if the patients were receiving RKT. [15] A single-center retrospective analysis showed similar actuarial graft survival at years 1, 2, 3 and 4 between groups of patients who got two kidney trans­plants versus those who received more than two transplants. However, these survival rates were significantly inferior when compared with the patients who received a first trans-plant. [16] A single-center study of 79 high-risk kidney transplant recipients including 22 re-transplants undergoing rapid steroid disconti­nuation showed a three-year actuarial graft and patient survival rates of 94% and 95%, res-pectively. [17] All patients in this study received induction with r-ATG followed by cyclos-porine/MMF maintenance. There has only been one study reported previously that was specifically comparing the outcomes of ESW (n = 59) versus CSM (n = 54) in RKT reci-pients. [18] This single-center retrospective ana­lysis reported similar AR rates as well as excellent and similar five-year graft (88% vs. 84%) and patient (95% vs. 91%) survival rates. Compared with ESW, more patients in the CSM group required lipid-lowering the­rapy along with the need for more antihyper-tensive medications. All patients in this study received r-ATG induction followed by CNI/ MMF maintenance immunosuppression with or without steroids, and one-third of the pa­tients received live donor kidney transplants.

To the best of our knowledge, our study is the first to analyze the influence of the induc­tion type on the outcomes of RKT recipients stratified by steroid maintenance. A graft survival benefit for CSM versus ESW was seen in patients who received alemtuzumab induction but not in those who underwent induction with either r-ATG or IL-2B. The reasons for this observation are not entirely clear. Depleting agent induction, especially with alemtuzumab, can be associated with profound and pro­longed leukopenia, which could drive reduc­tions in the doses or discontinuation of anti-proliferative agents such as MMF that may increase the risk for immune-mediated allo-graft damage. CSM might confer protection in these situations through giving added immuno-suppression and also by enabling the use of MMF as CSM, through its myeloproliferative effect, is typically associated with higher levels of WBC count when compared with ESW. [19] However, there were no significant differences in the treated AR rates at 12 months between the CSM and ESW groups in the alemtuzumab-induced patients. Leuko-penia may also hamper the use of antiviral agents, adding to the risk for infectious com­plications. All these could potentially contri­bute to suboptimal outcomes, particularly in the alemtuzumab-induced group who subse­quently underwent ESW. This point is espe­cially important as more patients who received alemtuzumab induction were discharged on no steroid (n = 252) compared with CSM (n = 192), with the trend increasing over the years. Patient survival was inferior in the CSM versus the ESW groups in patients who under­went r-ATG induction, a finding that was not observed in patients who received induction with either alemtuzumab or the IL-2B agent. Again, the reasons for this finding are not entirely clear. One could speculate that r-ATG induction followed by triple immunosuppres-sion in CSM patients results in enhanced immunosuppression with increased vulnera­bility for infectious and neoplastic compli­cations with adverse patient outcomes. Even though alemtuzumab also is a powerful deple­ting agent, increased patient death was not observed in alemtuzumab-induced patients continued on CSM versus ESW. As mentioned early, a considerable number of patients in the alemtuzumab induced group may not have continued MMF or may be on lower doses of it due to associated leukopenia. This could be attenuating the cumulative immunosuppres-sion and reducing patient complications.

Our study has several limitations. Retros­pective analyses can prove the association but not causation. Despite using an adjusted model, residual confounding factors could exist. Selection bias to different induction agents and steroid maintenance could likely exist due to center-wise differences in practice patterns. Some early steroid withdrawal protocols with­draw steroids at seven days post-transplant. If these patients were discharged from the hos­pital in less than seven days, they would be wrongly categorized as being on steroids. Details on the doses of induction agents were not available, which may have an impact on the outcomes. Changes in maintenance immu-nosuppressive regimen since initial hospital discharge were not captured. This is parti­cularly important as many patients initially discharged on no steroids get restarted on CSM, particularly after rejection episodes. Therapeutic levels of CNI and doses of MMF were not available that could have potentially influenced graft outcomes.

In summary, our analysis of a recent cohort of deceased donor RKT recipients using the OPTN/UNOS registry found a graft survival advantage for the addition of maintenance steroids to a CNI/MMF regimen in those who underwent induction with alemtuzumab but not r-ATG or IL-2B agent. On the other hand, there was an adverse association between patient survival and steroid maintenance in r-ATG-induced patients. The reasons for these observations are not completely understood and needs further studies.


   Acknowledgment Top


This work was supported in part by the Health Resources and Services Administration contract 231-00-0115. The content is the res­ponsibility of the authors alone and does not necessarily reflect the views or policies of the Department of Health and Human Services, nor does mention of trade names, commercial products or organizations imply endorsement by the US Government.

 
   References Top

1.Meier-Kriesche HU, Schold JD, Kaplan B. Long-term renal allograft survival: Have we made significant progress or is it time to rethink our analytic and therapeutic strategies? Am J Transplant 2004;4:1289-95.  Back to cited text no. 1
    
2.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;4:378-83.  Back to cited text no. 2
    
3.Nankivell BJ, Borrows RJ, Fung CL, O'Connell PJ, Allen RD, Chapman JR. The natural history of chronic allograft nephropathy. N Engl J Med 2003;349:2326-33.  Back to cited text no. 3
    
4.2010 Annual Report of the U.S. Organ Procure­ment and Transplantation Network and the Scientific Registry of Transplant Recipients: Transplant data 2004-2009, Rockville, MD, U.S. Department of health and Human Services, Health Resources and Services Administration, Health­care Systems Bureau, Division of Transplantation.  Back to cited text no. 4
    
5.Rao PS, Schaubel DE, Wei G, Fenton SS. Evaluating the survival benefit of kidney retrans-plantation. Transplantation 2006;82:669-74.  Back to cited text no. 5
    
6.Cai J, Terasaki PI. Induction immunosuppression improves long-term graft and patient outcome in organ transplantation: An analysis of United Network for Organ Sharing registry data. Trans­plantation 2010;90:1511-5.  Back to cited text no. 6
    
7.Vincenti F, Schena FP, Paraskevas S, Hauser IA, Walker RG, Grinyo J; FREEDOM Study Group. A randomized, multicenter study of steroid avoidance, early steroid withdrawal or standard steroid therapy in kidney transplant recipients. Am J Transplant 2008;8:307-16.  Back to cited text no. 7
    
8.Kandaswami R, Melancon JK, Dunn T, et al. A prospective randomized trial of steroid-free main­tenance regimens in kidney transplant recipients-an interim analysis. Am J Transplant 2005;5: 1529-36.  Back to cited text no. 8
    
9.Luan FL, Steffick DE, Gadegbeku C, Norman SP, Wolfe R, Ojo AO. Graft and patient survival in kidney transplant recipients selected for de novo steroid-free maintenance immunosuppression. Am J Transplant 2009;9:160-8.  Back to cited text no. 9
    
10.Kaufman DB, Leventhal JR, Axelrod D, Gallon LG, Parker MA, Stuart FP. Alemtuzumab induc­tion and prednisone-free maintenance immuno-therapy in kidney transplantation: Comparison with basiliximab induction-long-term results. Am J Transplant 2005;5:2539-48.  Back to cited text no. 10
    
11.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 multi-center trial comparing early (7 day) corticosteroid cessation versus long-term, low-dose cortico-steroid therapy. Ann Surg 2008;248:564-77.  Back to cited text no. 11
    
12.Knight SR, Morris PJ. Steroid avoidance or withdrawal after renal transplantation increases the risk of acute rejection but decreases cardio­vascular risk. A meta-analysis. Transplantation 2010;89:1-14.  Back to cited text no. 12
[PUBMED]    
13.Rizzari MD, Suszynski TM, Gillingham KJ, et al. Ten-year outcomes after rapid discontinuation of prednisone in adult primary kidney transplan­tation. Clin J Am Soc Nephrol 2012;7:494-503.  Back to cited text no. 13
    
14.Woodle ES, Alloway RR, Buell JF, et al. Multivariate analysis of risk factors for acute rejection in early corticosteroid cessation regimens under modern immunosuppression. Am J Transplant 2005;5:2740-4.  Back to cited text no. 14
    
15.Schold JD, Santos A, Rehman S, Magliocca J, Meier-Kriesche HU. The success of continued steroid avoidance after kidney transplantation in the US. Am J Transplant 2009;9:2768-76.  Back to cited text no. 15
    
16.Ahmed K, Ahmed N, Khan MS, et al. Influence of number of retransplants on renal graft out­come. Transplant Proc 2008;40:1349-52.  Back to cited text no. 16
    
17.Khwaja K, Asolati M, Harmon JV, et al. Rapid discontinuation of prednisone in higher-risk kid­ney transplant recipients. Transplantation 2004; 78:1397-9.  Back to cited text no. 17
    
18.Mujtaba MA, Taber TE, Goggins WC, et al. Early steroid withdrawal in repeat kidney trans­plantation. Clin J Am Soc Nephrol 2011;6:404-11.  Back to cited text no. 18
    
19.Ko TY, Haddy JA, Marcus RJ, et al. Steroid avoidance in renal transplant patients maintained on a cyclosporine-based protocol. Exp Clin Transplant 2007;2:664-9.  Back to cited text no. 19
    

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Correspondence Address:
Kalathil K Sureshkumar
Division of Nephrology and Hypertension, Department of Medicine, Allegheny General Hospital, Pittsburgh, PA 15212
USA
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DOI: 10.4103/1319-2442.134954

PMID: 24969182

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