From Potential Donor to Actual Donation: Does Socioeconomic Position Affect Living Kidney Donation? A Systematic Review of the Evidence Phillippa Bailey,1,3 Charles Tomson,2 Saira Risdale,2 and Yoav Ben-Shlomo1 Evidence from Europe, Australia and the United States demonstrates that socioeconomically deprived individuals with advanced chronic kidney disease are less likely to receive a living kidney transplant compared with less deprived individuals. This systematic review focuses on how socioeconomic position (SEP) may influence hypothetical and actual living kidney donors and where appropriate, summarizes the quantitative evidence. In the general population, a higher SEP appears to be associated with an increased ‘hypothetical’ willingness to be a living kidney donor but with marked heterogeneity in the absolute differences (I2 = 95.9%, P G 0.001). In a commercial setting, lower SEP motivates people to donate. Outside of this setting, there is no evidence of discordance in the SEP of donors and recipients that would suggest undisclosed financial exchange. There is evidence for a complex interaction between SEP and other variables, such as ethnicity, sex, and the national economic climate. Some evidence suggests that measures to remove financial disincentives to donation are associated with an increase in living donation rates. Future research needs to study how SEP impacts the potential donor population from willingness to donate, progression through donor assessment to actual donor nephrectomy. Keywords: Living kidney donation, Socioeconomic position, Transplantation. (Transplantation 2014;98: 918Y926)


idney transplantation is associated with better survival and quality of life compared with remaining on dialysis (1, 2) with better outcomes for living compared with deceased-donor transplants (3Y5). Prospective live donors are assessed according to national and international guidelines (6Y8). The long-term risks of living donor nephrectomy are very small (9Y11) with evidence of good outcomes in white populations (12Y15). The quality of life of most living donors is at least equal to the general population and returns to predonation levels postdonation (16Y22). In the UK, a country with universal healthcare that is free at the point of access, people from deprived populations

are more likely to have chronic kidney disease (23Y26), more likely to require dialysis (27, 28) but less likely to receive a living kidney transplant (LKT) (29). The same has been demonstrated in the Netherlands (30). Despite universal donor and partial recipient coverage with Medicare, renal patients of lower socioeconomic position (SEP) in the United States have a decreased likelihood of an LKT (31Y33), with evidence that socioeconomic factors explain some of the variation in transplantation rates seen between racial groups (34). In Australia, SEP has been found to be associated with living-donor but not deceased-donor transplant rates, suggesting that SEP may not affect recipient suitability for transplantation (35).

This report is an independent research arising from a Doctoral Research Fellowship (P.B.) supported by the National Institute for Health Research (NIHR). Y.B.S. is the equity theme lead for the NIHR Collaboration for Leadership in Applied Health Research and Care West (CLARHC West) at University Hospitals Bristol NHS Foundation Trust. CLAHRC West is part of the NIHR and is a partnership between University Hospitals Bristol NHS Foundation Trust and the University of Bristol. The views expressed in this publication are those of the authors and not necessarily those of the NHS, the National Institute for Health Research or the Department of Health. The authors declare no conflicts of interest. 1 School of Social and Community Medicine, Canynge Hall, University of Bristol, Bristol, United Kingdom. 2 The Richard Bright Renal Unit, Southmead Hospital, Bristol, United Kingdom. 3 Address correspondence to: Phillippa Bailey, B.A., B.M., B.Ch., M.R.C.P., D.T.M.&H. School of Social and Community Medicine, Canynge Hall, University of Bristol, Bristol, BS8 2PS, United Kingdom. E-mail: [email protected]

P.B. conceived the review and performed the systematic review literature search; analyzed the data and performed the meta-analysis, the data synthesis, and interpretation; wrote the article; and approved the submitted version. C.T. contributed to data synthesis and interpretation, writing of the article, provided feedback on the article, and approved the submitted version. S.R. performed a subset analysis (data extraction and quality assessment) of a random sample of studies for validity, and approved the submitted version. Y.B.S. contributed to data synthesis and interpretation and to the writing of the article, provided feedback on the article and approved the submitted version. Supplemental digital content (SDC) is available for this article. Direct URL citations appear in the printed text, and links to the digital files are provided in the HTML text of this article on the journal’s Web site (www.transplantjournal.com). Received 13 June 2014. Accepted 18 July 2014. Copyright * 2014 by Lippincott Williams & Wilkins ISSN: 0041-1337/14/9809-918 DOI: 10.1097/TP.0000000000000428




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Bailey et al.


Living kidney donation (LKD) is not a single step, but rather a pathway, and therefore SEP may be associated with:

kidney donors, and where appropriate summarizes the quantitative evidence using meta-analytical techniques.

(a) the number of potential donors available to an individual, (b) the attitudes of potential donors and recipients to LKD, (c) the medical suitability of potential donors, (d) the likelihood of a potential donor progressing through donor evaluation, and (e) reasons potential donors do not progress to donor nephrectomy.

Our search results are presented in Figure 1 following the PRISMA guidelines (36). Thirty-three suitable studies (see SDC, http://links.lww.com/TP/B59, study characteristics) were classed into six subgroups for synthesis (Table 1).

Understanding how SEP may influence LKD requires further examination to identify where any ‘‘barriers’’ amenable to intervention may arise. It may then be possible to counter such problems and increase the number of people from deprived areas receiving LKTs. This systematic review focuses on how SEP may influence both hypothetical and actual living


Hypothetical Living Kidney Donors and Attitudes to Donation Twelve cross-sectional studies, from the United States, Europe, Africa, and Asia, examined SEP and individual attitudes to LKD (37Y48). Measures of SEP included education level, income, health insurance, and employment status. Only one study (40) assessed the attitudes of true potential kidney

FIGURE 1. Results of systematic search for articles that have examined the influence of socioeconomic position on living kidney donation.

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Study subgroups and methodological quality assessment Methodological quality assessment

Study subgroup for synthesis

Number of studies

Mean Newcastle-Ottawa Scale score (max 9)



6 5 2 2 4

3 7 7 N/A N/A



(i) Hypothetical living kidney donors and attitudes to donation (ii) Actual living kidney donors in a Commercial setting Noncommercial setting (iii) Interaction of SEP with ethnicity and sex (iv) Secular economic factors and LKD (v) Qualitative studies exploring socioeconomic influences on living kidney donors (vi) Interventions to remove potential socioeconomic disincentives to LKD SEP, socioeconomic position; LKD, living kidney donation.

donors by questioning relatives of individuals requiring a kidney transplant. The remainder examined a subgroup of the general population (e.g., census sample) hence the responses are hypothetical. Nine studies were believed to be similar enough in design and data outputs to undertake a meta-analysis (Fig. 2).

Five studies reported that higher SEP was associated with increased willingness to donate, three found no association and one showed an inverse association. Overall, higher SEP appeared to be associated with an increased reported willingness to donate a kidney to a relative (16%, 95% confidence interval [95% CI] 5%Y27% P = 0.04). However, there was

FIGURE 2. Forest plot of random effects meta-analysis showing the relationship between high socioeconomic position and reported willingness to donate a living kidney stratified by intended recipient. *, the 95% CI using the Wald method is invalid due to the small size of the low SEP group. The true 95% CI is 0.37Y0.96.

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Bailey et al.


marked heterogeneity in the estimates (I2 = 93.6%, P G 0.001), making the pooled estimate nongeneralizable. If this was combined with two studies in which the relationship to the recipient was unstated, we observed an overall pooled estimate for the effect of a higher SEP on reported willingness to donate a kidney to any recipient of 15% (95% CI, 4%Y26% P = 0.08; I2 = 95.9%, P G 0.001). The meta-analysis demonstrates a large degree of heterogeneity, both in effect size and direction, between these studies which have all been designed to assess attitudes to LKD. The summary pooled estimate is therefore of little value other than demonstrating that conclusions are population and question variant specific. As a result, we have removed the overall pooled estimate from the Forest Plot. We repeated the meta-analysis excluding one study of school children (42), who are generally not allowed to be living kidney donors (6). The findings were relatively unchanged (17%, 95% CI 5%Y30%, P = 0.07; I2 = 93.7%, P G 0.001). One of the included studies from the United States (39) found that concern regarding ‘out-of-pocket expenses’ was associated with a decreased expressed willingness to be a living donor, but it was not assessed whether those expressing financial concern had a low SEP. Of the studies not combined in the meta-analysis, one (n = 753) (37) reported no relationship between SEP and reported willingness to donate a living kidney. One abstract (45) assessed attitudes specifically to paired-exchange donation and found no relationship with SEP. The same study population was used to investigate racial variation in attitudes to LKD (48) and socioeconomic variables explained some of the variation observed between racial groups.

payment from recipient to donor is illegal but commonplace (57). Two qualitative studies are discussed later (54, 56). Five studies examined the motivation of primarily LUDs (Fig. 3). The majority of donors reported a financial motivation for donation (50, 51). Four studies (49, 51, 55, 58) assessed the SEP of LUDs, and all found them to be of a low SEP, with the majority living below the poverty line (62%Y70%). Where studied, financial motivation was rarely reported by living-related donors (50).

Actual Living Kidney Donors

Interaction of SEP With Ethnicity and Sex Four studies explored the possibility of SEP explaining the variation in LKD reported with ethnicity and sex (59, 60, 64, 65). As already described, large donor-recipient SEP discordance appears more common in white populations when compared to Hispanics and African-Americans (59, 60). In one study of U.S. national data (64), the incidence of LKD was higher in higher income groups in both

Commercial Organ Donation Eight studies examining commercial living kidney donors and SEP were identified. Four were from Iran (49Y52), which has a compensated and government-regulated living unrelated donor (LUD) renal transplant program (53). Three were from Pakistan, India, and the Philippines (54Y56), where


Non-Commercial Organ Donation Four studies examined the SEP of living kidney donors (59Y62) in the United States, where commercial donation is rare. All studies reported concordance in the SEP of donors and recipients, which may be evidence against unreported payment from recipient to donor, although subtle differences in individual SEP were not examined. Living unrelated pairs were of higher SEP than living related (including spousal) pairs (60, 61). Large donor-recipient SEP discordance appeared more common in white populations when compared to Hispanics and African-Americans (59, 60). A study from the United Kingdom demonstrated that donor-recipient relationships differ at different levels of SEP (63). Spouses or partners comprise a smaller proportion of donors of lower SEP. The adjusted analysis suggested this may be explained by differences in the age of the recipients; spouse or partner donors were significantly older in the higher SEP group compared to those of lower SEP. Greater financial security was postulated as a reason older partners might be more likely to donate.

Motivation of living unrelated kidney donors in the setting of a commercial organ donation.

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African American and white populations. Notably, the total incidence of LKD was higher in the African American population than in the white population, but ratios varied by income. The incidence of LKD was lower in the African American population than that in the white population in the lowest income quintile, but higher in the African American population in the three highest income quintiles. The authors report that their findings point to the higher concentration of African American ESRD patients and their prospective donors in lower-income populations as the major barrier to LKD in this group. Women constitute the majority of living kidney donors internationally (66, 67); one study from Canada (65) has postulated socioeconomic reasons for this sex disparity. This study targeted true ‘‘potential living kidney donors,’’ defined as all first-degree relatives and partners of individuals who had required a renal transplant. Each potential donor was assessed through phone interviews and classed as ‘‘acceptable’’ if there were no medical or immunologic reasons for exclusion. Of the acceptable donors, there appeared to be a significant attrition of employed men but not women, suggesting that employment may be a barrier to donation for the (traditionally) highest earner. Secular Economic Factors and LKD ‘‘Secular’’ is an economic term meaning ‘long-term’. Two abstracts from the United States (68, 69) reported declines in LKD rates correlating with periods of national economic instability. One reported that the attrition in LKD between 2004 and 2008 (69) was independently associated with donor income, with 17% more attrition in those with lower incomes in a fully adjusted analysis. In the other study, overall, fewer individuals donated during periods of greater economic uncertainty, but LUDs (classifying spouses as unrelated) showed the inverse relationship (68). The authors proposed that spousal donor-recipient pairs sharing one economic household may obtain a net financial benefit during economic instability from the transplant by returning a chronically ill recipient to work. These correlations do not equate to causal relationships, and economic problems are suggested as both a barrier and a driver to LKD. Qualitative Studies Exploring Socioeconomic Influences on Living Kidney Donors Two studies (54, 56) explored the motivations and concerns of LUDs in a commercial organ trade setting. The shared themes identified included donor poverty and financial motivation to donation. One single-center study followed potential donors undergoing donor evaluation (70). 24.4% of the original cohort became ‘‘unwilling to donate’’ and reported ‘‘economic stress because of suspension of their job’’ as one reason for this. However, it was not ascertained if those withdrawing with economic concerns were those with a lower SEP. In a pilot qualitative focus-group study (71), intended transplant recipients reported concerns about financial risks to potential donors as a barrier to initiating discussions about donation, although this was not an issue raised by potential donors themselves. As a pilot study, theme saturation was not assessed.


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Interventions to Remove Potential Socioeconomic Disincentives to LKD Two studies assessed the effect of legislation, removing financial disincentives to donation. In Israel (72) the number of LKTs performed before and after the implementation of the ‘‘Organ Transplantation Law’’ in 2008, were compared. The law reduced financial disincentives to LKD by allowing reimbursement of loss of earnings and of the costs generated by donation. Having been relatively stable, the annual number of LKTs rose significantly from 71 in 2010 to 117 in 2011 (P = 0.003). The annual number of patients undergoing kidney transplantation abroad decreased from 155 in 2006 to 35 in 2011 (P = 0.006). The legislation was wide-ranging, including banning reimbursement for transplant tourism, so it is unclear whether the observed effects resulted from the disincentive to travel abroad rather than the removal of perceived financial disincentives to donation per se. In the United States (73), a series of cross-sectional analyses assessing the number of LKTs were performed before and after the introduction of state legislation supporting donors, including tax benefits and paid and unpaid leave. Legislation was not universal, allowing states with and without legislation to be compared. Over the study period, the unadjusted mean overall LKD rate for states with enacted legislation was not greater than that for states with none (P 9 0.05). When time trends were compared for living-related and unrelated donations there seemed to be a plateau effect for living-related donations so that in both states with and without supportive legislation, rates declined after 2002, whilst there was a modest effect on LUDs, suggesting policies had a selective effect on this sub-group

DISCUSSION This review shows that research exists to support the hypothesis that SEP affects LKD, but the research is extremely heterogeneous. The evidence suggests that a higher SEP is associated with an increased reported willingness to be a living kidney donor. This should be interpreted with caution because the majority of studies assessed the attitudes of individuals in a hypothetical scenario rather than in the position of truly being an eligible donor for a relative or friend, and it is unclear how attitudes, beliefs, self-efficacy, and subjective norms translate into actual behavior (74Y76). In a commercial setting, socioeconomic deprivation motivates people to donate. Outside of this setting, there is no evidence of differences between the SEP of donors and recipients that would suggest financial exchange. The review also highlights the complex interaction of SEP with other variables, such as ethnicity, sex, and national economic climate. There is contradictory evidence to suggest that measures to remove financial disincentives to donation are associated with an increase in LKD rates, but because studies were ecological, and measures were not introduced in isolation, it cannot be concluded that increased rates are really attributable to removal of financial barriers. There remains genuine equipoise as to whether socioeconomic deprivation acts as a barrier or facilitator to LKD, with evidence to support both. A low SEP has been postulated as an incentive for donation in spousal pairs sharing an economic

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Criteria for considering studies in the review based on the PEO structure Inclusion criteria

Population 1

Potential living kidney donors; any living individual known to a recipient who could donate a kidney to them

Population 2

Potential living kidney transplant recipients; individuals with deteriorating CKD stage 4 or worse predicted to require, or already receiving, renal replacement therapy in any form (failing transplant, dialysis) SEP Incorporating economic (e.g., income), social (e.g., education) and work status (e.g., occupation) variables This may be measured at individual and/or area levels, and may refer to the donor or the recipient Progression toward LKD. This includes: Willingness to volunteer for living kidney donor assessment Progression through donor evaluation to actual donor nephrectomy (or transplantation if measured by the recipient) Progression toward LKT if recipient. Abstract and full-text All languages Quantitative: randomized controlled trials; cross-sectional studies; ecological studies; cohort studies; case-control studies Qualitative: phenomenological; ethnography; grounded theory.



Types of study

Exclusion criteria Age G18 years Altruistic donors (not known to intended recipient) Deceased organ donors Potential donors to paediatric recipients (age G 16 years) Age G18 years Stable CKD stage 4

Nonprimary research articles: Letters Commentaries


PEO, population exposure outcome; LKD, living kidney donation; SEP, socioeconomic position; LKT, living kidney transplantation; CKD, chronic kidney disease.

household because returning a chronically ill recipient to work may result in a net financial benefit (68). However sharing an economic household may be a disincentive to LKD in lower SEP families as they lack the capacity to ‘‘absorb the financial consequences of donation’’ (59). Examining Other Prosocial Acts LKD is an example of prosocial behavior (77) because a donor accepts some risk to self to help another. Although no other act is exactly comparable, findings from studies of SEP and other prosocial behaviors may inform our under standing of the relationship in transplantation: there is no consensus from the literature. Evidence from Europe suggests that, in general, blood donors, and those donating more frequently, are higher-income individuals (78), and higher SEP is associated with a more positive attitude toward deceased organ donation (79). Evidence from the United States, in contrast, suggests an inverse relationship between SEP and generosity, with lower SEP associated with greater prosocial behavior (80) and greater compassion toward those experiencing suffering (81). Research has suggested the existence of a ‘U-shaped income-giving profile’ in which those in lower and higher income brackets give higher percentages of their income to charity (82). This may mean that studies

examining SEP as a binary variable fail to identify the variation in donor behavior observed when SEP is classified with better resolution. Quality of Systematic Review and Included Studies Our systematic review methodology was thorough, and no study addressing our question was excluded. One limitation is that the search, study selection, quality assessment, and data extraction were only performed in their entirety by one reviewer, but a random sample of studies was independently assessed by a second reviewer. The quality of individual studies is detailed in the SDC (http://links.lww.com/TP/B59, Study characteristics). Few studies examined the actual population of interest, potential living donors, focusing instead on the general population, actual living kidney donors or recipients. There was a lack of research assessing the process of LKD in a prospective fashion using a cohort approach. There was a tendency when assessing potential donor attitudes to assess a hypothetical rather than actual scenario. Finally, few studies attempted to adjust their findings for other variables or explicitly test for potential interactions with age, ethnicity, sex, or other individual level characteristics.

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Guidelines for Future Research There is a need for better quality prospective research examining how SEP may impact on the true eligible potential donor population as they progress from being asked to donate to actual donor nephrectomy. It is premature to undertake formal intervention trials that are designed to reduce any socioeconomic barriers; it is important to first identify specific barriers to donation and assess the feasibility of any appropriate intervention. We have recently designed a mixedmethods multiphase multicenter study to address some of these questions in the United Kingdom (83). All observed health inequalities warrant further investigation, and if modifiable variables are identified, efforts made to redress them. Patients should have access to the best available treatment, regardless of SEP. There is a need to understand why this is not the case with LKTs and to identify potential areas for future intervention.


2. 3. 4.

5. 6.

7. 8. 9. 10.

MATERIALS AND METHODS The criteria for considering studies in the review based on the population, exposure, and outcome structure are summarized in Table 2. A literature search was performed in December 2013 by P.B. The following keywords and variants were used: living, donor(s), donation, transplant(s), kidney, renal, socioeconomic, deprivation, income, finance, and education. The following databases were searched: EMBASE/Medline/PsycINFO/ ASSIA/CINAHL/SIGLE/Cochrane Library/CRD York/British Library EThOS (see SDC, http://links.lww.com/TP/B59 Detailed search strategies). Additional reference list searches were performed, and three authors provided further data information. The quality of the studies was assessed using the Newcastle-Ottawa Scale (84), a tool for the assessment of nonrandomized studies for systematic reviews. Studies are scored out of a maximum of nine according to the selection and comparability of study groups, and the ascertainment of the exposure/outcome (see SDC, http://links.lww.com/TP/B59 NewcastleOttawa Scales). Content screening of search results and data extraction were performed by P.B. An independent subset analysis of a random sample of studies, including quality assessment and data extraction, was performed by a second reviewer (S.R.) for validity. Any disagreements were discussed for a unanimous decision.

Data Synthesis and Analysis Thirty-three suitable studies were identified, and all were included. The studies were combined according to the research question and the point on the living-donor pathway being examined. Overall, a narrative descriptive review was performed because of the wide heterogeneity of the studies. It was felt that data from nine studies examining the attitudes of hypothetical living kidney donors toward donation might be appropriately combined into a meta-analysis, performed using Stata 13. Data were extracted from these studies to populate a 22 table of a binary SEP exposure variable (high vs. low) against a binary outcome variable of being ‘‘willing to donate’’ or ‘‘not willing to donate.’’ A random effects metaanalysis was performed because of the marked heterogeneity between studies. This assumption was checked by examining the I2 statistic of the pooled absolute differences in the proportion of individuals who reported willingness to be a living kidney donor by SEP. A sensitivity analysis was performed with the highest quality studies. Results were stratified by the intended recipient of the hypothetical transplant.


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From potential donor to actual donation: does socioeconomic position affect living kidney donation? A systematic review of the evidence.

Evidence from Europe, Australia and the United States demonstrates that socioeconomically deprived individuals with advanced chronic kidney disease ar...
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