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Clinical Outcomes Associated With Induction Regimens Among Retransplant Kidney Recipients in the United States

Schold, Jesse1; Poggio, Emilio2; Goldfarb, David2; Kayler, Liise3; Flechner, Stuart2

doi: 10.1097/TP.0000000000000507
Original Clinical Science

Background Numerous studies have evaluated outcomes and risk factors associated with induction protocols among kidney transplant recipients. However, few studies have evaluated outcomes in the subset of retransplant recipients who often have unique immunologic condition and risk profile and represent an increasing proportion of transplant patients in the United States.

Methods We evaluated the association of common induction treatments (alemtuzumab, thymoglobulin, interleukin-2 receptor blockers, and no induction) given at transplantation with clinical outcomes among adult recipients retransplant between 2003 and 2011 using national Scientific Registry of Transplant Recipients data (n = 14,336). We used a propensity score analysis to minimize potential selection biases for allocation of treatment.

Results In adjusted models, there were no significant differences between induction groups for outcomes of delayed graft function, 1-year acute rejection, 1-year BK virus or patient death. Acute rejection before hospital discharge was lowest among patients treated with thymoglobulin and alemtuzumab. The no induction group had the highest average 1-year estimated glomerular filtration rate (62 mL/min/1.73kg/m2) and lowest incidence of any malignancies within 1 year (1.0%). Hospitalizations after transplantation were highest among patients treated with thymoglobulin (42% at 1 year). Recipients with alemtuzumab had the highest relative risk for graft loss (adjusted hazard ratio, 1.19; 95% confidence interval, 1.01–1.40, relative to patients treated with thymoglobulin).

Conclusion There is moderate variation in clinical outcomes associated with induction treatment among retransplant kidney recipients in the United States, including higher graft loss rates among recipients treated with alemtuzumab but similar patient survival between all regimens.

A retrospective US-based re gistry analysis of induction immunosuppression for kidney retransplantation reveals variable but small differences in outcomes. The data do not identify a single preferred algorithm for retransplant induction therapy.

1 Department of Quantitative Health Sciences, Cleveland Clinic, Cleveland, OH.

2 Glickman Urological and Kidney Institute, Cleveland Clinic, Cleveland, OH.

3 Department of Surgery, Montefiore Medical Center, Bronx, NY.

Received 14 February 2014. Revision requested 10 March 2014.

Accepted 17 September 2014.

Funding for this study was provided by Sanofi, Inc. Dr. Schold received support from Sanofi, Inc. to conduct this study. No other authors received support for this study.

The authors declare no conflicts of interest.

The data reported here have been supplied by the Minneapolis Medical Research Foundation as the contractor for the Scientific Registry of Transplant Recipients (SRTR). The interpretation and reporting of these data are the responsibility of the author(s) and in no way should be seen as an official policy of or interpretation by the SRTR or the US Government.

J.S., E.M., D.G., L.K., S.F. participated in research design and writing of the article. J.S. participated in data analysis.

Correspondence: Jesse D. Schold, Ph.D., Department of Quantitative Health Sciences, Cleveland Clinic, 9500 Euclid Avenue, JJN3-01, Cleveland, OH 44195. (

Since 1998, 13% of adult kidney transplants (KTX) performed in the United States were to recipients that had previously received a kidney transplant.1 In 2012, there were 1,930 adult repeat KTX in the United States, representing the largest number of repeat transplants to date.1 Repeat KTXs have significantly lower graft survival relative to primary KTXs but a significant life expectancy benefit relative to maintenance dialysis.2,3 Previous KTXs have significant challenges in access to transplantation and are significantly more likely to be sensitized.4,5 Complications and time to primary graft loss are also associated with outcomes during repeat transplantation.6 Repeat transplant recipients are approximately half as likely to participate in research studies as compared to primary transplant recipients due to explicit exclusion criteria, higher presence of comorbidities or lower interest in research.7 However, it is important to understand factors associated with outcomes in this growing transplant population that are otherwise rarely addressed in research settings.

Use or nonuse of induction therapy and specific induction agents has changed over time and there remains significant variation in use by country, center, and patient condition.8 Several prospective studies have evaluated KTX outcomes associated with induction therapy. A randomized prospective study found a lower incidence of acute rejection among patients treated with thymoglobulin versus no induction, but an increase in adverse events.9 A 12-month randomized trial reported equivocal outcomes for a primary composite endpoint between thymoglobulin and interleukin-2 receptor blocker (IL-2 RB) groups, but reduction in acute rejection in the thymoglobulin-treated group.10 A recent prospective trial found a reduction in acute rejection among patients treated with alemtuzumab compared to those receiving thymoglobulin or basiliximab.11 Interestingly, these results were similar among KTXs defined as higher risk for rejection. Two meta-analyses of prospective trials indicated significant differences in renal function, acute rejection, and other adverse events based on induction, but no differences between types of IL-2 RBs.12,13

Among primary KTXs in the Organ Procurement and Transplantation Network (OPTN)/United Network of Organ Sharing (UNOS) database, significant differences in the incidence of posttransplant lymphoproliferative disorder especially among patients treated with monoclonal antibodies and thymoglobulin have been reported.14,15 Kuo et al.16 reported no association between induction therapy and graft or patient survival among zero-mismatched deceased donor KTXs but significant increases in rejection without induction therapy. Other studies have found differential effects of induction therapy modified by patient risk profile and concomitant therapies.17-20

Limited information exists concerning induction among retransplant kidney recipients. Our aim was to evaluate outcomes associated with induction use among retransplant recipients in the United States. We hypothesize that outcomes associated with type and use of induction may be unique among retransplant recipients given previous treatment and a different immunologic state among this population. Additionally, we sought to describe variability in induction agent use by U.S. center and concomitant maintenance immunosuppression among adult retransplant KTXs.

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Study Population

Among 14,336 adult (age ≥18 years) recipients of repeat KTXs between 2003 and 2011, 18% received no induction, 57% thymoglobulin, 16% IL-2 RB, and 10% alemtuzumab. Transplant characteristics by induction are displayed in Table 1. Patients with IL-2 RB induction were less likely to be highly sensitized or African American. Patients receiving alemtuzumab were more likely to receive expanded criteria and donation after circulatory death kidneys. Recipients with thymoglobulin were less likely to receive living donor kidneys compared to other induction groups. Thymoglobulin was most commonly used with a regimen consisting of tacrolimus and mychophenalate mofetil (Fig. 1). Recipients without induction therapy or those receiving alemtuzumab were less likely to receive maintenance steroids (Fig. 1).





Induction treatment use changed over the study period. In 2003, 50% of the study population received thymoglobulin, 24% no induction, 21% IL-2 RB, and 5% alemtuzumab. In 2011, 63% of recipients received thymoglobulin, 14% no induction, 12% IL-2 RB, and 12% alemtuzumab. There was substantial variation in induction use by individual transplant center. Almost half of centers had less than 5% of retransplant recipients on a no induction regimen, whereas several centers had greater than 90% of patients treated without induction (Fig. 2A). Thymoglobulin was used in at least 80% of retransplants in over one third of the centers, whereas almost 8% of centers used thymoglobulin in less than 1% of patients (Fig. 2B). Over half of centers had less than 5% of retransplants on IL-2 RB induction, whereas approximately 5% of centers had more than half of retransplants treated with an IL-2 RB (Fig. 2C). More than 70% of centers had less than 1% of patients treated with alemtuzumab, whereas several centers used alemtuzumab for induction in at least 75% of recipients (Fig. 2D).



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Propensity Score

On multivariable analysis, use of induction was significantly associated of body mass index, insurance type, human leukocyte antigen matching, panel reactive antibody, dialysis duration, functional status, donor type, steroid use, maintenance immunosuppression type, and transplant center. The concordance index of the model was 0.89. As expected, the estimated probability of treatment without induction was higher for those who actually did not receive induction. The average estimated probability of treatment with no induction based on all factors in the multivariable model was 51% for no induction, 11% for thymoglobulin, 11% for IL-2 RB, and 9% for alemtuzumab.

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Delayed Graft Function

Among deceased donor recipients, delayed graft function (DGF) occurred in 23% (Table 2). DGF was lowest with IL-2 RB induction (21%) and highest with alemtuzumab (27%; P = 0.04). In multivariable models, differences between study groups were not statistically significant (Table 3).





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Acute Rejection

Early acute rejection (between transplantation and hospital discharge) was 3.8%. This proportion was highest without induction (4.8%) and lowest with alemtuzumab (1.3%; P < 0.001, Table 2). Differences in early rejection remained significant in multivariable models, indicating that relative to patients treated with thymoglobulin, patients without induction had 82% greater adjusted likelihood (adjusted odds ratio [AOR], 1.82, 95% confidence interval [95% CI], 1.48–2.25), and patients with IL-2 RB had over twofold likelihood (AOR, 2.40; 95% CI, 1.76–3.28) of early acute rejection (Table 3). Patients receiving alemtuzumab had significantly reduced likelihood of early acute rejection (AOR, 0.45; 95% CI, 0.25–0.81) compared to thymoglobulin. The proportion of patients treated for acute rejection within 1 year was 9.0% and did not significantly differ by induction group in unadjusted (Table 2) or multivariable models (Table 3).

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One-Year Renal Function

The average 1-year serum creatinine level in the study population was 1.44 mg/dL, there were no differences in unadjusted levels by induction group (Table 2). However, in the adjusted models, significantly lower levels were associated with no induction treatment (Table 3). Estimated GFR was similar between groups in unadjusted models, but with adjustment, the no induction group had significantly higher estimated GFR at 12 months (61.5 mL/min/1.73 kg/m2).

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One-Year Malignancy

Malignancy within 1 year of transplantation occurred in 1.24%. This proportion was not significantly different by induction group in unadjusted models (Table 2). However, on multivariable analysis, the highest risk was associated with IL-2 RB relative to patients on thymoglobulin. Patients with no induction had the lowest likelihood of malignancy (AOR, 0.55; 95% CI, 0.33–0.90; Table 3).

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One-Year BK Virus

The overall proportion of patients treated for BK virus (BKV) within 1 year was 3.8%. There were no differences in this proportion between induction groups in unadjusted (Table 2) or multivariable models (P = 0.82, Table 3).

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One-Year Hospitalizations

The proportion of patients hospitalized at 1 year was 39%. This proportion varied significantly by induction group with the highest proportion of patients among patients treated with thymoglobulin (42%, Table 2). In the multivariable model, significant differences persisted. No induction (AOR, 0.79; 95% CI, 0.72–0.86) and alemtuzumab (AOR, 0.77; 95% CI, 0.64–0.92) were associated with lower likelihood of hospitalization relative to thymoglobulin.

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Graft and Patient Survivals

Median follow-up for recipients in the study was 4.0 years. Overall graft survival was significantly different by induction group (Table 2). Five-year graft survival was lowest with alemtuzumab (74.0%) and highest with IL-2 RB (79%). After multivariable adjustment, patients with alemtuzumab had significantly higher hazard for overall graft loss relative to patients treated with thymoglobulin (adjusted hazard ratio [AHR], 1.19; 95% CI, 1.01–1.40, Table 3) but no other statistically significant differences between treatment groups. These results were similar, restricting the study population to deceased donor recipients (AHR, 1.25; 95% CI, 1.03–1.51); however, there were no differences in adjusted graft survival between study groups among living donor recipients including alemtuzumab (AHR, 1.08; 95% CI, 0.78–1.48). There were no significant differences in patient survival in Kaplan-Meier plots or multivariable models between treatment groups.

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Modifying Effect of Induction Use During Primary Transplantation

Of 9,755 patients that were within one of the induction study groups at primary transplantation and the primary transplant occurred after 1987, representing the time period that Scientific Registry of Transplant Recipients (SRTR) data is available, 2,569 (26%) used the same induction therapy during both transplants. This included 83% without induction, 12% IL-2 RB, 18% thymoglobulin, and 8% alemtuzumab. Among patients on thymoglobulin for the retransplant, patients with IL-2RB in the primary transplant had significantly higher 1-year acute rejection rates (12.5% vs. 7.0%, P = 0.01). There were no differences in rates of graft loss, patient survival, DGF, BK virus, hospitalizations, or malignancies. Among patients on IL-2 RB for retransplant, there were higher rates of BK virus for patients that were on thymoglobulin for their primary transplantation (14.3% vs. 5.9%, P = 0.02) but no differences for any of the other endpoints. Adjusted graft survival was similar for patients on the same induction therapy during the repeat transplantation (AHR, 1.01; 95% CI, 0.87–1.18).

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The primary outcomes of the study indicate variations in certain clinical outcomes among adult kidney retransplants associated with use and type of induction. DGF, 1-year acute rejection, and 1-year BKV were not significantly different between patients that did or did not receive induction or between types of induction. Early acute rejection episodes were less common with thymoglobulin and alemtuzumab. Patients without induction had the lowest 1-year serum creatinine levels and malignancy rates. Patients receiving thymoglobulin had the highest likelihood of 1-year hospitalizations, and patients with alemtuzumab had the highest risk of overall graft loss. Patient survival was not significantly different between treatment groups. Cumulatively, the study seems to indicate a different risk profile associated with induction regimens but no evidence of an effect on patient mortality within the median follow-up of 4 years.

Part of the motivation for this study was to evaluate outcomes in a subset of the transplant population often excluded from research studies.7 A retrospective analysis may provide novel insights into the outcomes for this substantial and growing subset of the renal transplant population. Furthermore, given that retransplant recipients may often have unique clinical considerations and are generally at higher risk for complications and graft loss relative to primary transplant recipients, it is possible induction protocols have a differential effect in this group. From a clinical perspective, findings may also inform caregivers how much, if any, weight to place on previous induction use in a repeat transplant setting.

Some outcomes of the study parallel findings depicted in studies evaluating primary transplant recipients. In an UNOS analysis of deceased donor KTX, Sureshkumar et al.20 reported significantly higher risks of graft loss among patients induced with alemtuzumab and IL-2 RB relative to thymoglobulin. Additionally, among higher-risk patients, differences between thymoglobulin and IL-2 RB were no longer evident. Our findings complement these findings because alemtuzumab was associated with higher adjusted risks for graft loss, but among retransplant recipients, differences between IL-2 RB and thymoglobulin were no longer evident. There have been different reported effects of induction on the risk of malignancies, but most studies suggest that use of any induction agent has a numerically higher risk than without induction.14,15,21 The association of induction with malignancies was consistent in the present study, although no differences could be determined between induction type. Most studies indicate a reduced incidence of rejection with the use of induction compared to no induction but effects generally do not translate to differences in graft survival.12,17,22,23 Other studies have also found differences in rejection rates by type of induction, but again, generally, these differences did not lead to differences in graft loss rates.10-12,24 In this study, early rejection rates were lower with thymoglobulin and alemtuzumab, but 1-year rates were similar for all regimens, suggesting that among higher risk KTX, the effects of induction for reducing rejection may only be observed early.

There is mixed evidence regarding the role of specific immunosuppression agents and BKV.25-30 In this population of re-transplant recipients, there were no differences in treatment of BKV with the caveat that treatment may be selective based on other clinical conditions. Findings did indicate significantly better renal function at 1 year among patients without induction treatment, in contrast to findings compiled in a large meta-analysis of prospective trials.13 Although differences in renal function were relatively small in this study and did not translate into differences in graft loss, further investigation of whether the effects of induction treatment on renal function in the retransplant population may be warranted. Consideration of retransplant recipient inclusion in research studies is needed given that they comprise a significant proportion of the transplant population and given their relatively higher event rate, retransplant recipients may help improve evaluation of novel therapeutic agents.31,32

Several limitations should be considered with the interpretation of our results. There is significant potential for selection bias and residual confounding associated with this observational analysis and potential systematic use of therapies for select patients that may impact outcomes. We attempted to minimize bias with use of a propensity score analysis; however, this does not account for factors unavailable in UNOS data.33,34 There is substantial variation in use of induction agent at the transplant center level. As such, some differences could be attributed to the relative experience with each of the induction agents within individual centers or a “learning curve” associated with use of induction in a relative small proportion of patients treated at centers. Despite adjustment for maintenance agents, some effects may be associated with the entire medication regimen rather than induction alone. These data do not include information on dose administration which may significantly modify the effects of specific agents. Information about cause of graft loss may also be associated with use of specific induction protocols and outcomes after transplantation; however, these data are lacking in the UNOS database. Results may only be interpreted as associations and cannot be inferred to delineate a direct cause and effect relationship due to the retrospective observational study design. Finally, some of the outcome variables in this study are subject to both clinical treatment patterns or judgment (e.g., delayed graft function, treatment for BK virus, and acute rejection) and may also represent center-level variation in treatment.35

Induction treatment is associated with variation in clinical outcomes among adult kidney retransplant recipients in the United States. Variations in early acute rejection, renal function and malignancies significantly vary based on induction treatment at the time of transplantation. In addition, overall graft loss rates were higher among patients treated with alemtuzumab, which was evident among deceased but not living donor recipients. There is no evidence of significant variations in long-term patient survival for this population associated with induction treatment. These findings may help to characterize the benefits and risks associated with induction regimens among retransplant recipients and guide future practice for tailoring treatment to individual patients’ clinical profile.

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The study used data from the SRTR. The SRTR data system includes data on all donor, wait-listed candidates, and transplant recipients in the United States, submitted by the members of the OPTN, and has been described elsewhere.36 The Health Resources and Services Administration, U.S. Department of Health and Human Services provides oversight to the activities of the OPTN and SRTR contractors.

The study population consisted of adult re-transplant kidney recipients in the SRTR database. Exclusions were unknown immunosuppression information at the time of transplantation, graft loss before initial discharge, induction agent other than those in the study groups, and less than 7-day follow-up (n = 1662). Study groups were defined based on induction medication coded during the initial hospital stay. Patients were not categorized to a study group based on medications coded as maintenance or treatment for rejection. Transplant and demographic characteristics were compared between groups based on chi-square tests for categorical variables and analysis of variance tests for continuous variables. For 1-year outcomes (acute rejection, serum creatinine, malignancy, BKV and hospitalization), models only included patients with at least 1 year of graft survival based on being at risk for these events, given that no exact date is available for these outcomes in the database. Both acute rejection and BKV were defined as treatment for the events as coded in follow-up forms at 6 months or 1 year. Overall graft survival was defined as the minimum of time to graft failure or patient death.

Multivariable logistic models were used for non–time-dependent dichotomous outcomes. Hosmer-Lemeshow tests were used to evaluate adequate model fit for these models. Cox proportional hazard models were used for time to overall graft loss and patient death. For these models, complementary log-log plots were examined along with martingale residual plots to evaluate the proportional hazard assumption. All multivariate models were adjusted for recipient and donor age, sex, race, recipient body mass index, primary diagnosis, human leukocyte antigen mismatching (during primary and repeat transplantation), panel reactive antibody level (categorized as 0, 1–9, 10–29, 30+), functional status, waiting time on dialysis, year of repeat transplantation, early acute rejection during primary transplant, length of primary transplant graft survival, and maintenance immunosuppression (categorized as tacrolimus and mychophenalate mofetil or other). All models other than for the outcome of delayed graft function were also adjusted for donor type. The model for delayed graft function was limited to deceased donor transplants and was additionally adjusted for donor cause of death, hypertension, diabetes, terminal creatinine, cold ischemia time, donation after circulatory death and expanded criteria status. In addition, we evaluated whether induction treatment during patients primary transplant modified the effects of induction use during the retransplant event.

To help mitigate potential selection bias associated with the use of and type of induction treatment, we used a propensity score analysis for each of the outcome models. We initially created a multivariable logistic model for the outcome of any use of induction (yes or no). We then incorporated the probability for an individual patient to receive induction treatment as an inverse probability treatment weight in each of the outcome models. Probability weights that were considered to be outliers (>99.5th or <0.5th percentile) were excluded. All analyses were conducted using SAS (v.9.2, Cary, NC). The study was approved by the Cleveland Clinic Institutional Review Board.

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