Centre-specific variation in renal transplant outcomes in Canada

S. Joseph Kim1, Douglas E. Schaubel2, John R. Jeffery3 and Stanley S. A. Fenton1

1 Division of Nephrology, University Health Network, University of Toronto, Toronto, ON, Canada, 2 Department of Biostatistics, School of Public Health, University of Michigan, Ann Arbor, MI, USA and 3 Section of Nephrology, University of Manitoba, Winnipeg, MB, Canada

Correspondence and offprint requests to: Dr Stanley S. A. Fenton, Division of Nephrology, Toronto General Hospital, University Health Network, 200 Elizabeth St, 13th floor, Eaton Wing North, Room 232, Toronto, Ontario, Canada, M5G 2C4. Email: stanley.fenton{at}uhn.on.ca



   Abstract
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Background. The ‘centre effect’ has accounted for significant variation in renal allograft outcomes in the United States and Europe. To determine whether similar variation exists in Canada, we analysed mortality and graft failure (GF) rates among Canadian end-stage renal disease patients who received a renal allograft from 1988 to 1997 (n = 5082) across 20 transplant centres.

Methods. Patients were followed from the date of transplantation to the time of GF and/or death. A Cox proportional hazards model was used to estimate mortality and GF hazard ratios (HRs) adjusted for relevant covariates, including centre volume. Centre-specific HRs were derived by comparing each centre's outcome rates against all others.

Results. Twenty centres were included in the analysis. There was significant centre-specific variation in recipient and transplant characteristics (e.g. age, diabetes mellitus, donor source and centre volume) as well as covariate-adjusted facility-specific outcome rates. Facility-specific HRs for GF (including death with a functioning graft) ranged from 0.51 to 1.77, while mortality HRs (including death beyond GF) showed a similar spread (0.44–1.84). These HRs represent a 3- to 4-fold difference in transplant outcomes among the 20 centres studied. Centres performing less than 200 transplants over the study period were associated with lower graft and patient survival.

Conclusions. These findings demonstrate significant centre-specific variation in the success of renal transplantation in Canada. Further studies are needed to elucidate the causes of this variation, with the goal of developing strategies to minimize the centre effect and ensure the best possible outcomes for all renal transplant recipients.

Keywords: Canada; centre-specific variation; outcome; registry; renal transplantation



   Introduction
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
End-stage renal disease (ESRD) has become an increasingly important public health issue over the last several years. With a rising number of ESRD patients comes an increasing need for greater effectiveness and efficiency in existing treatments for chronic kidney disease. Transplantation has been definitively shown to improve the quality of life and long-term survival of ESRD patients when compared with dialysis [1,2]. At present, however, the demand for organs far exceeds the supply and, thus, strategies to optimize functional graft survival are of utmost importance. Numerous single- and multicentre studies have evaluated the factors that impact on both patient and graft survival. One of these factors, the centre effect, has been shown consistently to be an important determinant of renal allograft outcome.

The centre effect in renal transplantation has been defined as the variation in centre-specific renal allograft outcomes beyond that which can be explained by random variation and adjustments for factors known to impact on these outcomes [3,4]. A number of studies from the United States and Europe have documented the importance of the centre effect as a prognostic factor in renal transplantation [417]. The variability in 1 year graft survival amongst US transplant centres, unexplained by adjustments for case-mix, has been shown to range from 30% to 40% [5,6]. This effect has persisted despite advances in transplantation, which have lead to improvements in short- and long-term graft and patient outcomes [18,19]. In order to determine if similar variation in the outcome of renal transplantation exists in Canada, we analysed centre-specific patient and graft survival rates using a nationwide, patient-specific organ-failure database.



   Subjects and methods
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Data were obtained for patients undergoing renal transplantation between 1 January 1988 and 31 December 1997, from the Canadian Organ Replacement Register (CORR) of the Canadian Institute of Health Information. CORR is a population-based, nationwide organ-failure registry that receives patient data, submitted annually, from each of the 87 renal programmes (dialysis and transplantation) in Canada [20]. Upon initiation of renal replacement therapy (RRT), data recorded on each patient include date of birth, sex, race, province of residence, pre-dialysis comorbid conditions and primary renal diagnosis. In addition, CORR receives annual RRT data from each centre that includes dialytic modality switches, transplantation and graft failures (GF). Information on patient death (date and cause) is reported along with other follow-up data. Beginning in 1988, CORR initiated the collection of pre-dialysis comorbidity data for all incident patients. Data were available on cardiovascular disease (i.e. angina, acute myocardial infarction, pulmonary oedema, stroke and peripheral vascular disease), chronic obstructive pulmonary disease, malignancies and ‘other serious illnesses’ (i.e. diseases that are expected to greatly reduce 5 year patient survival, but which are not easily categorized under the other groupings, e.g. HIV infection).

The study population included Canadian ESRD patients who received a primary, solitary renal transplant between 1 January 1988 and 31 December 1997 (n = 6305). Patients were followed from the date of transplantation to the date of death, GF or 31 December 1997. Only adult patients were studied [i.e. patients aged < 20 years were excluded from the analysis (n = 422)]. Patients from centres at which less than 50 patients were transplanted (during 1988 to 1997) were excluded, in order to avoid imprecise centre-specific hazard ratios (HRs) (n = 8). Patients with missing covariate data were also excluded from the analysis of patient and graft outcomes (n = 793). The final sample size was 5082 patients from 20 different centres.

A switch to dialysis as the primary mode of RRT was considered a GF event. For the regression modelling, each centre was compared with all other centres with respect to the outcomes of interest while adjusting for the aforementioned covariates. The Cox proportional hazards model was used to estimate centre-specific mortality and GF HRs adjusted for age, sex, race, donor source, primary renal diagnosis, calendar period of transplant, time on dialysis, centre volume and comorbidity.

In analyses comparing centre-specific outcomes, the selection of the reference centre is difficult. Since the natural question is how each centre is performing relative to the remaining centres, we chose to fit 20 separate models to estimate the 20 centre-specific HRs. Taking mortality as an example, the HR for a given centre can be interpreted as the covariate-adjusted death rate at that centre, divided by the covariate-adjusted death rate for all remaining centres. The disadvantage of this approach (i.e. fitting separate models) is computation time, compared with an approach which arbitrarily selects one centre as the reference (to which all others are compared) and fits a single model. This disadvantage, which is borne by the computer, is offset by the interpretability of the HRs and, in contrast to the reference-centre approach, pertains to very natural comparisons. All statistical analyses were performed using SAS version 8.2 (SAS Institute, Inc., Cary, NC, USA).



   Results
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Note that in Table 1 and the figures, centre numbers and letters do not have any relationship to each other. For example, Centre 1.1 in Figure 1 and Centre 2.1 in Figure 2 need not represent the same facility. Our objective was to identify significant variation in centre-specific, case-mix-adjusted outcomes, as opposed to singling out facilities with extreme outcome rates.


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Table 1. Centre-specific volumes and selected recipient and donor characteristics of Canadian renal transplant centres, 1988–1997 (n = 5082)

 


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Fig. 1. Adjusted centre-specific GF HRs, 1988–1997. HRs are adjusted for age, sex, race, donor source, primary renal diagnosis, time on dialysis, calendar period of transplant, centre volume and comorbidity.

 


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Fig. 2. Adjusted centre-specific mortality HRs, 1988–1997. HRs are adjusted for age, sex, race, primary renal diagnosis, donor source, time on dialysis, calendar period of transplant, centre volume and comorbidity.

 
Among individual transplant centres, the percentage of patients aged ≥65 years at transplant ranged from 1.1% to 13.8%, while the average across all centres was ~5.9% (Table 1). The proportion with diabetes mellitus as a primary renal disease ranged from 5.5% to 23.9% (national mean: 18.7%). Considerable heterogeneity was also observed in the distribution of centre-specific donor source, with the proportion of living donor organs ranging from 1.3% to 32.0% (national mean: 20.7%). The median number of transplants per centre over the study period was 206 (range: 55–622). Four centres performed less than 100 transplants, while another four performed ≥400 transplants.

Table 2 displays both demographic and clinical characteristics of the study population along with covariate-adjusted HRs for GF and mortality. The majority of the population was under the age of 65, of male sex and of Caucasian race. The most common causes of ESRD were glomerulonephritis and diabetes mellitus. Deceased donors outnumbered living donors by almost 4:1. Approximately 23% of renal transplant recipients had at least one of the specified comorbid conditions at the start of dialysis. Furthermore, a significant effect of dialysis time was ascertained with a 1% and 2% increase in the risk of GF and mortality, respectively, for every month on dialysis prior to transplantation. Age, race and centre-volume effects were evident for mortality and GF rates with younger recipients, Asian recipient race and larger centre-volumes exhibiting more favourable outcomes. Recipients of black race had significantly reduced overall mortality, but GF rates were comparable to Caucasian recipients. Patients with a history of vascular disease (cardiovascular, cerebrovascular and peripheral vascular) were observed to have worse overall outcomes. GF and mortality HRs for patients with prior malignancy were 0.88 and 0.61, respectively, but their confidence intervals (CIs) included 1.00 (i.e. not statistically significant). To examine the effect of changes in the burden of comorbidity on dialysis prior to transplantation, comorbidity-by-waiting-time interaction terms were added to the regression model. These interaction terms were not statistically significant (data not shown), indicating that any misclassification of patients with respect to comorbidity status by the use of pre-dialysis comorbidity data did not importantly impact on the overall results.


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Table 2. Baseline characteristics of transplant population by renal centre and HRs for GF and mortality in Canadian renal transplant recipients, 1988–1997 (n = 5082)

 
Centre-specific GF (including death) and mortality (followed past GF) HRs are presented in Figures 1 and 2, respectively. Covariate-adjusted GF HRs showed wide variation between centres, ranging from 0.51 to 1.77. Among the 20 centres, six had significantly elevated GF HRs [range: 1.26 (95% CI: 1.01–1.57) to 1.77 (95% CI: 1.45–2.17)] while four showed decreased rates of graft loss [range: 0.51 (95% CI: 0.38–0.69) to 0.69 (95% CI: 0.56–0.85)]. In a subanalysis with GF censored at death, the variation in HRs (0.53–1.97) remained appreciable (data not shown). Covariate-adjusted mortality HRs showed a similar variation to GF rates, ranging from 0.44 to 1.84. Six centres had significantly elevated mortality HRs [range: 1.36 (95% CI: 1.01–1.86) to 1.84 (95% CI: 1.29–2.62)] while five showed decreased mortality rates [range: 0.44 (95% CI: 0.24–0.81) to 0.65 (95% CI: 0.48–0.88)]. When death was censored at GF, the spread in HRs (0.44–1.65) persisted (data not shown).

Figure 3 shows fitted graft-survival probabilities for male renal transplant recipients of deceased donor organs, between the ages of 45 and 64 years, with no comorbid conditions, whose primary renal disease was glomerulonephritis and who were transplanted in 1994–1997. Estimated probabilities in Figure 3 are based on a Cox regression model with ‘GF including death with a functioning graft’ as the end-point. One year graft survival probabilities ranged from 81% to 93%, while 3 and 5 year survival probabilities ranged from 70% to 89% and from 59% to 84%, respectively. With respect to patient survival (followed past GF), 1, 3 and 5 year probabilities were in the range 90–98%, 82–96% and 71–93%, respectively (Figure 4). Moreover, for covariate patterns with lower graft and patient survival probabilities (e.g. patients with diabetes), the disparity in outcomes were even greater (data not shown).



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Fig. 3. Fitted graft survival by centre for referent patients. Estimated probabilities are based on a Cox regression model that used ‘GF including death’ as the end-point. Diamond, 1 year fitted graft-survival; triangle, 3 year fitted graft-survival; square, 5 year fitted graft-survival. Referent patient: age 45–64 years, male, Caucasian, primary renal diagnosis of glomerulonephritis, deceased donor, no comorbid conditions, transplant time period 1994–1997.

 


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Fig. 4. Fitted patient survival by centre for referent patients. Estimated probabilities are based on a Cox regression model that used ‘death followed past GF’ as the end-point. Diamond, 1 year fitted graft-survival; triangle, 3 year fitted graft-survival; square, 5 year fitted graft-survival. Referent patient: age 45–64 years, male, Caucasian, primary renal diagnosis of glomerulonephritis, deceased donor, no comorbid conditions, transplant time period 1994–1997.

 


   Discussion
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Our results show significant centre-specific variation in the outcome of renal transplantation in Canada from 1988 to 1997. There appeared to be considerable heterogeneity in transplant activity using centre volume as a surrogate marker. Larger centres (≥200 transplants over the time period studied) showed superior graft and patient outcomes. In addition, the patient characteristics of each centre varied substantially in a number of areas known to impact on transplant outcomes, such as recipient age, proportion of deceased and living donor transplants performed and the percentage of patients with diabetes. Despite adjustment for various known prognostic factors, this variation in transplant outcomes persisted. It also appeared that increasing time from transplantation worked to increase the disparities in centre-specific outcomes (at 1, 3 and 5 years) as projected from the Cox regression model. The variation in transplant outcomes seen in this study is consistent with that seen in the recent transplant literature [1214,16,17,21,22].

In this population, black race was not found to be predictive of GF while overall mortality was found to be lower in these recipients. The latter has been documented in previous reports [23] and a similar race-effect has been noted in the dialysis literature [24]. Although black race has generally predicted worse graft outcomes in other registry analyses, the number of black recipients was relatively small in Canada during 1988 to 1997 and, thus, the HR for GF may be an imprecise estimate of the true effect. A history of malignancy was also found not to be predictive of adverse graft and patient survival. This likely reflects the rigorous selection process that patients undergo prior to wait-listing and, thus, a past history of malignancy in this group may not portend an inferior survivorship.

The centre effect in renal transplantation was first formally described by Opelz et al. [3] based on an analysis of the UCLA Kidney Transplant Registry. They examined first transplants done between January 1969 and December 1973 with a clinical follow-up of ≥3 months. Ninety-five centres that performed more than one deceased donor transplant during this time period and 84 centres that performed more than one living donor transplant were included in the analysis. They found a bell-shaped distribution when graft survival was plotted against centre volume. Smaller transplant centres were more likely, by chance, to have extreme results with a high deviation from the mean. However, no evidence was found in this study to confirm the suspicion that smaller centres displayed a greater frequency of poorer outcomes as compared with larger centres.

Centre volume and transplant outcome has not shown a consistent relationship in subsequent reports [1,68]. More recently, however, Terasaki et al. [9] analysed data from the United Network for Organ Sharing Scientific Renal Transplant Registry between October 1987 and September 1999 to compare results from the larger transplant centres against ‘the rest’ [9]. Larger centres were defined as those performing more than 1000 transplants during the study period. Fourteen out of 254 centres met this criterion and these larger centres were noted to have contributed ~20% of the total number of transplants. The 10 year graft survival rates at larger centres were not > 5% higher than those of other centres. One month graft survival was only modestly higher in larger centres for regrafts and in highly sensitized (PRA > 70%) recipients. Larger centres had a slightly higher graft survival rate when the recipient had type 1 diabetes, when the donor was older than age 60 and when the donor was a spouse. Most of these differences were apparent only 2–3 years after transplantation, causing the authors to speculate that differences in long-term management, or a previously existent historical difference that had recently disappeared, explained the observed phenomenon. Our results suggest that centre volume might independently impact on graft and patient outcomes. Since smaller programmes tend to be more selective with respect to potential donors and recipients, non-adjustment for transplant covariates that were unavailable in the CORR dataset (e.g. delayed graft function, HLA mismatches) likely attenuates the difference seen between smaller and larger centres. Experienced long-term patient management in larger centres may be driving the observed difference. However, confirmation and further evaluation of this association requires additional study.

A multitude of reports have analysed, in great detail, the impact of other factors on the centre-specific variation in renal transplantation outcomes. Most studies appear to support the persistence of the centre effect at 1 year post-transplantation and beyond [1,58,10]. Others have shown that centre effects are most significant within the first year after transplantation and diminish in importance over time [21]. In addition, there appears to be no clear correlation between 1 year graft survival rates and long-term graft half-lives [68]. The centre effect is less pronounced in living donor transplants while being practically non-existent in HLA-identical transplants [5,7,10]. The degree of HLA matching appears to account for some of the variation seen between centres, but is only significant in centres with lower overall 1 year graft survival rates [4,7,1215]. Physician and surgeon experience has been shown to positively impact on patient and graft survival while accounting for a small portion of the observed variation in centre-specific outcomes [16]. Careful and well-organized clinical management, albeit difficult to quantitate, has also been emphasized as an important factor in determining a centre's success in renal transplantation [16,21].

A recent analysis of the renal transplant centre effect in Australia by Briganti et al. [22] highlights the impact of recipient and donor factors on centre-specific variations in graft survival. Through hierarchical modelling, the authors found that no centres performed significantly better or worse than the average experience. Discrepancies between our results and those of Briganti et al. could be due to differences in factors adjusted for, methods of analysis or, perhaps, differences in the countries themselves. In addition, the follow-up in the study by Briganti et al. terminated at 1 year. At this relatively short time post-transplant, true differences in centre-specific patient and graft outcomes might be more difficult to discern.

Some limitations of our study deserve mention. We did not adjust for differences in background mortality rates, which are likely to vary by region throughout the country. Furthermore, registry databases are limited with respect to the breadth and specificity of the information that they can provide [25]. For example, comorbid diseases captured by the database are done so in a dichotomous fashion (absent or present) without mention of disease severity. Other transplant-related factors, such as panel reactive antibodies, donor characteristics (age, sex and cause of death), HLA matching, cold ischaemic time, delayed graft function or acute rejection, were not available in the database. These factors may importantly contribute to the centre-specific differences in transplant outcomes and may reflect both the case-mix and selection criteria of donors and recipients within individual transplant programmes. We also did not have information on immunosuppression protocols or progression of comorbid illnesses. However, it may be inappropriate to adjust for these latter factors even if data were available. Immunosuppression and progression of comorbidities pertain to practice patterns and patient management, respectively. These factors are centre characteristics that we are, in part, attempting to measure.

In summary, based on this analysis of a national organ-failure registry, there appears to be significant variability in centre-specific outcomes in renal transplantation in Canada, which is unexplained by adjustment for a number of covariates that impact on transplant outcome. These findings are in accordance with studies performed in other countries where national registry data are available. In order to elucidate the reasons for this variation, a detailed, prospective, observational, cohort study that incorporates data on comorbid disease severity, donor and recipient factors and practice patterns will be required. Only then can effective interventional strategies be devised and implemented to ensure the best possible transplant outcomes for all ESRD patients.



   Acknowledgments
 
These results were presented in part at the American Society of Nephrology 2000 meeting and the Canadian Society of Nephrology 2001 meeting. The collection and maintenance of CORR data is made possible by the wholehearted collaboration of the 87 renal programmes across Canada. The contribution of the current and past full-time staff assigned to the register at the Canadian Institute for Health Information (formerly the Hospital Medical Records Institute) has also been essential to the success of the register. The Canadian Society of Nephrology, the Canadian Society of Transplantation. The Canadian Association of Transplantation, The Canadian Association of Nephrology Nurses and Technologists and their constituent members, have also made an essential contribution to the register since its inception in 1981. CORR is wholly supported by grants from the Federal, Provincial and Territorial Ministries of Health through the Canadian Institution of Health Information Budget.

Conflict of interest statement. None declared.



   References
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 

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Received for publication: 12.10.03
Accepted in revised form: 3. 3.04





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