Neighborhood Poverty and Racial Disparities in Kidney Transplant Waitlisting

RESULTS

Among the 35,346 subjects included in the analysis, the mean age was 61 yr (±15); 20,229 (57%) were black; 17,675 (50%) were men; 6873 (20%) lived in impoverished communities; 15,721 (45%) had diabetes as their primary etiology of ESRD; 25,847 (73%) had two or more comorbidities at the initiation of dialysis; and most had body mass indices >24.9 kg/m² with 9555 (28%) overweight, 8089 (24%) obese, and 1497 (4%) morbidly obese according to World Health Organization guidelines. The median distance from a patient's residence to the nearest transplant center was 48 mi. This was similar to the median distance of 49 mi observed in the source population (i.e., the population from which any exclusion criteria were applied). Six percent of the study population lived in small remote rural areas versus 63% in major urban areas (Table 1).

A greater proportion of black versus white patients lived <20 mi (28 versus 20%) from the nearest transplant center (Table 2). Blacks were younger (58 ± 15 yr versus 64 ± 14 yr) and less likely to have received erythropoietin before the initiation of dialysis (24 versus 29%, P < 0.0001) than white patients (Table 2). In addition, blacks were more likely to live in high poverty areas, with 28% of blacks (versus 9% of whites) residing in areas with >25% of the population living below the poverty line (Figure 1, Table 2).

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Figure 1.

Proportion of incident ESRD patients by neighborhood poverty. Neighborhood poverty was estimated by the proportion of individuals in a census tract residing below the federal poverty line.

A total of 4153 patients (11.8%) were waitlisted and 22,818 were censored by the end of the study period. Of those censored, 9598 (27.2%) transferred out of ESRD Network 6 before the end of the study, 12 (0.03%) were lost to follow-up, and 13,208 (37.4%) died. Patients who were placed on the transplant waiting list were significantly younger than those not waitlisted (47 ± 12 yr versus 63 ± 14 yr, P < 0.0001), and were less likely to have two or more comorbid conditions (52 versus 76%, respectively) (Table 1). Before adjustment, black patients were 13% more likely to be placed on the transplant waiting list than white patients [95% confidence interval (CI): 1.06 to 1.20] (Table 1).

After controlling for demographic and clinical factors, distance from a patient's residence was not associated with time to waitlisting. Compared with patients living <20 mi from the nearest transplant center, the likelihood of waitlisting was not significantly different for patients >20 mi away from the nearest transplant center (Table 3).

Compared with normal weight patients, underweight [hazard ratio (HR): 0.77, 95% CI: 0.62 to 0.96] or morbidly obese patients (HR: 0.63, 95% CI: 0.51 to 0.78) were less likely to be waitlisted, as were those patients 40 yr and older (compared with patients 20 to 39 yr) (Table 3). In addition, female gender (HR: 0.88, 95% CI: 0.82 to 0.96) and the presence of diabetes (HR: 0.78, 95% CI: 0.72 to 0.85) decreased the likelihood of waitlisting.

Hypertension (HR: 1.17, 95% CI: 1.05 to 1.32), overweight compared with normal weight (HR: 1.29, 95% CI: 1.17 to 1.42), erythropoietin use (HR: 1.28, 95% CI: 1.18 to 1.40), and higher mean albumin (HR: 1.06, 95% CI: 1.04 to 1.08) were associated with an increased likelihood of waitlisting (Table 3). The overall P value for trend for distance in our final model was not significant (P = 0.8874), nor was the effect of distance and waitlisting by race (Figure 2).

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Figure 2.

Proportion waitlisted by race and distance to transplant center (miles). Hazard ratios are adjusted for covariates used in final model.

The relationship between race and waitlisting was modified by neighborhood poverty (two-way interaction term for race and neighborhood poverty, P = 0.0009). As neighborhood poverty increased, the likelihood of waitlisting decreased for blacks compared with whites in each poverty category. Compared with patients living in the wealthiest neighborhoods, blacks were 57% less likely than whites to be waitlisted in the poorest communities (Table 4).

We examined the best- and worst-case scenarios of competing risks in a sensitivity analysis that treated all censored patients as if they were waitlisted (model 2) or not waitlisted (model 3). If all of the censored patients were waitlisted, those living >20 mi from the transplant center were significantly less likely to waitlist than those living <20 mi away (P < 0.0001). When we assumed that all censored patients were not waitlisted, our conclusions about the effect of distance on waitlisting did not change; distance did not affect waitlisting (Table 3).

In a sensitivity analysis exploring the effect of distance and waitlisting by age <65 yr versus age ≥65 yr, it was found that including the patients who died or were lost to follow-up did not meaningfully change the HR estimates (results not shown).

DISCUSSION

We found that black patients were less likely than whites to be placed on the kidney transplant waiting list, and this disparity was not associated with the distance to the nearest transplant center. Furthermore, we observed that neighborhood poverty was associated with waitlist placement and we report for the first time that racial disparities differ as neighborhood poverty increases.

Previous studies have reported that patients may have difficulty traveling to transplant centers to complete pretransplant referral and evaluation. In a Scottish cohort, ESRD patients were less likely to be waitlisted if they received dialysis treatment in a facility that did not have a transplant center, but patients living the farthest away (>100 km) were more likely to be waitlisted. In a random sample of Canadian dialysis patients, differences in the likelihood of transplantation occurred between provinces, but not within regions, indicating that proximity to a transplant facility was not predictive of waitlisting.⁹ Rodriguez et al.¹⁰ found that time to transplantation was longer among both black and white incident ESRD patients who lived in zip code areas with ≥75% of black residents. Volkova et al.¹¹ recently reported that increasing poverty was associated with a greater disparity in ESRD incidence rates between blacks and whites. Socioeconomic status (SES) has been suggested as a risk factor for racial disparities in ESRD outcomes; however, there is little evidence to support or explain the association between SES and waitlisting outcomes.^12,13

The few studies that have examined racial differences in waitlisting have shown that racial differences are not entirely explained by patient factors. Limited access to healthcare has been proposed as an explanation; however, as Karter et al.¹⁴ illustrated, racial differences in ESRD incidence are still observed in a fully insured population. In a national study of incident ESRD dialysis patients, Wolfe et al.¹⁵ found differences in waitlisting by race that were not explained by age, sex, ESRD cause, geographic region, or referral practices, but the effect of SES on waitlisting outcomes remains poorly understood.

We found that black patients were less likely to be waitlisted than whites in all neighborhood poverty levels, and that this disparity was most striking in the poorest communities. In areas with 20 to 24.9% of the census tract living below the poverty level, black patients were 58% less likely to be waitlisted than their white counterparts. In communities with >25% of the census tract living below the poverty level, blacks were 57% less likely to be waitlisted than whites (Table 4).

There are likely several explanations for this observed disparity. Race is often a surrogate for several social, behavioral, cultural, and biologic factors, whereas patient ethnicity may influence physician's beliefs about a patient's risky behaviors and likelihood of treatment adherence, resulting in referral bias.^16,17 Additionally, patient preference may play a role: black patients have been shown to be less likely to want a transplant.¹⁸ Exploring the role of these factors in the observed racial differences in waitlisting outcomes is important in developing effective solutions for improving equality in access to healthcare.

This study, to our knowledge, is the first to examine residential distance to the nearest transplant center as a risk factor for kidney transplant waitlisting. This study extends the existing body of literature by incorporating neighborhood poverty as a proxy for SES, noting that poverty explains some of the racial disparities associated with waitlisting. Our study has several strengths. This study population more adequately represents the black ESRD population than prior studies (57% black) versus Wolfe et al. (35% black) and Furth et al. (32% black).^15,19 The data used in this analysis were from a universal, population-based surveillance system from three southeastern states. The ESRD and UNOS data are complete and virtually all cases of waitlist placement in Network 6 were captured, thus the potential for misclassification bias of the outcome is limited.

Our study follow-up was complete (99%) and thus our results cannot be attributed to selection bias. Furthermore, a competing risks analysis was utilized to assess whether censoring due to deaths and loss to follow-up was informative.²⁰ When we examined the best-case scenario that all censored patients were waitlisted, we found that distance could affect waitlisting (P < 0.0001), but there was no trend of dose response (Table 3, model 2). It is extremely unlikely that all censored patients were waitlisted because this would represent 75% of the study population; current reported waitlisting rates are generally between 10 and 15%.⁵ The more likely scenario is that none of the censored patients were waitlisted; results from model 3 assuming censored patients were not waitlisted were consistent with our original model, supporting our conclusion that distance is not associated with kidney transplant waitlisting (Table 3, model 3).

There are several limitations to this research. First, we were unable to ascertain health status at the time of waitlisting and comorbid risk factors may have changed over time. There is also possible misclassification bias of the distance from a patient's residence to the transplant center. The Euclidean distance we used may underestimate the mileage and/or time to a transplant center. In addition, our database did not contain information on the transplant center that each patient attended for their transplant referral appointment, thus we assumed that patients attended the nearest transplant center. We did include transplant facilities in the states surrounding ESRD Network 6 to control for those individuals who may travel outside of their home ESRD network for referral and evaluation at other transplant facilities. Another potential source of misclassification error is self-classification of race.

Although we adjusted for multiple potential confounders, we cannot exclude the possibility of residual confounding. Most importantly, we were unable to control for poverty at an individual level and future studies should aim to gather both individual- and neighborhood-level poverty data. There also may be a variety of unmeasured patient characteristics that precluded waitlisting (e.g., medical nonadherence or patient refusal). Finally, because our analyses were restricted only to Network 6, we may not be able to generalize these findings outside of Georgia, North Carolina, and South Carolina.

Racial disparities in access to kidney transplantation are complex and are likely explained by a combination of patient- and healthcare facility-related factors; however, neighborhood poverty appears to play a strong, previously under-recognized role.^21–27 Although distance was not a significant predictor for placement on the kidney transplant waiting list, to our knowledge this is the first study to show that as neighborhood poverty increases, so does racial disparity in waitlisting, with black patients being 57% less likely than whites to be waitlisted in the poorest communities. Focusing on poor communities may be an effective way to improve fair allocation of kidney organs.

Few studies have examined access to waitlisting for kidney transplantation among patients living farther away from a transplant center, where patients must undergo a required referral and assessment. The results of this analysis show that distance from a patient's residence to the nearest transplant center does not explain the racial variation in placement on the kidney transplant waiting list. This may be interpreted as a relative success for transplant centers, because there appears to be no difference in waitlisting for patients who live far away compared with those who live close to the center. Although distance did not explain these racial disparities, we did find that neighborhood poverty had a large effect on waitlisting outcomes between blacks and whites. These findings suggest that ESRD networks may improve access to kidney transplantation and better address racial inequities by examining more closely the poorer communities within their respective networks.

CONCISE METHODS

DISCLOSURES

The analyses upon which this publication is based were performed under Contract Number 500-96-P704, entitled, “Operation Utilization and Quality Control Peer Review Organization (PRO) for the State of Georgia,” sponsored by the CMS, Department of Health and Human Services. The conclusions and opinions expressed and methods used herein are those of the author; they do not necessarily reflect CMS policy.