Duration of end-stage renal disease and kidney transplant outcome
Alex Goldfarb-Rumyantzev1,
John F. Hurdle1,2,
John Scandling3,
Zhi Wang1,
Bradley Baird1,
Lev Barenbaum4 and
Alfred K. Cheung1,5
1 University of Utah School of Medicine, 2 The Geriatric Research, Education and Clinical Center, Veterans Affairs Salt Lake City Healthcare System, 3 Division of Nephrology, Kidney and Pancreas Transplant Program, Stanford University Medical Center, Stanford, CA, USA 4 RenalService.com, Inc. and 5 Veterans Affairs Salt Lake City Healthcare System, Salt Lake City, UT
Correspondence and offprint requests to: Alexander Goldfarb-Rumyantzev, MD, PhD, Division of Nephrology and Hypertension, University of Utah Health Sciences Center, 85 North Medical Drive, East Rm 201, Salt Lake City, UT 84112, USA. Email: alex.goldfarb{at}hsc.utah.edu
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Abstract
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Background. Patients nearing end-stage renal disease (ESRD) increasingly choose pre-emptive renal transplant (PRT) to avoid pre-transplant dialysis and to minimize ESRD. Compared with long-term dialysis, PRT has been shown to increase allograft survival. However, the merit of short-term dialysis is not well characterized, and it may be the better medical choice in some patients. The goal of the study was to characterize the relationship between the duration of dialysis vs allograft and patient survival.
Methods. We performed a retrospective nationwide cohort study of all kidney transplants (Tx) between January 1, 1990 and December 31, 1999, with a follow-up period through December 31, 2000. Participants were identified using the United States Renal Data System (USRDS), which tracks all ESRD cases in the nation including patients on dialysis and with kidney Tx. Patients with the history of more than one kidney Tx were excluded. Allograft survival and recipient survival were the primary outcomes of this study. Duration of ESRD as a continuous variable as well as divided into categories (14 days, 1560 days, 61180 days, 181365 days, 12 years, 23 years, 35 years and >5 years) was the primary risk factor of interest. Models were adjusted for multiple donor and recipient factors, including demographics and co-morbidities, as well as for Tx procedure characteristics.
Results. A total of 81 130 patient records were used for analysis (age 44.1±14.3 years, 61% males, 24% black, 29% diabetic, pre-transplant ESRD duration 27.1±26.4 months, 26% living donors). ESRD duration, as a continuous variable, is associated with a modest increase in the risk of graft failure over time [hazard ratio (HR) 1.02 per year of ESRD duration, P<0.001]. When ESRD is studied as a categorical variable (duration of 014 days vs longer durations), the increased risk of allograft failure reached statistical significance only when the time on dialysis was
181 days. The duration of ESRD was a significant risk for recipient death (HR 1.04 per year, P<0.001); however, mortality risk reached statistical significance only when the patient had been on dialysis for
1 year.
Conclusions. This study of USRDS records suggests that a short (<6 months) dialysis course has no detrimental effect on graft and patient survival, and should not be deferred if medically indicated.
Keywords: dialysis; duration of ESRD; kidney transplant; pre-emptive transplant; survival; transplant outcome
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Introduction
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According to the United States Renal Data System (USRDS), there are
300 000 patients with end-stage renal disease (ESRD) in this country. By definition, ESRD begins when renal replacement therapy is initiated. Once the kidneys have failed, the patient faces three management options: haemodialysis (HD), peritoneal dialysis (PD) or transplantation. The decision to transplant is made carefully. The surgical procedure itself is taxing on a patient already ill, one probably suffering from co-morbidities such as hypertension or diabetes. As donors are relatively rare, ethical as well as financial considerations come into play with each transplantation procedure.
How long the graft is expected to survive and how long the patient is expected to live are both critical elements in the decision-making process that governs management of ESRD. Factors that predict graft survival have been studied extensively in adults and children [1,2]. Donor and recipient age [3], pre-existing donor hypertension and diabetes [4], non-heart-beating donors [5], prolonged cold storage time [6], re-transplantation [7], multiple blood transfusions [8] and body mass index of the donor and recipient [9] have been demonstrated to play important roles in the post-transplant outcome [1], along with a host of other factors.
Traditionally, ESRD patients would take a course of HD or PD, or both, possibly followed by one or more transplants. Increasingly patients are opting for transplantation as the very first ESRD treatment modality, a choice labelled pre-emptive transplant. Much of the enthusiasm for pre-emptive transplantation stems from reports that they are advantageous for graft and patient survival [1013]. Increased time on dialysis prior to a transplant is a predictor of negative short-term graft outcome [14] and transplant recipient survival [15].
While pre-emptive transplant would appear to have an advantage over traditional therapy, it is unclear if this represents a negative effect intrinsically associated with dialysis or the fact that patients who had a transplant after dialysis generally have a longer history of ESRD or have accumulated more co-morbid conditions. Aside from prolonging the ESRD course, suggested mechanisms that may account for the worsening outcome by exposure to dialysis include: increased rate of acute rejection, delayed graft function, vascular access complications and various immunological mechanisms [13,16].
Our study addresses several factors that confounded earlier comparisons of dialysis duration with pre-emptive transplant. Lead time bias, which occurs because candidates for pre-emptive transplants have better residual kidney function than patients already on dialysis, is a variable rarely accounted for in previous work. Categorical dialysis modelling strategies, where dialysis is modelled as a categorical variable (e.g. the patient was on dialysis or not, or the patient had dialysis for 0175 days, 176365 days, etc.) can obscure subtle or moderate factors influencing outcomes that cannot be resolved when patients are lumped together in a few, large groups. Lastly, socio-economic variables are often ignored in previous studies, even though it has been shown that educational level and ethnicity are predictors of receiving a pre-emptive transplant in the first place [12]. An important question remains: are there subgroups of patients who might have better outcomes if they received short-course dialysis before transplant (e.g. patients with renal failure awaiting transplant, for whom the graft is not yet available or those with overt uraemic complications where dialysis prior to transplant might improve the pre-transplant health status)?
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Subjects and methods
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Data set
Participants were identified using the USRDS, a federally mandated registry that tracks all renal transplant and ESRD cases in the nation. The selection period was January 1, 1990 to December 31, 1999, with a follow-up period lasting through December 31, 2000. Only recipients with no prior history of kidney transplant were selected from the database (n = 81 130). The sample included both paediatric and adult recipients. Records were excluded if they were missing the outcome variables.
Variables
The primary variables of interest included those pertinent to the timing of the transplant that were available in the USRDS database: total duration of the pre-transplant ESRD period (the difference between the date of the first ESRD service and the date of the transplant) and time on the transplant waiting list. To preserve subtle effects that might vary with duration interval, we modelled these as categorical variables, broken down into the relatively fine intervals of 014 days, 1560 days, 61180 days, 181365 days, 12 years, 23 years and 35 years. The covariates of interest included the following.
Recipient variables
These comprised age, gender, race, height, weight, history of hypertension, diabetes, renal replacement therapy (RRT) modality immediately prior to the transplant, predominant RRT modality during the ESRD course (defined as the RRT modality used for >50% of the whole ESRD duration), number of different RRT modalities used during the ESRD course, specific combinations of the RRT modalities during the ESRD course, and education level, primary source of payment and citizenship (as a surrogate of a socio-economic status).
Co-morbidities
To adjust for a patient's co-morbidities, we calculated a co-morbidity score similar to one proposed by Davies et al. [17]. The co-morbidity score used in our study was calculated based on the following co-existing conditions, each of them contributing one point: cardiovascular disease (defined in USRDS as symptomatic cardiovascular disease or proven coronary artery disease with or without angina); symptomatic peripheral vascular disease; diabetes mellitus; and hypertension.
Donor variables
These were: type of donor (cadaveric or living); heartbeating status of donor; age; gender; race; height; weight; citizenship; and number of matched human leukocyte antigens (HLAs).
Transplant procedure variables
These comprised the day of the week the transplant was performed, the year of the transplant and cold storage time.
Outcome measures and definitions
There were two outcomes in this study: graft survival, calculated as the time between the transplant and subsequent allograft failure (or censor); and recipient survival, calculated either as the time between the transplant and subsequent recipient death (or censor), or as the time between ESRD onset and subsequent recipient death (or censor). Both were modelled as continuous variables. Allograft survival was censored at the earliest of the following events: loss to follow-up, patient death or the study completion date, and was analysed as days to graft-failure or censor. Patient survival was censored at the earliest of: loss to follow-up or study completion date, and was analysed as days to recipient death or censor.
The definition of graft failure did not include patient death with a functioning graft, the latter determined in the USRDS as a single binary variable. In cases where the value of this variable was missing and the patient's death date was found to be equal to the graft failure date, we assumed that the patient died with a functioning graft, unless the cause of death specified was coded specifically as one of graft failure or renal failure.
Statistical models
Categorical variables across subgroups were compared using cross-tabulation. Continuous variables were summarized using means and SDs. KaplanMeier graphs were used to display hypothesized relationships and Cox regression models were used to analyse time to event. To avoid colinearity between the primary variables of interest, we analysed them in separate Cox models. To evaluate if the effect of primary variables of interest on the outcome was different between two different RRT modalities, additional KaplanMeier and Cox analyses were performed with stratification by predominant dialysis modality. SAS (SAS Institute, Cary, NC) was used for survival analysis (KaplanMeier and Cox proportional hazards models), while S-Plus (Insightful, Seattle, WA) [18] was used for descriptive statistics, and tree-based modelling for data imputation.
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Results
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Descriptive statistics
The baseline characteristics of the recipients (n = 81 130) and donors are presented in Table 1. Recipients were 44.1±14.3 years old, 60.5% male, 69% White/24% African American, 29% diabetic, 49% hypertensive, and had ESRD an average 2.2±2.2 years prior to transplantation.
Kidney donors were 34.6±15.6 years old, 56% were males, 82% White/11.9% African American and 25.7% living donors.
Multivariate analysis
Duration of ESRD and graft survival
The KaplanMeier plot in Figure 1 shows that graft outcome worsens as the duration of ESRD increases, supporting the results of earlier studies. The Cox models shown in Table 2 also demonstrate a modest overall increase in graft failure as ESRD duration is prolonged, a 2% increase in risk per year overall [hazard ratio (HR), 1.02 per year, P<0.001]. Analysis stratified by the donor type demonstrated the same results for cadaveric and living donors. Time on the transplant waiting list, however, did not show a significant association with the risk of graft failure in the whole patient group (HR 0.99, P = 0.243).

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Fig. 1. Association of ESRD duration with graft survival. Analysis is stratified by the duration of pre-transplant dialysis course: 014 days, 1560 days, 61180 days, 181360 days, 12 years, 23 years, 35 years and >5 years. Increasing pre-transplant ESRD duration was associated with progressively shorter graft survival.
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Table 2. Cox model evaluation of the association between ESRD duration and time on the transplant waiting list vs graft and recipient survivala
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An important pattern in the relationship between short-term ESRD and transplant outcome emerges when pre-transplant ESRD duration is analysed with a fine time granularity (i.e. 014 days, 1560 days, 61180 days, 181365 days, 12 years, 23 years, 35 years and >5 years). A longer course of ESRD was indeed associated with a higher risk of graft failure, although the difference became statistically significant only after 180 days. The HR of graft failure increases from this point in a nearly linear fashion, until ESRD duration reaches 3 years, when there is no further increase (Figure 2). Analysis stratified by the donor type yielded similar results for both cadaveric and living donors. To evaluate a potential difference in the association of ESRD duration with graft outcome between different dialysis modalities, we stratified the Cox model by the predominant dialysis modality (Table 3). We found that the association between ESRD duration and graft survival was similar between HD (HR 1.02 per year, P<0.001) and PD (HR 1.03 per year, P<0.001).

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Fig. 2. Hazard ratio of the graft failure in different categories of the pre-transplant ESRD duration. Compared with the reference (ESRD duration 14 days), the hazard ratio of graft failure became significant only after 180 days of pre-transplant ESRD. The hazard increased from this point in a linear fashion, until the ESRD duration reached 3 years, when there was no further increase in the risk of graft failure.
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Table 3. Cox model evaluation of the association between ESRD duration and time on the transplant waiting list with graft and recipient survivala stratified by the predominant pre-transplant dialysis modality
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Duration of ESRD and recipient survival (calculated from the time of transplant)
The Kaplan Meier plot in Figure 3 shows that a longer duration of ESRD was also associated with poorer recipient survival. In the Cox models, overall recipient survival decreased with increased duration of ESRD for all patients (HR 1.04 per year, P<0.001) as well as recipients of cadaveric (HR 1.04 P<0.001) and living kidneys (HR 1.06 P<0.001) analysed separately. Longer overall duration on the waiting list was also associated with recipient mortality (HR 1.02, P<0.05) (Table 2). When ESRD duration was categorized into finer time blocks, the higher risk of recipient mortality only became significant when ESRD duration reached 1 year (HR 1.35, P<0.05). From that point, the hazard increased linearly (Figure 4). Separate analysis of the cadaveric kidney recipients yielded similar results; in the recipients of a living kidney, the effect of ESRD duration on survival became significant at 181365 days (HR 1.98 P<0.05). When Cox analysis was stratified by the predominant ESRD modality, the overall results were similar between HD (HR 1.04, P<0.001) and PD (HR 1.07, P<0.001) (Table 3).

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Fig. 3. Longer duration of ESRD associated with worse recipient survival. Analysis is stratified by the duration of pre-transplant ESRD course: 014 days, 1560 days, 61180 days, 181360 days, 12 years, 23 years, 35 years and >5 years.
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Fig. 4. Hazard ratio of the recipient mortality in different categories of the pre-transplant ESRD duration. Compared with the reference (ESRD duration 14 days), the hazard ratio of the recipient death became significant only after 1 year of pre-transplant ESRD and from that point increased in a linear fashion.
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Duration of ESRD and recipient survival (calculated from the time of onset of ESRD)
To avoid lead time bias, analysis was also performed with recipient survival calculated from the time of ESRD onset rather than from the time of transplant surgery. KaplanMeier curves are flat for the time that the patient remained on dialysis pre-transplant, since only patients who survived until transplant are evaluated (Figure 5). The curves represent different durations of the follow-up, where the longest duration was in the group which was on pre-transplant dialysis for the longest time. On visual examination, the slopes of the KaplanMeier curves seem to be similar in those patients who received a kidney transplant after
14 days, 1560 days or 61181 days of dialysis. Patients who received the kidney 181365 days after being on dialysis had a faster rate of decline, and those who were on dialysis for more than a year had the fastest rate of graft loss (including those who received a kidney after being on dialysis for >5 years). In the Cox models, when the duration of ESRD and time on the waiting list was analysed as a continuous variable, longer ESRD duration and time on the waiting list was associated with a better recipient survival (HR 0.85 per year, P<0.001, and HR 0.90 per year, P<0.001, respectively) (Table 2). There was no significant advantage in recipient survival with increased duration of ESRD when the latter is analysed as a categorical variable until the ESRD duration reached 3 years and greater. This better outcome was likely to be at least partly attributed to survival bias.

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Fig. 5. Recipient survival from the time of ESRD onset. Analysis is stratified by the duration of pre-transplant ESRD course: 014 days, 1560 days, 61180 days, 181360 days, 12 years, 23 years, 35 years and >5 years. KaplanMeier curves are flat for the time the patient remained on dialysis pre-transplant, since only patients who survived until transplant were evaluated in the study. The slopes of the KaplanMeier curves are similar in those patients who received a kidney transplant after 14 days, 1560 days and 61181 days of ESRD. Patients who received the kidney 181365 days after being on dialysis have a sharper rate of decline, while those who were on dialysis for more than a year had the fastest rate of decline.
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Discussion
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The literature on the association between pre-emptive transplant and ESRD duration vs survival is rich and at times inconsistent. Recent reports have suggested that increased duration of pre-transplant ESRD is associated with poor graft and recipient outcome [14,15]. While pre-emptive transplant without the patient going on dialysis at all has been shown to be advantageous to the graft survival in several studies [10,12,13], some of these studies examined the time on dialysis only as a binary or continuous variable [12,13], assuming a linear relationship between this variable and the outcome. For example, in the study of Kasiske et al., pre-emptive transplantation was associated with a reduced risk of graft failure and patient death [12]. These authors evaluated dialysis exposure only as a binary variable, rather than as a continuous variable, therefore, the association between duration of pre-transplant ESRD and transplant outcome cannot be deduced from the data. Mange et al. [13] examined records of 8481 patients from the USRDS who were or were not dialysed before receiving a kidney transplant from a living donor. Pre-emptive transplant was defined as no exposure to dialysis for any period of time. They demonstrated that pre-emptive transplantation of kidneys from living donors without previous dialysis was associated with longer allograft survival than transplantation performed after the initiation of dialysis. The primary variable of interest was evaluated in the binary format (exposure to dialysis) as well as categorized duration of dialysis with the smallest increment in the duration of dialysis of 0174 days, with an HR of 1.6 compared with pre-emptive transplant.
Meier-Kriesche et al. [10] reported that longer waiting time on dialysis was found to be a significant risk factor for death-censored graft survival and patient death for those subjects with a functioning graft after renal transplantation. However, the smallest category of dialysis duration the authors analysed was 06 months. This particular duration of dialysis worsened graft survival, but has not worsened patient survival. Since their model was not adjusted for socio-economic status and education level, the effects of these potential confounders is not clear.
Previous studies have usually calculated recipient survival from the time of transplant to the time of patient death. This type of analysis may introduce a lead time bias, in which patients with shorter ESRD duration have a starting time advantage; in effect, they are healthier by definition. Additionally, residual kidney function may confound the result of these studies, as those with shorter duration of ESRD are likely to have better preserved kidney function [19].
To address the lead time bias, we also calculated recipient outcome from the time of onset of ESRD, instead of the time of transplant. When the recipient survival was calculated from the time of ESRD onset, the survival had a sharper rate of decline only when the pre-transplant ESRD duration was >180 days. In addition, in our Cox models, the duration of ESRD and time on the waiting list were analysed as continuous variables, and longer duration was associated with a better recipient survival. We recognize that this outcome may potentially be explained by survivor bias, where only those patients with long duration of dialysis who survived to transplant were included in the study. In the present study, the duration of dialysis was analysed as both a continuous and a categorical variable, rather than simply as a binary variable describing pre-emptive vs non-pre-emptive transplant. The 60-day rule (a convention adopted by USRDS that a dialysis modality must continue for at least 60 days in order to be considered stable, therefore dialysis duration for <60 days may not be reflected by the binary variable describing pre-transplant dialysis) was not applied, instead the actual number of days for which the patient was dialysed prior to transplant was analysed.
There are many potentially confounding variables in renal transplant outcome studies, such as socio-economic status, age, race, citizenship and primary payer. Kasiske et al. demonstrated that some of these factors (race, ethnicity and education) are associated with receiving a pre-emptive transplant [12]. In the study by Meier-Kriesche et al. [10], the authors have not adjusted for socio-economic status and education level. In the study by Mange et al. [13], the authors have not adjusted for socio-economic status or education, instead their model was adjusted for race and median household income for the ZIP code of the recipient. We adjusted our Cox models for recipient education level, primary source of payment and citizenship, as a surrogate for differences in the socio-economic status.
Finally, it is unclear from the existing literature if both HD and PD used prior to transplant affect the outcome of the transplant to the same extent. We stratified the Cox models by predominant dialysis modality and demonstrated that the association between duration of dialysis and the graft and recipient survival for patients on HD and PD are essentially the same. This study did not address other factors associated with dialysis prior to transplantation either in a negative (e.g. loss of job) or a positive (e.g. potentially better compliance after exposure to dialysis) way.
We confirmed that a longer duration of ESRD is associated with a worsening graft outcome; however, the association only becomes significant after 6 months of dialysis therapy, and after 3 years no significant change in risk was evident. Similarly, a longer duration of ESRD was also associated with a worsening recipient survival as well when calculated from the time of transplant; however, it only becomes significant after 1 year of ESRD duration.
This retrospective study did not address the mechanism of association described above; however, we speculate that clinically significant accumulation of ESRD-related co-morbidities and loss of residual kidney function occur only after 6 months of exposure to dialysis. The negative effect of dialysis therapy and/or ESRD on the graft survival (but not recipient survival) plateaus at 1 year after initiation of dialysis. That can potentially be explained by the fact that predictors of the graft survival (e.g. oxidative stress, loss of residual renal function, aberrant T, B cell and cytokine production [20]) might be peaking at 1 year. Additional factors affecting recipient survival (e.g. cardiovascular calcification) continue to accumulate after 1 year of dialysis therapy.
Since dialysis for up to 6 months does not appear to affect graft survival adversely, these results suggest that patients who have uraemic symptoms should not defer dialysis while waiting for kidney transplant. While the time on the waiting list is still associated with the graft and recipient outcome, duration of pre-transplant ESRD is a better predictor of the graft and recipient survival.
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Acknowledgments
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We are indebted to Greg Stoddard for his statistical assistance. This study was funded by the Dialysis Research Foundation. The data reported here were originally supplied by the USRDS. The interpretation and reporting of these data are the responsibility of the authors and in no way should be seen as official policy or interpretation of the US government.
Conflict of interest statement. None declared.
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Received for publication: 7. 7.04
Accepted in revised form: 16. 9.04