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NDT Advance Access originally published online on July 21, 2006
Nephrology Dialysis Transplantation 2006 21(10):2900-2907; doi:10.1093/ndt/gfl329
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© The Author [2006]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Medical and non-medical determinants of access to renal transplant waiting list in a French community-based network of care

Sahar Bayat1, Luc Frimat1,2,, Nathalie Thilly1, Carole Loos1, Serge Briançon1 and Michèle Kessler2

1Department of Epidemiology and 2Department of Nephrology, University Hospital of Nancy, France

Correspondence and offprint requests to: Luc Frimat, Service de néphrologie, Hôpitaux de Brabois, 54500 Vandoeuvre les Nancy, France. Email: l.frimat{at}chu-nancy.fr



   Abstract
Top
 Abstract
Introduction
 Subjects and methods
 Results
 Discussion
 Research support,...
 References
 
Background. Evaluation of adult candidates for kidney transplantation diverges from one centre to another. Concurrently, ethnic background, female gender, late referral to a nephrologist, distance from transplantation department and private ownership of a dialysis facility have been associated with poor access to kidney transplantation. We assessed determinants of access to a waiting list in a French community-based network of care.

Methods. From July 1997 to June 2003, 1725 adults living in Lorraine, who started renal replacement therapy in one of the 13 facilities of the network, were included. We compared, first, the patients registered on the waiting list with those not registered and, second, the patients registered before starting dialysis with those registered after.

Results. Using logistic regression, registration on the waiting list was exclusively associated with age and medical factors, except for one variable: medical follow-up in the department performing transplantation [odds ratio (OR): 1.67 (95%CI: 1.05–2.67)]. Registration before starting dialysis was not associated with medical factors but with age [OR of patients younger than 45 years vs those older than 65 years: 3.85 (95%CI: 1.05–24.92)] and medical follow-up in the department performing transplantation [OR: 3.56 (95%CI: 1.98–6.67)].

Conclusions. In a French community-based network, patients followed by the nephrology department performing transplantation are more likely to be registered on the transplant waiting list early in the course of chronic kidney disease. Age over 55 per se is a considerable barrier to access to kidney transplantation. Medical guidelines should allow a standardization of criteria for registration.

Keywords: access to waiting list; kidney transplant; network of care



   Introduction
Top
 Abstract
 Introduction
Subjects and methods
 Results
 Discussion
 Research support,...
 References
 
Incidence and prevalence of end-stage renal disease (ESRD) requiring renal replacement therapy (RRT), i.e. haemodialysis (HD), peritoneal dialysis (PD) or kidney transplantation, are still increasing [1]. Kidney transplantation is associated with longer survival and lower long-term cost [2,3]. Pre-emptive transplantation results in longer allograft survival than transplantation performed after the initiation of dialysis, especially when living-donor kidneys are used [4]. But, given the graft shortage, transplantation with a cadaveric-donor kidney before start of RRT is not commonly achievable. On the other hand, all patients are not equally suited for transplantation, and there is a body of evidence showing that selection criteria of the potential transplant recipient diverges from one centre to another [5–9].

Ideally, placement on the waiting list should be based solely on medical factors in accordance with medical guidelines. However, previous studies showed that Blacks, Hispanics, women and elderly were less likely to receive a renal transplant in some countries. Moreover, late referral to a nephrologist, distance from transplantation department and private ownership of dialysis facilities have been associated with poor access to kidney transplant waiting lists [10–21].

The network of care––NEPHROLOR––was set up, in the French administrative region Lorraine, to improve quality of care of all patients with chronic kidney disease (CKD). Access to a renal transplant waiting list is one key point to achieve optimal care. Therefore, a population-based study was designed: first, to describe medical and non-medical factors associated with registration on the waiting list and, second, to depict factors linked to registration before start of dialysis. We studied factors associated with placement on the waiting list rather than factors associated with transplantation, as these are partly non-modifiable factors.



   Subjects and methods
Top
 Abstract
 Introduction
 Subjects and methods
Results
 Discussion
 Research support,...
 References
 
Organisation of care for CKD in Lorraine region
Lorraine, one of the 22 administrative regions of metropolitan France, is a region with an urban and rural population reaching 2 306 827 inhabitants, according to the 1999 census [22]. The crude incidence of ESRD was 152.4 per million inhabitants in 2003 [1]. The NEPHROLOR network of care was set up in 2002, combining the nine public, two private not-for-profit and two private for-profit facilities, operating dialysis units in Lorraine. In Lorraine, as in most French regions, renal transplantation is performed within the university nephrology department, which is the only transplant centre of the region. Compared with other French regions, Lorraine has a relatively generous graft supply with a mean waiting time between placement on the waiting list and transplantation of 9.6 months in 2004.

Figure 1 depicts the process of the nephrology referral and planning process of RRT in the NEPHROLOR network. Firstly, the family physician refers a patient to a nephrology facility for CKD. Secondly, the nephrologist decides whether or not to refer the ESRD patient to a transplant department performing kidney transplantation. This step is skipped for patients living in the neighbourhood of the university nephrology department. About 30% of patients are evaluated for dialysis and kidney transplantation concurrently while 70% are prepared only for haemodialysis and/or peritoneal dialysis [23]. In Lorraine, direct access through self-referral to the transplant department is possible but very rare. Finally, a patient with a favourable evaluation is registered on the national waiting list, called CRISTAL, of the Agence de Biomédecine, the French national agency of organ transplantation. This step is mandatory to receive a transplant either from a living or a cadaveric donor.


Figure 1
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  		Fig. 1. The process of the nephrology referral and planning of RRT for patients with CKD in the NEPHROLOR network. Evaluation of a potential transplant recipient could start at three different moments during the course of CKD: very early referral to a nephrologist with early registration before starting dialysis and possible pre-emptive transplantation (arrow 1), concurrent evaluation for planned dialysis and registration (arrow 2) and late referral with dialysis start in an emergency setting and possible evaluation for transplantation a second time (arrow 3).

 
Depending on practice patterns, a potential transplant recipient can undergo transplantation evaluation at three different time points in the course of CKD. Some patients referred very early to a nephrologist can benefit from early registration before starting dialysis and, by chance, from a pre-emptive transplantation (Figure 1, arrow 1). Some other patients are concurrently evaluated for planned dialysis and registration (Figure 1, arrow 2). In this case, transplantation occurs after start of dialysis. The remainder of patients start unplanned dialysis and possibly benefit from a transplant evaluation when they are on dialysis (Figure 1, arrow 3). To perform an exact evaluation of this process of care, we decided to focus on all ESRD patients even if they had been registered before start of dialysis.

Study population
Since June 1997, all adult patients living in Lorraine and starting RRT (dialysis or pre-emptive transplantation) in a NEPHROLOR facility were progressively registered in a regional database [1,10]. For the present study, we included all incident patients between 1 July, 1997 and 30 June, 2003. In order to identify all ESRD patients living in Lorraine and placed on the waiting list, the list of patients registered on the French national waiting list between 1 January, 1996 and 31 December, 2004 was extracted from the CRISTAL database and the list of transplanted patients from the database of the transplantation department of Lorraine.

Data collection
For each inclusion of a new patient in the NEPHROLOR database, a standardized form is prospectively filled out at the initiation of RRT [1,10]. Three categories of variables possibly related to registration on the transplant waiting list were studied. The first included social and demographic data: age, sex, current occupation and residence at first RRT. Current occupation was classified in three groups: employed, unemployed and retired. The distance between the patient's residence and the department performing transplantation was calculated in kilometres. In France, legal regulations prohibit considering ethnic differences in the French ESRD registry. However, we know that, in Lorraine, almost all patients were Caucasians, with a significant proportion of natives from Italy, and North Africa. In the French ESRD registry, descriptions about income or education were not available [1].

The second category included clinical, anthropometric and biological data at first RRT: existence of diabetes, cardiovascular disease (coronary artery disease, peripheral vascular disease, congestive heart failure and cerebrovascular disease), respiratory disease, hepatic disease, psychiatric disorder (severe depression or other psychiatric disorder) and past history of malignancy. Patients who were confined to a wheelchair or were bedridden were considered to have physical impairment of ambulation. Body mass index (BMI) was categorized as <20, 20–24.99 and ≥25 kg/m2, haemoglobin as <11 and ≥11 g/dl and serum albumin as <3, 3–3.49 and ≥3.5 g/dl. Blood type was available for patients registered on the waiting list.

The third category included data related to medical follow-up in the NEPHROLOR network: ownership of nephrology facility where the first RRT was performed (public, private not-for-profit or private for profit), date of first RRT, urgent vs planned first dialysis session, type of dialysis (HD or PD), date of registration on the waiting list for registered patients, donor type (cadaveric or living) for transplanted patients. We also took into account the effect of a medical follow-up in the department performing transplantation vs 12 other facilities without transplantation.

Statistical analyses
As the oldest patient registered on the waiting list was 78 years old, we decided to exclude patients older than 80 years on the first day of RRT (13.33%) from statistical analysis.

Impact of baseline characteristics on registration on the waiting list was univariately analysed using the {chi}2 test. Subsequently, all variables univariately significantly associated with registration with P ≤ 0.10 were presented stepwise to a multiple logistic regression model to assess their independent value for registration. Within each step, significant risk factors were selected with a forward strategy using the likelihood ratio statistic, with P = 0.05 on the criterion level of selection. Two variables, age categories and current occupation, were highly correlated. For instance, 100% of the patients over 65 years were retired and so the quantitative risk estimated for each variable might be imprecise in multivariate analysis [24]. Therefore, we decided to exclude the variable current occupation from the multivariate analysis.

Identification of factors associated with registration before start of dialysis was studied in the same way. As the private not-for-profit facilities of NEPHROLOR provide care principally to the patients dialysed at home (PD or HD) or in self-care units and do not follow CKD patients before dialysis onset, the variable ownership of the facility was dichotomized as public vs private for-profit. For patients placed on the waiting list before their first RRT, we did not have biological data at registration date. Thus, serum albumin and haemoglobin were not included in the analyses.

Statistical analyses were performed with SAS software (version 9.1; SAS Institute Inc., Cary, NC, USA).



   Results
Top
 Abstract
 Introduction
 Subjects and methods
 Results
Discussion
 Research support,...
 References
 
Patients’ characteristics
During the study period, 1725 adults started RRT in the NEPHROLOR network. Their mean age was 65.4 ± 15.3 years, 998 (57.9%) were male, 573 (33.2%) had diabetes and 656 (38%) had cardiovascular disease. About 369 (24.7%) of the 1495 patients aged 80 years or younger were registered on the transplant waiting list.

Among patients placed on the list, 69 (18.7%) were registered before their first RRT. Mean age was 41.1 ± 12.6 years. Forty of them (58%) were male. Three (4.3%) had diabetes, three (4.3%) cardiovascular disease, three (4.3%) a past history of malignancy and two (2.9%) physical impairment. Thirty-three (47.8%) underwent pre-emptive transplantation (seven living donors) with a mean delay of 5.4 months between registration on the waiting list and transplantation. The 36 others started dialysis after a mean delay of 5.1 months and 35 underwent transplantation during the study period.

The mean age of the 300 patients registered on the waiting list after their first RRT was 47.7 ± 13.5 years. A total of 180 (60%) of them were male. Forty-five (15%) had diabetes, 38 (12.7%) cardiovascular disease, 16 (5.3%) past history of malignancy and 26 (8.7%) physical impairment. During the study period, 250 underwent transplantation (nine living donors). Nine of them (3%) died while on the waiting list before transplantation.

The mean delay between registration on the waiting list and the day of transplantation did not differ between patients registered before and after start of dialysis, respectively, 10 ± 10.1 and 9.3 ± 9.1 months.

Registration on the transplantation waiting list
Table 1 shows the medical factors associated with registration on the waiting list in univariate analyses. The patients placed on the waiting list were younger than those not registered––46.5 ± 13.6 and 67.8 ± 10.0 years. Except for cirrhosis, all co-morbidities were more frequently observed in the non-registered sub-group. Serum albumin and haemoglobin levels were higher in patients placed on the waiting list, while BMI was lower.


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  		Table 1. Medical factors associated with registration on the waiting list (univariate analyses, n = 1495 patients, age ≤ 80 years)

 
Table 2 shows the effect of non-medical factors on the registration in univariate analyses. Sex and the type of first modality of dialysis were not associated with registration. Patients placed on the waiting list were more likely to be employed. Living in the neighbourhood of the department performing transplantation was not associated with registration. Patients who had a planned first session and whose medical follow-up was done in the department performing transplantation were more likely to be registered. We also looked at the effect of the calendar period of the first RRT, which was not associated with registration.


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  		Table 2. Effect of non-medical factors on registration on the waiting list (univariate analyses, n = 1495 patients, age ≤80 years)

 
Table 3 presents factors associated with registration on the waiting list using a logistic regression model. The younger the patient, the more likely was the registration on the waiting list. For example, compared with a patient older than 65 years, a patient younger than 44 years was 54 times more likely to be placed on the waiting list. Among comorbidities, psychiatric disorders, cardiovascular disease, diabetes, past history of malignancy and physical impairment were independent factors associated with non-registration. Patients with serum albumin greater than 3.5 g/dl were 2.7 times more likely to be placed on the waiting list compared with those having serum albumin less than 3 g/dl. Patients followed in the nephrology department performing transplantation were 67% more likely to be registered.


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  		Table 3. Factors associated with registration on the waiting list (multivariate logistic regression analysis, n = 1495 patients, age ≤80 years)

 
Registration on the waiting list before first RRT
Table 4 presents the factors having an influence on registration before first RRT in univariate analyses. Patients registered before their first RRT were younger and more likely to be employed than those registered after. Sex and distance from a department performing transplantation were not associated with early registration.


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  		Table 4. Effect of medical and non-medical factors on early registration on the waiting list before start of dialysis (univariate analyses, n = 369 patients)

 
Diabetic patients were more frequently placed on the waiting list after dialysis onset. No other comorbidity was associated with early registration. No patient starting RRT in a private for-profit facility was registered before dialysis onset. Early registration rate was higher among individuals followed in the department performing transplantation. Ten percent of the patients registered before dialysis onset, and 3% of the patients registered after starting dialysis had a transplant from a living donor (P = 0.05).

Table 5 presents factors obtained using a logistic regression model associated with early registration on the kidney transplant waiting list. Patients whose medical follow-up was done in the department performing transplantation were four times more likely to be placed on the waiting list before first RRT. Compared with patients older than 65 years, those younger than 44 years were four times more likely to be registered before first RRT.


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  		Table 5. Factors associated with early registration on the waiting list (multivariate logistic regression analysis, n = 369 patients)

 


   Discussion
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
Research support,...
 References
 
Our population-based study suggests that, in Lorraine, access to the transplant waiting list is primarily associated with medical determinants. Differences due to sex, ownership of dialysis facility and distance to transplant centre that have been identified in the US and Scotland, were not found in our French administrative region [11–13,18,19,21]. We did, however, confirm a new non-medical factor associated with registration; i.e. medical follow-up in the department performing transplantation [18].

We used a prospective cohort database that involved 100% of the Lorraine inhabitants starting RRT in the NEPHROLOR network and two independent databases to identify patients registered on the waiting list and patients transplanted. Therefore, our data can be assumed to be highly reliable and complete. We expected to eliminate bias due to selective reporting. Unlike the Scottish evaluation [18], we could take into account all the major comorbidity and pre-emptive renal transplantation.

The present findings confirm previous reports on an inverse correlation between age and registration on the waiting list [11,12,16–18]. Compared with their younger counterparts, patients aged over 65 years were 54 times less likely to be placed on the waiting list. The level of this risk was higher than in previous studies. This difference could be due to differences in study design (inclusion of pre-emptive transplantation in our study) or in population health. Interestingly, when adjusted for comorbidity and serum albumin, age remained strongly associated with registration. This suggests that the chances of being evaluated for registration are significantly lower in older subjects, even if they are in good medical condition. At the same time, older patients had a lesser chance of being placed on the Lorraine waiting list early in the course of their CKD. A similar trend has been reported in the US, where patients who were younger, better educated, White and working full-time were more often placed on the waiting list before dialysis [25].

Comorbidity plays a major role in discriminating the RRT population for evaluation for transplantation. In the present study, presence of a psychiatric disorder strongly and independently limited access to the waiting list. This probably reflects voluntary selection by health professionals, linked with non-compliance. Cardiovascular diseases were independently associated with a decrease in registration rate. Comparing patients without diabetes to those with, the chances of being registered for diabetics were more than 2-fold lower. This confirms a previous French study performed in the Rhône-Alpes region, which demonstrated that diabetic patients were not even evaluated for transplantation [17]. The question can, therefore, be raised as to whether nephrologists too promptly contraindicate kidney transplantation for diabetic patients without comorbidity. In the elderly and diabetics, transplantation is the only treatment that can significantly reduce the ESRD-linked mortality risk [2]. Today, both RRT patients and cadaveric kidney donors are getting older and older. In this way, more and more RRT elderly in good condition could benefit from kidney transplantation. Nevertheless, the question remains open as to whether improved access to the transplant waiting list in favour of this population would penalize the younger population.

In contrast with previous reports from the US and Scotland [11–13,18], sex was not a determinant of access to the waiting list in Lorraine. We hypothesized that men and women are equally selected for registration.

A previous study has shown that lower BMI was independently associated with reduced adjusted rates of registration on the waiting list in the US [26]. In the present study, the univariate analysis (Table 1) shows that the BMI was lower in the patients registered on the list compared with those not registered. However, the multivariate analysis did not confirm this relationship in the NEPHROLOR network.

Previous studies in Scotland [18] and the US [27] suggested that peritoneal dialysis patients were more likely to benefit from transplantation. In the NEPHROLOR network, the dialysis modality was not associated with registration on the waiting list. This confirms results of a national French study of access to transplantation according to modality [28].

In the present study, there was no relationship between geographic factors and the process of registration. Access to the transplantation waiting list was equivalent wherever the patient lived in Lorraine. In addition, the type of ownership of the facility is not associated with placement on the waiting list. Nevertheless, the univariate analysis (Table 4) shows that patients followed in a for-profit facility were not evaluated before start of dialysis. This point was not confirmed in the multivariate analysis. As the ESRD patients starting dialysis in for-profit facilities are very old (mean age 65.56 years), we assumed that the related nephrologists select patients for registration, as do those in other facilities. Finally, contrary to what has been reported in the US [21], in the NEPHROLOR network, patients have the same chance of being registered whatever the ownership of the healthcare facility.

Due to the lack of data, we did not assess impact of referral. Emergency first dialysis is strongly associated with timing of referral, and could be a surrogate indicator of late referral or sub-optimal pre-ESRD care [10]. It was associated with a lower probability of waiting-list placement in univariate analysis. But, as this variable was not retained in the multivariate analysis, it would most likely be directly linked with other variables that impact the evaluation for registration, i.e. diabetes, cardiovascular diseases and nutritional status.

As in the Scotland study [18], our analysis showed a significant centre effect, with patients having a 67% better chance of registration if they were followed up in the department performing transplantation. This could mean that indications and contraindications were more accurately evaluated by nephrologists who care for transplant patients daily. A recent European comparison of access to waiting lists showed that, adjusted for age, sex, year of start of RRT and comorbidity, the relative risk to receive a transplant ranged from 0.23 for Lombardy to 3.86 for Norway [29]. Respective graft shortage could not be the unique explanation. This difference is certainly a sign of considerable variations in transplant indications across borders. European recommendations for evaluation exist [5] but are not applied. Moreover, the moment when the evaluation should start is not detailed. Correlated with early referral, early information on transplantation delivered concurrently with information on dialysis may lead to an early pre-transplant evaluation and placement on the waiting list before dialysis onset, according to patient preference. This is particularly crucial for employed patients for whom dialysis may lead to job loss.

Our study has limitations. Although data were gathered prospectively, the study design was retrospective. The process of registration is time-dependent, as patients are listed at different time points while some may die prior to listing. So, a Cox regression analysis would be more appropriate for this type of investigation. In our study, as the date of the first visit to a nephrologist was not recorded, we did not have an index date (time 0). Therefore, Cox regression could not be used. Moreover, we wanted to take into account the entire process of registration, including registration before dialysis and pre-emptive transplantation. Therefore, we used a logistic regression. For sensitivity analysis, we used a Cox analysis with the date of the first RRT as the index date, excluding pre-dialysis registration. The results did not change substantially.

In conclusion, non-medical factors like sex or geographical criteria do not limit access to the transplant waiting list in the NEPHROLOR network. After taking into account age and comorbidity, the CKD patients followed up in the nephrology department performing transplantation were more likely to be placed on the waiting list. Moreover, they had a better chance of being listed before their first RRT. Thus, access to the waiting list in the NEPHROLOR network can be improved by encouraging nephrology facilities without transplantation to extend the selection criteria of transplant candidates and to start, if possible, pre-transplant evaluation before dialysis onset. Currently, policies for assignment to the transplant waiting list differ somewhat from centre to centre [7]. Our study would encourage the nephrology community to build valuable check-up guidelines for dialysis patients.



   Research support, acknowledgments
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 Research support,...
References
 
We would like to thank the patients, staff and medical directors of the participating clinics of Lorraine. We would like to thank the French registry REIN (Réseau Epidémiologique et Information on Néphrologie) and the Agence de la Biomédecine for the contribution of data. EPIREL study was supported by a grant from the Hospital Program of Clinical Research (PHRC 1996) of the French Ministry of Health.

Conflict of interest statement. None declared.



   References
Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 Research support,...
 References
 

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Received for publication: 13. 2.06
Accepted in revised form: 9. 5.06


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D. L. Segev, L. M. Kucirka, P. C. Oberai, R. S. Parekh, L. E. Boulware, N. R. Powe, and R. A. Montgomery
Age and Comorbidities Are Effect Modifiers of Gender Disparities in Renal Transplantation
J. Am. Soc. Nephrol., March 1, 2009; 20(3): 621 - 628.
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