American Journal of Transplantation 2015; 15: 1061–1067 Wiley Periodicals Inc.

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Copyright 2015 The American Society of Transplantation and the American Society of Transplant Surgeons doi: 10.1111/ajt.13097

Socioeconomic Status and Ethnicity of Deceased Donor Kidney Recipients Compared to Their Donors J. T. Adler1,2, J. A. Hyder1,3, N. Elias2,4, L. L. Nguyen1,4,5, J. F. Markmann2,4, F. L. Delmonico2,4 and H. Yeh2,4,* 1

Center for Surgery and Public Health at Brigham and Women’s Hospital, Boston, MA 2 Division of Transplant Surgery, Massachusetts General Hospital, Boston, MA 3 Department of Anesthesiology, Mayo Clinic, Rochester, MN 4 Harvard Medical School, Boston, MA 5 Division of Vascular and Endovascular Surgery, Brigham and Women’s Hospital, Boston, MA  Corresponding author: Heidi Yeh, [email protected]

Public perception and misperceptions of socioeconomic disparities affect the willingness to donate organs. To improve our understanding of the flow of deceased donor kidneys, we analyzed socioeconomic status (SES) and racial/ethnic gradients between donors and recipients. In a retrospective cohort study, traditional demographic and socioeconomic factors, as well as an SES index, were compared in 56,697 deceased kidney donor and recipient pairs transplanted between 2007 and 2012. Kidneys were more likely to be transplanted in recipients of the same racial/ethnic group as the donor (p < 0.001). Kidneys tended to go to recipients of lower SES index (50.5% of the time, p < 0.001), a relationship that remained after adjusting for other available markers of donor organ quality and SES (p < 0.001). Deceased donor kidneys do not appear to be transplanted from donors of lower SES to recipients of higher SES; this information may be useful in counseling potential donors and their families regarding the distribution of their organ gifts. Abbreviations: DSA, donor service area; HRSA, Health Resources and Services Administration; KDRI, kidney donor risk index; MHI, median household income; OPTN, Organ Procurement and Transplantation Network; SES, socioeconomic status; SRTR, Scientific Registry of Transplant Recipients; ZCTA, zip code tabulation area Received 03 July 2014, revised 20 October 2014 and accepted for publication 08 November 2014

Introduction

transplant evaluation, waitlisting and organ receipt (1–3). While many factors contribute to these observed differences, there may also be contributions from challenges in accessing healthcare and physician bias (4–6). Such disparities are concerning in any field of medicine, but they present additional challenges specific to the field of transplantation. Some ethical and legal scholars have suggested that the practice of soliciting deceased organ donation uniformly across ethnicity and SES carries with it the obligation to subsequently provide transplantation itself uniformly across ethnicity and SES (7). This idea is also supported by the Declaration of Istanbul (8). In addition, there are practical implications to the perception and misperception of inequality in deceased donor allocation. Mistrust in the medical system is well documented for non-White ethnic groups (9,10), and multiple studies have shown that lower deceased donor donation rates among Blacks and Hispanics in the United States (11) are, in part, related to distrust of the medical system (12–16). Among potential donors, focus group studies have revealed perceptions that organs only go to ‘‘rich’’ recipients and not to minorities (17). Media coverage of celebrity transplant recipients further drives these perceptions of inequality (18), and this could undermine the motivations of possible donors who may feel that they and their peers have no chance to benefit from organ donation because their gifts would preferentially go to recipients who already enjoy significant advantages (19). Innovative campaigns to improve donation rates (20) could gain valuable momentum from objective data demonstrating that socially disadvantaged groups are not being exploited as deceased donors for the sake of socially advantaged recipients. While these issues are not solely responsible for lower deceased organ donor rates among ethnic minorities, increased transparency of organ distribution may serve to increase donation (16). Thus, we investigated the SES, income and ethnicity of deceased kidney donors, as compared to the recipients who received those kidneys.

Methods Donor and recipient populations

Disparities in kidney transplantation exist based on ethnicity and socioeconomic status (SES) in access to referral,

For this retrospective cohort study, patient demographics and characteristics for all isolated kidney transplants performed in the United States

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Adler et al between January 1, 2007, and December 31, 2012, were obtained from the Scientific Registry of Transplant Recipients (SRTR). The SRTR data system includes data on all donors, wait-listed candidates and transplant recipients in the US, submitted by the members of the Organ Procurement and Transplantation Network (OPTN), and has been described elsewhere. The Health Resources and Services Administration (HRSA), U.S. Department of Health and Human Services provides oversight to the activities of the OPTN and SRTR contractors. This study was approved under an exemption by the Institutional Review Board of Partners HealthCare.

estimate of donor SES. This was intended to find the covariates that confounded the main predictor of interest. Finally, the covariates that failed the initial screen were reintroduced simultaneously. They were each subject to the same criteria as the significant predictors. If these criteria were not met, the covariates were removed. This constituted the end of the purposeful selection process. As it was our primary covariate of interest, we decided a priori to retain donor SES irrespective of P value to evaluate the relationship to recipient SES. Compared to the ethnicity analysis, no further pairs were deleted due to missing covariate data.

Donors and recipients were matched to the single zip code of residence as recorded at the time of donation or transplant. All patients with complete covariate data were included in this analysis: a total of 58 443 deceased donor kidney transplants were performed during this period, of which 1746 (2.9%) were excluded due to invalid or missing zip code data. Further modelspecific exclusions are detailed below.

This approach is intended to create the most parsimonious model possible while including significant predictors and confounding variables. Priority was given to confounding on donor SES. Purposeful selection minimizes the challenges of multiple testing by limiting the comparisons needed to create the model.

Recipients were matched to their donors by organ such that the ‘‘direction’’ of organ transfer applies only to that particular kidney, since the vast majority of donors donate more than one kidney. Organ quality was measured with the kidney donor risk index (KDRI), a combination of donor factors (age, height, weight, ethnicity, history of hypertension, history of diabetes, cause of death, serum creatinine, hepatitis C virus status and donation after circulatory death status) to summarize the quality of donor kidneys relative to other donors (21). Median household income (MHI) by zip code tabulation area (ZCTA), a commonly used indicator of SES based on geography (22), was obtained from the US Census American Community Survey (23).

Statistical analysis Continuous variables were analyzed using Student’s t test when data were normally distributed and Wilcoxon rank-sum test for non-normally distributed data. Categorical variables were tested with Chi square due to large sample sizes. An alpha level of 0.05 was used as criteria for statistical significance. We did not adjust for multiple comparisons in this analysis. All statistical analyses and data linkages were performed using SAS 9.3 (SAS, Cary, NC).

Results Definition of the SES index Utilization of the SES index was based on prior work in solid organ transplantation (24) according to an index derived in the Medicare population by the Agency for Health Research and Quality (22). Briefly, this creates a normalized (to a mean of 50, but without a standard deviation as originally created by the AHRQ) score from zip code level data based on unemployment, poverty, MHI, property values, education and crowded housing. United States Census data from 2010 was utilized to construct the SES index for each zip code crosswalked from the ZCTAs. The zip codes were then weighted by population and divided into even quintiles to compare to the general population of the United State. An SES index was assigned to all available donor and recipient zip codes for further analysis. This provided a more robust assessment of SES than income alone, because single measures such as MHI do not always accurately reflect overall SES (25).

Organ flow: Analytic methods In addition to describing the characteristics of the donor and recipient populations as a group, the directionality of individual organs was calculated by analyzing matched pairs of donors and recipients. For comparison between ethnic groups (as defined in the SRTR dataset), only White, Black, Hispanic and Asian were used. Because the remaining ethnic groups (defined as Other in our analysis) contributed minimally (less than 2% of study population), they were excluded. The SES index and MHI were tested with both the raw numbers (and the associated direction) and by using ZCTA population-weighted quintiles. We then further explored the relationship between donor and recipient SES by building a linear regression model based on purposeful selection as described by Bursac et al (26). The association between recipient SES and other recipient factors was analyzed using purposeful selection. Covariates that had a p value of less than 0.25 were entered into the first linear regression model. If a covariate was not significant at p < 0.10, it was removed from the model if it was also found not to be a confounder of donor SES. Confounding was defined as a greater than 10% change in the effect

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Characteristics of deceased kidney donor and recipient populations There were 56 697 kidney donor and recipient pairs with zip code information for both individuals (Table 1). Donors and recipients were primarily male (59.9% and 60.3%, respectively), but this proportion did not differ between the two groups (p ¼ 0.12). 98.3% of donors and 94.0% of recipients had United States citizenship (p < 0.001). Donors were younger than recipients (38.9  0.07 vs. 52.7  0.06 years [mean  standard error], p < 0.001). Whites represented the largest single ethnicity percentage of both donors and recipients, but donors were more commonly White than recipients were (68.9% vs. 44.7%, p < 0.001). MHI was slightly higher in donors than recipients ($48 678 vs. $48 333, p ¼ 0.02). The mean SES index was also slightly higher in kidney donors compared to recipients (50.5  0.02 vs. 50.3  0.02, p < 0.001). Individual kidney flow by gender and age We measured the flow of kidneys by gender and age to compare the differences between organ donors and recipients (Table 2). Given the known differences between donors and recipients, we would expect that flow would closely match these differences if organs were evenly allocated. This was seen most easily with age, where 76.0% of kidneys went to recipients who were older than their donors (p < 0.001). This was as expected, because donors are typically younger than recipients. Gender was more balanced, and it was not statistically different: where the female to male transfer was 23.4% and the male to American Journal of Transplantation 2015; 15: 1061–1067

SES of Deceased Kidney Donors and Recipients Table 1: Characteristics of deceased donors and transplant recipients Variable Age (years, mean  standard error) Gender (n, %) Male Female Citizenship (n, %) United States Resident alien Non-US citizen Race/ethnicity (n, %) White Black Hispanic Asian Other Median household income (dollars, median [interquartile range]) SES index (mean  standard error)

Donors

Recipients

p Value

38.9  0.07

52.7  0.06

Socioeconomic status and ethnicity of deceased donor kidney recipients compared to their donors.

Public perception and misperceptions of socioeconomic disparities affect the willingness to donate organs. To improve our understanding of the flow of...
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