Perspective Financial Incentives for Living Kidney Donors: Are They Necessary? Dominique E. Martin, PhD,1 and Sarah L. White, PhD2 In the face of the perceived failure of altruistic organ donation programs to generate sufficient kidneys to meet demand, introducing financial incentives for living donors is sometimes argued as the only effective strategy by which lives currently lost while awaiting kidney transplantation might be saved. This argument from life-saving necessity is implicit in many incentive proposals, but rarely challenged by opponents. The core empirical claims on which it rests are thus rarely interrogated: that the gap between supply of and demand for donor kidneys is large and growing, the current system cannot meet demand, and financial incentives would increase the overall supply of kidneys and thus save lives. We consider these claims in the context of the United States. While we acknowledge the plausibility of claims that incentives, if sufficiently large, may successfully recruit greater numbers of living donors, we argue that strategies compatible with the existing altruistic system may also increase the supply of kidneys and save lives otherwise lost to kidney failure. We conclude that current appeals to the life-saving necessity argument have yet to establish sufficient grounds to justify trials of incentives. Am J Kidney Dis. -(-):---. ª 2015 by the National Kidney Foundation, Inc. INDEX WORDS: Kidney transplantation; end-stage renal disease (ESRD); living donors; transplant waiting list; organ procurement; altruistic organ donation; financial incentives; medical ethics.
INTRODUCTION “Altruistic” organ donation, in which donors (or their families) do not materially gain from donation,1 is the prevailing international norm in organ procurement programs. However, in the face of the perceived failure of current altruistic donation programs to generate a sufficient supply of kidneys to meet demand, the introduction of a regulated market that offers payment in return for living provision of a kidney is sometimes held to be the only effective strategy by which the lives currently lost while awaiting kidney transplantation might be saved.2-7 For some, financial incentives or other benefits representing a material gain for living kidney donation thus become a moral “imperative.”5,8 This argument from life-saving necessity (necessity argument) is implicit in many proposals for the introduction of markets in human kidneys, but is rarely challenged by market opponents. Proponents and opponents of financial incentives agree that efforts to reduce the premature loss of lives from end-stage renal disease (ESRD), including optimization of organ donation, are ethically warranted. Removal or reimbursement of the financial costs incurred by living kidney donors is also widely regarded as ethically acceptable.1,9,10 Debate instead habitually centers on differing evaluations of the consequences of financial incentives, especially regarding their impact on kidney vendors. Although we hold serious concerns regarding risks of impaired autonomy, exploitation, and harm to kidney vendors,11 in this article, we set aside these familiar components of the incentives debate and Am J Kidney Dis. 2015;-(-):---
focus solely on examining the necessity argument and the rarely contested empirical assumptions it contains (Box 1). Examining data from the United States, in which context the necessity argument is usually invoked, we consider the claims that the current system of altruistic donation cannot meet current and future demand, and that conversely, financial incentives would produce a substantial increase in, if not sufficiency of, kidneys for transplantation. We consider the donor potential within the existing altruistic system and discuss alternative uncontroversial strategies by which society might meet its ethical obligation to prevent the premature loss of human life from ESRD.
EVALUATING THE PROBLEM The supply-demand gap between the number of waitlisted candidates and the number of kidney transplantations performed each year in the United States is invoked to support the claim that unmet needs for transplantation constitute a “disaster,”12 costing thousands of lives and requiring immediate From the 1Centre for Health Equity, School of Population and Global Health, The University of Melbourne; and 2Charles Perkin Centre, Sydney Medical School, The University of Sydney, Sydney, Australia. Received October 22, 2014. Accepted in revised form March 6, 2015. Address correspondence to Dominique E. Martin, PhD, Level 4, 207 Bouverie Street, The University of Melbourne, 3010, Australia. E-mail: [email protected] 2015 by the National Kidney Foundation, Inc. 0272-6386 http://dx.doi.org/10.1053/j.ajkd.2015.03.041 1
Martin and White Box 1. Premises of the Argument From Life-Saving Necessity 1. Society has an ethical obligation to prevent the premature loss of human life when possible through the provision of necessary health care resources and services. 2. A large number of lives are currently lost prematurely as a result of end-stage renal disease; a proportion of these could be saved through timely provision of a kidney transplant if more kidneys were available. 3. Existing organ procurement systems based on altruistic donation are unable to meet current and anticipated future demand for kidney transplants. 4. Financial incentives for living provision of kidneys will increase the overall number of kidneys available for transplantation. 5. Potential ethical concerns about payment for living kidney provision can largely be addressed through market regulation; regardless, these concerns are insufficient to outweigh the overriding ethical obligation to maximize the saving of lives when possible. 6. Therefore, society has an ethical obligation to introduce financial incentives for living provision of kidneys.
intervention in the form of incentives for living kidney provision. We therefore begin by considering the scale of this gap. Table 1 compares current supply and demand, noting that demand may be enumerated as: (1) the total number of candidates on the kidney transplant waiting list, active and inactive (94,183 as of December 31, 2012); (2) the number of candidates on the active waiting list (57,903 as of December 31, 2012); or (3) the number of new candidates added to the waiting list in 2012 (31,157).13 On the one hand, it is argued that the organ shortage should be defined in terms of the total waiting list on the basis that many inactive candidates were once healthy enough to receive a transplant but become ineligible due to delayed transplantation.14 On the other hand, deceased donor kidneys can only be allocated to active candidates; thus, effective demand is confined to the active waitlist.15 At a minimum, meeting the demand for kidney transplantation would require that the annual number of kidney transplants exceed the number
of new additions. In 2012, a total of 31,157 candidates were added to the kidney transplant waiting list and 16,801 were removed due to transplantation: a shortfall of 14,356 transplants.13 However, .30% of adult waiting list additions in 2012 were inactive within 7 days of listing (n 5 10,587).13 Approximately 50% of initially inactive adult candidates will be activated within 12 months of listing; approximately one-third of initially inactive candidates will remain inactive, with these continuously inactive candidates tending to be older, obese, and other marginal candidates with poorer expected posttransplantation survival.16,17 Further, a large proportion (w40%) of candidates who die while inactive do so within 2 years of listing.15 These observations suggest that up to one-third of candidates listed initially as inactive may not be suitable for transplantation. The increased use of inactive status since the amendment to Organ Procurement and Transplantation Network policy 3.5.11 in 2003 (Fig 1) and the complexity of wait list dynamics16 may therefore result in overstatement of the gap between supply and effective demand for kidneys, particularly when cited in public commentaries on incentive proposals.18 Nevertheless, it is important to recognize that waiting lists, while an indicator of demand, are a poor reflection of true population need for kidney transplantation. A significant proportion of the population that might benefit from kidney transplantation is never wait-listed, either as active or inactive candidates. Schold et al19 estimate that successful efforts to increase access to transplantation for all candidates with a good prognosis (defined in their study as life expectancy . 5 years) would approximately double the existing waiting list.20 However, what this and other studies also report is that the reasons for nonlisting relate primarily to structural, geographic, and socioeconomic barriers to waiting list access, such as
Table 1. Kidney Transplant Waiting List Dynamics in 2012
Total (active and inactive) patients as of December 31, 2012 Active patients as of December 31, 2012 Patients added to the waiting list during 2012 Removed from waiting list: underwent transplantation Removed from the waiting list: died Removed from the waiting list: too sick to undergo transplantation & othera a
Adults
Children
92,885
1,298
57,378 30,274
525 883
16,025
776
5,209 5,029
27 57
Other reasons include patient refused transplant, patient improved (transplant not needed), and “other.” Data from: OPTN/SRTR 2012 Annual Data Report.13 2
Figure 1. New additions to the kidney transplant waiting list (adult and pediatric candidates) in each calendar year by patient status (active/inactive within 7 days of listing) compared to the total number of kidney transplantations performed in adult and pediatric patients in the same year. Data from OPTN/SRTR 2012 Annual Data Report.13 Am J Kidney Dis. 2015;-(-):---
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financial disincentives at the dialysis facility level, suboptimal distribution of transplant centers, limited health system capacity to evaluate and perform transplantation on patients, lack of insurance coverage, poverty, inadequate patient education, and other patient characteristics.20,21 Thus, without separate reforms to address the underlying bases of these access disparities, suitable candidates currently unable to access the waiting list would be unlikely to benefit from the introduction of financial incentives (or other strategies to increase donor rates). The growth of the kidney transplant waiting list in the United States over the past 2 decades has been driven by an increasing burden of treated ESRD, primarily diabetes related, and increased rates of waitlisting, particularly among older patients.22 Future demand for kidney transplantation will similarly depend on the interaction between trends in the underlying burden of disease, the case mix of patients with ESRD, and waitlisting practices. It is therefore significant that the number of individuals commencing renal replacement therapy in the United States appears to have stabilized. Compared to annualized growth in incident cases of 5.9% from 1991 to 2001, this rate decreased to 1.4% per annum over the past decade and to ,1% over the past 5 years.22 Annual growth of the prevalent ESRD population is lower than it has ever been despite a 25% decline in the mortality rate among dialysis patients during the past decade.22 However, current demand for donor kidneys remains formidable. Further, improved waitlist access for currently underserved populations has the potential to increase future demand for transplantation, even if the underlying ESRD burden recedes. Increasing the number of available kidneys is clearly necessary to achieve the best outcomes for patients: the question for the necessity argument is whether the current and potential future demand described can be met through an altruistic system.
EVALUATING POSSIBLE SOLUTIONS In 2003, Sheehy et al23 estimated the annual number of brain-dead potential donors in the United States to be between 10,500 and 13,800. By comparison, there were 8,144 actual donors in 2012.24 Substantial variation exists between donor service areas in terms of donor and organ yield metrics, indicating scope for greater efficiency.24 For example, it has been estimated that more than 5,000 additional kidneys would be transplanted annually if all organ procurement organizations performed at the level of the highest performing organization in terms of organ yield.25 There is also wide variation in rates of kidney discard across organ procurement organizations, with high rates of discard often observed in association with below-average rates of kidney recovery. The Am J Kidney Dis. 2015;-(-):---
number of kidneys discarded in the United States in 2012 was 2,759, a discard rate of 19%.24 Although some donor service areas face greater issues with donor medical status and/or diseased organs, the fact that w20% of discards occur because a recipient cannot be found indicates that allocation systems play a major role.26,27 Under the new kidney allocation system, regional sharing of kidneys with a kidney donor profile index . 85% is anticipated to reduce this rate of discard.28 Further, it is hoped that increasing the pool of potential recipients for high kidney donor profile index organs will act as an incentive to centers to recover more kidneys. Another factor in the current discard rate may be the routine use of procurement biopsies.29 Thus, optimization of organ recovery from eligible brain-dead donors and minimization of discards could significantly increase the yield of deceased donor kidneys. Increased use of organs from donors following circulatory death (DCDs) might also expand the existing deceased donor pool. DCDs account for 12% of all deceased donors in the United States.24 By comparison, DCDs account for up to 50% of deceased donors in select European countries.30 Several strategies have been proposed to increase the DCD pool in the United States.31 There were 993 DCDs in 2012 (3 per million population), resulting in 1,593 kidney transplants. If the DCD rate were to increase, for example, to the 8 donors per million population per year achieved in the United Kingdom,32 this would be equivalent to approximately 2,500 donors and 4,000 kidney transplants annually (based on 1.6 kidney transplants per DCD).22 Some of this number would constitute donors who would have otherwise proceeded down a brain death pathway; however, even after accounting for potential displacement of brain death donors, expanded use of DCDs has the potential to increase the overall donor pool. With respect to living donation, the decline in the rate of living related donation in the United States over the last decade is poorly understood,13 but has been taken to mean that any substantive increase in kidney supply from living providers will depend on novel recruitment methods such as financial incentives.33 This claim is at odds with the findings of repeated studies that the majority of Americans are in principle willing to donate a kidney to a loved one,34-36 suggesting that motivation is not the major barrier to living related donation. Instead, research increasingly shows that financial barriers prevent or discourage many from becoming living related donors; a recent study, for example, showed that the decrease in living donation since 2004 was confined to middle- to lowincome populations.37 3
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Financial barriers or disincentives represent the costs that prospective and actual living donors may incur. Conversely, financial incentives represent material gains for donors, with a commercial value greater than actual costs incurred as a consequence of donation or donor evaluation. Despite international consensus regarding the ethical acceptability of removing financial disincentives to living donation,38 few countries provide comprehensive support to address disincentives. In the United States, a recent report from the National Living Donor Assistance Center (NLDAC) showed that living donors who qualified for support incurred average travel costs of $2,767, and that 39% identified lost wages of $2,784 on average.9 Thus, living donors commonly incur nearly $6,000 in out-of-pocket costs, or 20% of the median household income for NLDAC program participants. It is possible that many potential living donors are deterred prior to entering a donor screening program due to financial concerns. A Canadian study reported that 36% of donors who received reimbursement of expenses indicated they might not have donated in the absence of this support.39 Some transplant candidates may not pursue the possibility of a living donor transplant due to factors that discourage efforts to identify and approach potential donors, especially among racial and ethnic minorities. Such factors may include insufficient knowledge of living donation, the aforementioned financial concerns, and distrust in health care providers.40 A number of programs designed to educate transplant candidates about living donation and/or facilitate engagement of potential living donors, for example, through use of advocates, have increased rates of living donor transplantation among program participants.41-44 Finally, as many as one-third of potentially willing related donors are incompatible with their recipient.45 Kidney paired donation (KPD) allows living donor kidney transplantation to proceed in such cases. Since 2005, KPD has become “the fastest growing source of transplantable kidneys” in the United States (Fig 2).46(p2,091) However, KPD transplantation remains clustered among a small number of transplantation centers, and wider implementation may therefore increase the number of transplantation procedures involving KPD.47 The development of advanced matching algorithms, incorporation of blood group ABO incompatible donor-recipient pairs, desensitization, 3-way exchanges, and chains continue to enhance the capacity of KPD transplantation.46,48
THE PROMISE OF FINANCIAL INCENTIVES The confidence that advocates of the necessity argument place in the efficacy of incentives is rarely 4
Figure 2. Number of kidney paired donations performed annually between 2000 and 2012. Data from OPTN/SRTR 2012 Annual Report.13
linked to specific incentive schemes. Instead, market advocates often suggest that a range of incentives would be effective, and policy makers need only test which would have the greatest impact or be most preferred by a particular community.49 Beard et al2 conclude that “likely kidney prices for living donors in developed countries will be in the tens of thousands of dollars.”(p211) The Working Group on Incentives for Living Donation proposes only that incentives “should be of adequate value (and able to improve the donor’s circumstances).”33(p308) In short, the promise of financial incentives largely relies on the intuition that if sufficient money is offered, a sufficient number of people will be willing to sell a kidney. This intuition aligns with the evidence from existing markets indicating that a number of individuals in all societies may be willing to sell a kidney, depending on an interaction of 3 key variables: (1) preferences regarding kidney selling and other income-generating options available, (2) the magnitude of incentive offered, and (3) economic status and immediate financial needs of individuals and their dependents. The international black market for kidneys demonstrates a ready supply of individuals who will decide that selling a kidney is their best option, particularly when facing economic crisis. Further, evidence from Iran’s poorly regulated but legal market for kidneys confirms that financial pressures underpin the decision to sell a kidney in most, if not all, cases.50,51 In a recent US survey, Gordon et al35 similarly found that participants willing to donate a kidney for “compensation” would primarily seek to pay off debts with the money received. Efforts to elicit public attitudes toward incentives in the United States have provided some insights into the potential influence of incentives on donor recruitment. Halpern et al,34 for example, found that a minority of Am J Kidney Dis. 2015;-(-):---
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individuals across all income groups were hypothetically more willing to provide a kidney to a stranger as the financial incentive increased. In a Dutch survey, 5.5% of participants reported a great or very great chance that they would provide a kidney in return for a financial incentive.52 Other international studies have found moderate levels of public support for “incentives”; however, examination of the specific incentives proposed indicates a preference for removal of disincentives, such as coverage of lost wages or nonmedical expenses incurred or the provision of insurance or health care services to protect donors against risks incurred through nephrectomy.35,36,53,54 We assume that some members of a population, eligible but unwilling to donate a kidney to a stranger or relative, would be motivated to do so in return for some amount of financial incentive.34,35 However, the potential impact of an incentive program on the existing unpaid willing donor pool must also be considered. Market advocates acknowledge this concern about “crowding out,” but argue that the evidence on public preferences indicates that the existence of incentives would not undermine public support for unpaid donation or willingness to donate to loved ones.4-6,35,55 However, to date, no survey has asked participants if they would be willing to donate to a relative if a kidney could instead be obtained from a paid provider, thereby eliminating the hypothetical need and hence motivation for their own donation. Real-world evidence shows that such crowding out is plausible. In Iran, the majority of kidney transplant recipients have potential living related donors available to them, but instead opt to purchase a kidney from an unrelated donor.56 The removal of options to purchase organs at home or overseas is associated conversely with increased living related donation, as seen recently in Israel and Qatar.57,58 Arguably, if the supply of kidneys from paid donors is sufficiently large, this could compensate for any crowding-out effect on altruistic living donation.6,55 However, it is plausible that financial incentives for living donation might also negatively affect the public’s willingness to participate in deceased donation due to change in its perceived social value or distrust in organ procurement programs. Evidence indicating that the great majority of Americans willing to donate their organs after death are opposed to cash payments for either living or deceased donation36 suggests that the potential for crowding out of altruistic deceased donation must be taken seriously. Iran has been cited as a counterexample to fears of deceased donation crowding out, given its recent development of an unpaid deceased donation system in parallel with a market in living donor kidneys. However, a 2011 Iranian study found that of the 58% of families who declined to authorize donation in one organ procurement organization, Am J Kidney Dis. 2015;-(-):---
15% did so due to concerns about potential gossip that they had donated for money.59 Even a small decline in deceased donor numbers in the United States would mean fewer life-saving heart, lung, and liver transplants.
ARE INCENTIVE TRIALS JUSTIFIED AT THIS TIME? Proponents of the necessity argument point to the deaths of individuals awaiting kidney transplantation as the consequence of prohibition of financial incentives2-7 and thus contend there is a moral imperative to reduce waitlist mortality by the introduction of regulated markets for kidneys.3-5,12 Although the consequentialist rhetoric of the necessity argument has exerted a powerful influence on debate, the actual potential of a regulated market to increase the overall supply of kidneys for transplantation is at present entirely speculative. In contrast, we argue that the capacity of the existing altruistic donation system has not been exhausted. Disappointment in current organ procurement organization performance should stimulate renewed and repeated efforts to diagnose and address system failures. Action should be informed by formal review of best practices and knowledge gaps, as undertaken during the 2014 Consensus Conference on Best Practices in Live Kidney Donation.60 To save lives, it is also necessary to reduce the need for kidney transplantation. Pursuit of an everincreasing supply of organs for transplantation is not only unsustainable for health systems, but is also unduly burdensome for potential donor populations and neglects equally critical responsibilities with respect to disease prevention. The obligation incumbent on health systems to prevent unnecessary loss of life from ESRD would therefore best be met through intervention in the modifiable causes of ESRD while simultaneously optimizing rates of kidney donation. Even if altruism-based strategies were proved to yield overall more kidneys for transplantation than an incentive-based system, this would not in itself preclude the use of incentives in conjunction with other strategies to increase donor rates unless there are reasonable grounds to expect that introducing incentive-based strategies would decrease the overall supply of kidneys for transplantation. We have argued that this risk must be taken seriously. However, retention of the prohibition would also be justified if the fifth premise of the necessity argument were proven false: that is, if it were shown that ethical concerns about the use of incentives are sufficient to outweigh the overriding ethical obligation to save lives when possible. Although we have deferred discussion of this latter point to another forum, we note that advocates of incentives have recently called for “pilot studies” on the grounds that these would assist 5
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in evaluating not only the efficacy of incentives, but also potential ethical concerns.33,34 Prior to any such trials, we contend that more robust incentive proposals should be presented. These should be subject to critical analysis and detailed impact assessment so that any decision to revoke the National Organ Transplant Act may be well informed and that the design of a clinical trial of incentives may be subject to rigorous scientific and ethical review before implementation. Detailed proposals specifying the mode(s) of delivery and magnitude of incentive(s) to be offered in designated populations will facilitate estimation of the likely efficacy of incentives in recruitment, the potential risks to vendor populations, and the potential impact on the existing altruistic system. The apparent simplicity of incentive proposals— merely recruit more living donors by offering payment—contrasts with the inherent complexities and costs associated with increasing the efficiency of the existing system. However, the introduction of incentives would also necessarily increase the operational and regulatory complexity of kidney transplantation and likely lead to unintended consequences.11 In conclusion, we note simply that the best-performing organ donation programs in the world currently rely on altruistic donors. Disincentives and barriers to participation in living donation and to the procurement of deceased donor organs, rather than insufficient public motivation to donate, constrain the availability of kidneys for transplantation. Financial incentives may threaten the success of established altruistic programs and ultimately lead to greater loss of lives.
ACKNOWLEDGEMENTS Both authors are members of the Declaration of Istanbul Custodian Group, and Dr Martin is co-chair of The Transplantation Society Ethics Committee. The views presented in this paper are the authors’ own and do not represent the opinions or positions of either organization. This commentary uses data from annual reports of the US Renal Data System (USRDS) and the Organ Procurement and Transplantation Network/Scientific Registry of Transplant Recipients (OPTN/SRTR; produced by the Minneapolis Medical Research Foundation and United Network for Organ Sharing under contract with HHS/HRSA). The interpretation and reporting of these data are the responsibility of the author(s) and in no way should be seen as an official policy or interpretation of the US government. We thank the 3 anonymous reviewers who provided very helpful feedback on an earlier draft of this manuscript. Support: None. Financial Disclosure: The authors declare that they have no relevant financial interests.
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Reevaluating the Need for Kidney Donor Incentives 25. Israni A. Donor potential if all organ procurement organisations (OPOs) in the US were performing as expected or better. Oral presentation at: World Transplant Congress 2014. July 26-31, 2014; San Francisco, CA. 26. Massie AB, Zeger SL, Montgomery RA, Segev DL. The effects of DonorNet 2007 on kidney distribution equity and efficiency. Am J Transplant. 2009;9(7):1550-1557. 27. Massie AB, Desai NM, Montgomery RA, Singer AL, Segev DL. Improving distribution efficiency of hard-to-place deceased donor kidneys: predicting probability of discard or delay. Am J Transplant. 2010;10(7):1613-1620. 28. Israni AK, Salkowski N, Gustafson S, et al. New national allocation policy for deceased donor kidneys in the United States and possible effect on patient outcomes. J Am Soc Nephrol. 2014;25:1842-1848. 29. Kasiske BL, Stewart DE, Bista BR, et al. The role of procurement biopsies in acceptance decisions for kidneys retrieved for transplant. Clin J Am Soc Nephrol. 2014;9:562-571. 30. Domínguez-Gil B, Haase-Kromwijk B, Van Leiden H, et al. Current situation of donation after circulatory death in European countries. Transpl Int. 2011;24(7):676-686. 31. Morrissey PE, Monaco AP. Donation after circulatory death: current practices, ongoing challenges, and potential improvements. Transplantation. 2014;97(3):258-264. 32. Johnson R. Organ Donation and Transplantation Activity Report 2012/13. Bristol, UK: NHS Blood and Transplant; 2013. http://www.nhsbt.nhs.uk/download/board_papers/sept13/Organ_ Donation_and_Transplantation_Activity_Report.pdf. Accessed June 1, 2015. 33. Working Group on Incentives for Living Donation. Incentives for organ donation: proposed standards for an inter nationally acceptable system. Am J Transplant. 2011;12(2):306312. 34. Halpern SD, Raz A, Kohn R, Rey M, Asch DA, Reese P. Regulated payments for living kidney donation: an empirical assessment of the ethical concerns. Ann Intern Med. 2010;152(6): 358-365. 35. Gordon EJ, Patel CH, Sohn M-W, Hippen B, Sherman LA. Does financial compensation for living kidney donation change willingness to donate? Am J Transplant. 2015;15(1):265-273. 36. Boulware LE, Troll MU, Wang NY, Powe NR. Public attitudes toward incentives for organ donation: a national study of different racial/ethnic and income groups. Am J Transplant. 2006;6(11):2774-2785. 37. Gill J, Dong J, Gill J. Population income and longitudinal trends in living kidney donation in the United States. J Am Soc Nephrol. 2015;26(1):201-207. 38. Tong A, Chapman JR, Wong G, Craig JC. Perspectives of transplant physicians and surgeons on reimbursement, compensation, and incentives for living kidney donors. Am J Kidney Dis. 2014. 39. Gill JS, Klarenbach S, Barnieh L, et al. Financial incentives to increase Canadian organ donation: quick fix or fallacy? Am J Kidney Dis. 2014;63(1):133-140. 40. Waterman AD, Rodrigue JR, Purnell TS, Ladin K, Boulware LE. Addressing racial and ethnic disparities in live donor kidney transplantation: priorities for research and intervention. Semin Nephrol. 2010;30(1):90-98. 41. Davis CL. How to increase living donation. Transpl Int. 2011;24(4):344-349.
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42. Waterman AD, Barrett AC, Stanley SL. Optimal transplant education for recipients to increase pursuit of living donation. Prog Transplant. 2008;18(1):55-62. 43. Rodrigue JR, Paek MJ, Egbuna O, et al. Making house calls increases living donor inquiries and evaluations for blacks on the kidney transplant waiting list. Transplantation. 2014;98(9):979-986. 44. Garonzik-Wang JM, Berger JC, Ros RL, et al. Live donor champion: finding live kidney donors by separating the advocate from the patient. Transplantation. 2012;93(11):1147-1150. 45. Gentry SE, Montgomery RA, Segev DL. Kidney paired donation: fundamentals, limitations, and expansions. Am J Kidney Dis. 2011;57(1):144-151. 46. Wallis CB, Samy KP, Roth AE, Rees MA. Kidney paired donation. Nephrol Dial Transplant. 2011;26(7):2091-2099. 47. Massie AB, Gentry SE, Montgomery RA, Bingaman AA, Segev DL. Center-level utilization of kidney paired donation. Am J Transplant. 2013;13(5):1317-1322. 48. Li Y, Song PX-K, Zhou Y, Leichtman AB, Rees MA, Kalbfleisch JD. Optimal decisions for organ exchanges in a kidney paired donation program. Stat Biosci. 2014;6(1):85-104. 49. Hippen B, Matas A. Incentives for organ donation in the United States: feasible alternative or forthcoming apocalypse? Curr Opin Organ Transplant. 2009;14(2):140-146. 50. Fry-Revere S. The Kidney Sellers: A Journey of Discovery in Iran. Durham, NC: Carolina Academic Press; 2014. 51. Beladi Mousavi SS, Alemzadeh Ansari MJ, Parsi A, Kiani E. Reasons for renal donation among living unrelated renal donors in Khuzestan Province, Southwestern Iran. Int J Organ Transplant Med. 2013;4(1):21-24. 52. Kranenburg L, Schram A, Zuidema W, et al. Public survey of financial incentives for kidney donation. Nephrol Dial Transplant. 2007;23(3):1039-1042. 53. Hoeyer K, Schicktanz S, Deleuran I. Public attitudes to financial incentive models for organs: a literature review suggests that it is time to shift the focus from ‘financial incentives’ to ‘reciprocity.’ Transplant Int. 2013;26(4):350-357. 54. Elias JJ, Lacetera N, Macis M. Sacred Values? The Effect of Information on Attitudes Toward Payments for Human Organs. Cambridge, MA: National Bureau of Economic Research; 2015. 55. Cherry MJ. Kidney for Sale by Owner. Washington, DC: Georgetown University Press; 2005. 56. Ghods AJ, Savaj S, Khosravani P. Adverse effects of a controlled living-unrelated donor renal transplant program on living-related and cadaveric kidney donation. Transplant Proc. 2000;32(3):541. 57. Padilla B, Danovitch GM, Lavee J. Impact of legal measures prevent transplant tourism: the interrelated experience of the Philippines and Israel. Med Health Care Philos. 2013;16(4):915-919. 58. Martin D, Fadhil R. The Doha model of organ donation and transplantation—thinking beyond citizenship. Griffith J Law Hum Dignity. 2014;2(2). 59. Dehghani SM, Gholami S, Bahador A, et al. Causes of organ donation refusal in Southern Iran. Transplant Proc. 2011;43(2):410-411. 60. LaPointe Rudow D, Hays R, Baliga P, et al. Consensus conference on best practices in live kidney donation: recommendations to optimize education, access, and care. Am J Transplant. 2015;15(4):914-922.
7
INTRODUCTION “Altruistic” organ donation, in which donors (or their families) do not materially gain from donation,1 is the prevailing international norm in organ procurement programs. However, in the face of the perceived failure of current altruistic donation programs to generate a sufficient supply of kidneys to meet demand, the introduction of a regulated market that offers payment in return for living provision of a kidney is sometimes held to be the only effective strategy by which the lives currently lost while awaiting kidney transplantation might be saved.2-7 For some, financial incentives or other benefits representing a material gain for living kidney donation thus become a moral “imperative.”5,8 This argument from life-saving necessity (necessity argument) is implicit in many proposals for the introduction of markets in human kidneys, but is rarely challenged by market opponents. Proponents and opponents of financial incentives agree that efforts to reduce the premature loss of lives from end-stage renal disease (ESRD), including optimization of organ donation, are ethically warranted. Removal or reimbursement of the financial costs incurred by living kidney donors is also widely regarded as ethically acceptable.1,9,10 Debate instead habitually centers on differing evaluations of the consequences of financial incentives, especially regarding their impact on kidney vendors. Although we hold serious concerns regarding risks of impaired autonomy, exploitation, and harm to kidney vendors,11 in this article, we set aside these familiar components of the incentives debate and Am J Kidney Dis. 2015;-(-):---
focus solely on examining the necessity argument and the rarely contested empirical assumptions it contains (Box 1). Examining data from the United States, in which context the necessity argument is usually invoked, we consider the claims that the current system of altruistic donation cannot meet current and future demand, and that conversely, financial incentives would produce a substantial increase in, if not sufficiency of, kidneys for transplantation. We consider the donor potential within the existing altruistic system and discuss alternative uncontroversial strategies by which society might meet its ethical obligation to prevent the premature loss of human life from ESRD.
EVALUATING THE PROBLEM The supply-demand gap between the number of waitlisted candidates and the number of kidney transplantations performed each year in the United States is invoked to support the claim that unmet needs for transplantation constitute a “disaster,”12 costing thousands of lives and requiring immediate From the 1Centre for Health Equity, School of Population and Global Health, The University of Melbourne; and 2Charles Perkin Centre, Sydney Medical School, The University of Sydney, Sydney, Australia. Received October 22, 2014. Accepted in revised form March 6, 2015. Address correspondence to Dominique E. Martin, PhD, Level 4, 207 Bouverie Street, The University of Melbourne, 3010, Australia. E-mail: [email protected] 2015 by the National Kidney Foundation, Inc. 0272-6386 http://dx.doi.org/10.1053/j.ajkd.2015.03.041 1
Martin and White Box 1. Premises of the Argument From Life-Saving Necessity 1. Society has an ethical obligation to prevent the premature loss of human life when possible through the provision of necessary health care resources and services. 2. A large number of lives are currently lost prematurely as a result of end-stage renal disease; a proportion of these could be saved through timely provision of a kidney transplant if more kidneys were available. 3. Existing organ procurement systems based on altruistic donation are unable to meet current and anticipated future demand for kidney transplants. 4. Financial incentives for living provision of kidneys will increase the overall number of kidneys available for transplantation. 5. Potential ethical concerns about payment for living kidney provision can largely be addressed through market regulation; regardless, these concerns are insufficient to outweigh the overriding ethical obligation to maximize the saving of lives when possible. 6. Therefore, society has an ethical obligation to introduce financial incentives for living provision of kidneys.
intervention in the form of incentives for living kidney provision. We therefore begin by considering the scale of this gap. Table 1 compares current supply and demand, noting that demand may be enumerated as: (1) the total number of candidates on the kidney transplant waiting list, active and inactive (94,183 as of December 31, 2012); (2) the number of candidates on the active waiting list (57,903 as of December 31, 2012); or (3) the number of new candidates added to the waiting list in 2012 (31,157).13 On the one hand, it is argued that the organ shortage should be defined in terms of the total waiting list on the basis that many inactive candidates were once healthy enough to receive a transplant but become ineligible due to delayed transplantation.14 On the other hand, deceased donor kidneys can only be allocated to active candidates; thus, effective demand is confined to the active waitlist.15 At a minimum, meeting the demand for kidney transplantation would require that the annual number of kidney transplants exceed the number
of new additions. In 2012, a total of 31,157 candidates were added to the kidney transplant waiting list and 16,801 were removed due to transplantation: a shortfall of 14,356 transplants.13 However, .30% of adult waiting list additions in 2012 were inactive within 7 days of listing (n 5 10,587).13 Approximately 50% of initially inactive adult candidates will be activated within 12 months of listing; approximately one-third of initially inactive candidates will remain inactive, with these continuously inactive candidates tending to be older, obese, and other marginal candidates with poorer expected posttransplantation survival.16,17 Further, a large proportion (w40%) of candidates who die while inactive do so within 2 years of listing.15 These observations suggest that up to one-third of candidates listed initially as inactive may not be suitable for transplantation. The increased use of inactive status since the amendment to Organ Procurement and Transplantation Network policy 3.5.11 in 2003 (Fig 1) and the complexity of wait list dynamics16 may therefore result in overstatement of the gap between supply and effective demand for kidneys, particularly when cited in public commentaries on incentive proposals.18 Nevertheless, it is important to recognize that waiting lists, while an indicator of demand, are a poor reflection of true population need for kidney transplantation. A significant proportion of the population that might benefit from kidney transplantation is never wait-listed, either as active or inactive candidates. Schold et al19 estimate that successful efforts to increase access to transplantation for all candidates with a good prognosis (defined in their study as life expectancy . 5 years) would approximately double the existing waiting list.20 However, what this and other studies also report is that the reasons for nonlisting relate primarily to structural, geographic, and socioeconomic barriers to waiting list access, such as
Table 1. Kidney Transplant Waiting List Dynamics in 2012
Total (active and inactive) patients as of December 31, 2012 Active patients as of December 31, 2012 Patients added to the waiting list during 2012 Removed from waiting list: underwent transplantation Removed from the waiting list: died Removed from the waiting list: too sick to undergo transplantation & othera a
Adults
Children
92,885
1,298
57,378 30,274
525 883
16,025
776
5,209 5,029
27 57
Other reasons include patient refused transplant, patient improved (transplant not needed), and “other.” Data from: OPTN/SRTR 2012 Annual Data Report.13 2
Figure 1. New additions to the kidney transplant waiting list (adult and pediatric candidates) in each calendar year by patient status (active/inactive within 7 days of listing) compared to the total number of kidney transplantations performed in adult and pediatric patients in the same year. Data from OPTN/SRTR 2012 Annual Data Report.13 Am J Kidney Dis. 2015;-(-):---
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financial disincentives at the dialysis facility level, suboptimal distribution of transplant centers, limited health system capacity to evaluate and perform transplantation on patients, lack of insurance coverage, poverty, inadequate patient education, and other patient characteristics.20,21 Thus, without separate reforms to address the underlying bases of these access disparities, suitable candidates currently unable to access the waiting list would be unlikely to benefit from the introduction of financial incentives (or other strategies to increase donor rates). The growth of the kidney transplant waiting list in the United States over the past 2 decades has been driven by an increasing burden of treated ESRD, primarily diabetes related, and increased rates of waitlisting, particularly among older patients.22 Future demand for kidney transplantation will similarly depend on the interaction between trends in the underlying burden of disease, the case mix of patients with ESRD, and waitlisting practices. It is therefore significant that the number of individuals commencing renal replacement therapy in the United States appears to have stabilized. Compared to annualized growth in incident cases of 5.9% from 1991 to 2001, this rate decreased to 1.4% per annum over the past decade and to ,1% over the past 5 years.22 Annual growth of the prevalent ESRD population is lower than it has ever been despite a 25% decline in the mortality rate among dialysis patients during the past decade.22 However, current demand for donor kidneys remains formidable. Further, improved waitlist access for currently underserved populations has the potential to increase future demand for transplantation, even if the underlying ESRD burden recedes. Increasing the number of available kidneys is clearly necessary to achieve the best outcomes for patients: the question for the necessity argument is whether the current and potential future demand described can be met through an altruistic system.
EVALUATING POSSIBLE SOLUTIONS In 2003, Sheehy et al23 estimated the annual number of brain-dead potential donors in the United States to be between 10,500 and 13,800. By comparison, there were 8,144 actual donors in 2012.24 Substantial variation exists between donor service areas in terms of donor and organ yield metrics, indicating scope for greater efficiency.24 For example, it has been estimated that more than 5,000 additional kidneys would be transplanted annually if all organ procurement organizations performed at the level of the highest performing organization in terms of organ yield.25 There is also wide variation in rates of kidney discard across organ procurement organizations, with high rates of discard often observed in association with below-average rates of kidney recovery. The Am J Kidney Dis. 2015;-(-):---
number of kidneys discarded in the United States in 2012 was 2,759, a discard rate of 19%.24 Although some donor service areas face greater issues with donor medical status and/or diseased organs, the fact that w20% of discards occur because a recipient cannot be found indicates that allocation systems play a major role.26,27 Under the new kidney allocation system, regional sharing of kidneys with a kidney donor profile index . 85% is anticipated to reduce this rate of discard.28 Further, it is hoped that increasing the pool of potential recipients for high kidney donor profile index organs will act as an incentive to centers to recover more kidneys. Another factor in the current discard rate may be the routine use of procurement biopsies.29 Thus, optimization of organ recovery from eligible brain-dead donors and minimization of discards could significantly increase the yield of deceased donor kidneys. Increased use of organs from donors following circulatory death (DCDs) might also expand the existing deceased donor pool. DCDs account for 12% of all deceased donors in the United States.24 By comparison, DCDs account for up to 50% of deceased donors in select European countries.30 Several strategies have been proposed to increase the DCD pool in the United States.31 There were 993 DCDs in 2012 (3 per million population), resulting in 1,593 kidney transplants. If the DCD rate were to increase, for example, to the 8 donors per million population per year achieved in the United Kingdom,32 this would be equivalent to approximately 2,500 donors and 4,000 kidney transplants annually (based on 1.6 kidney transplants per DCD).22 Some of this number would constitute donors who would have otherwise proceeded down a brain death pathway; however, even after accounting for potential displacement of brain death donors, expanded use of DCDs has the potential to increase the overall donor pool. With respect to living donation, the decline in the rate of living related donation in the United States over the last decade is poorly understood,13 but has been taken to mean that any substantive increase in kidney supply from living providers will depend on novel recruitment methods such as financial incentives.33 This claim is at odds with the findings of repeated studies that the majority of Americans are in principle willing to donate a kidney to a loved one,34-36 suggesting that motivation is not the major barrier to living related donation. Instead, research increasingly shows that financial barriers prevent or discourage many from becoming living related donors; a recent study, for example, showed that the decrease in living donation since 2004 was confined to middle- to lowincome populations.37 3
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Financial barriers or disincentives represent the costs that prospective and actual living donors may incur. Conversely, financial incentives represent material gains for donors, with a commercial value greater than actual costs incurred as a consequence of donation or donor evaluation. Despite international consensus regarding the ethical acceptability of removing financial disincentives to living donation,38 few countries provide comprehensive support to address disincentives. In the United States, a recent report from the National Living Donor Assistance Center (NLDAC) showed that living donors who qualified for support incurred average travel costs of $2,767, and that 39% identified lost wages of $2,784 on average.9 Thus, living donors commonly incur nearly $6,000 in out-of-pocket costs, or 20% of the median household income for NLDAC program participants. It is possible that many potential living donors are deterred prior to entering a donor screening program due to financial concerns. A Canadian study reported that 36% of donors who received reimbursement of expenses indicated they might not have donated in the absence of this support.39 Some transplant candidates may not pursue the possibility of a living donor transplant due to factors that discourage efforts to identify and approach potential donors, especially among racial and ethnic minorities. Such factors may include insufficient knowledge of living donation, the aforementioned financial concerns, and distrust in health care providers.40 A number of programs designed to educate transplant candidates about living donation and/or facilitate engagement of potential living donors, for example, through use of advocates, have increased rates of living donor transplantation among program participants.41-44 Finally, as many as one-third of potentially willing related donors are incompatible with their recipient.45 Kidney paired donation (KPD) allows living donor kidney transplantation to proceed in such cases. Since 2005, KPD has become “the fastest growing source of transplantable kidneys” in the United States (Fig 2).46(p2,091) However, KPD transplantation remains clustered among a small number of transplantation centers, and wider implementation may therefore increase the number of transplantation procedures involving KPD.47 The development of advanced matching algorithms, incorporation of blood group ABO incompatible donor-recipient pairs, desensitization, 3-way exchanges, and chains continue to enhance the capacity of KPD transplantation.46,48
THE PROMISE OF FINANCIAL INCENTIVES The confidence that advocates of the necessity argument place in the efficacy of incentives is rarely 4
Figure 2. Number of kidney paired donations performed annually between 2000 and 2012. Data from OPTN/SRTR 2012 Annual Report.13
linked to specific incentive schemes. Instead, market advocates often suggest that a range of incentives would be effective, and policy makers need only test which would have the greatest impact or be most preferred by a particular community.49 Beard et al2 conclude that “likely kidney prices for living donors in developed countries will be in the tens of thousands of dollars.”(p211) The Working Group on Incentives for Living Donation proposes only that incentives “should be of adequate value (and able to improve the donor’s circumstances).”33(p308) In short, the promise of financial incentives largely relies on the intuition that if sufficient money is offered, a sufficient number of people will be willing to sell a kidney. This intuition aligns with the evidence from existing markets indicating that a number of individuals in all societies may be willing to sell a kidney, depending on an interaction of 3 key variables: (1) preferences regarding kidney selling and other income-generating options available, (2) the magnitude of incentive offered, and (3) economic status and immediate financial needs of individuals and their dependents. The international black market for kidneys demonstrates a ready supply of individuals who will decide that selling a kidney is their best option, particularly when facing economic crisis. Further, evidence from Iran’s poorly regulated but legal market for kidneys confirms that financial pressures underpin the decision to sell a kidney in most, if not all, cases.50,51 In a recent US survey, Gordon et al35 similarly found that participants willing to donate a kidney for “compensation” would primarily seek to pay off debts with the money received. Efforts to elicit public attitudes toward incentives in the United States have provided some insights into the potential influence of incentives on donor recruitment. Halpern et al,34 for example, found that a minority of Am J Kidney Dis. 2015;-(-):---
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individuals across all income groups were hypothetically more willing to provide a kidney to a stranger as the financial incentive increased. In a Dutch survey, 5.5% of participants reported a great or very great chance that they would provide a kidney in return for a financial incentive.52 Other international studies have found moderate levels of public support for “incentives”; however, examination of the specific incentives proposed indicates a preference for removal of disincentives, such as coverage of lost wages or nonmedical expenses incurred or the provision of insurance or health care services to protect donors against risks incurred through nephrectomy.35,36,53,54 We assume that some members of a population, eligible but unwilling to donate a kidney to a stranger or relative, would be motivated to do so in return for some amount of financial incentive.34,35 However, the potential impact of an incentive program on the existing unpaid willing donor pool must also be considered. Market advocates acknowledge this concern about “crowding out,” but argue that the evidence on public preferences indicates that the existence of incentives would not undermine public support for unpaid donation or willingness to donate to loved ones.4-6,35,55 However, to date, no survey has asked participants if they would be willing to donate to a relative if a kidney could instead be obtained from a paid provider, thereby eliminating the hypothetical need and hence motivation for their own donation. Real-world evidence shows that such crowding out is plausible. In Iran, the majority of kidney transplant recipients have potential living related donors available to them, but instead opt to purchase a kidney from an unrelated donor.56 The removal of options to purchase organs at home or overseas is associated conversely with increased living related donation, as seen recently in Israel and Qatar.57,58 Arguably, if the supply of kidneys from paid donors is sufficiently large, this could compensate for any crowding-out effect on altruistic living donation.6,55 However, it is plausible that financial incentives for living donation might also negatively affect the public’s willingness to participate in deceased donation due to change in its perceived social value or distrust in organ procurement programs. Evidence indicating that the great majority of Americans willing to donate their organs after death are opposed to cash payments for either living or deceased donation36 suggests that the potential for crowding out of altruistic deceased donation must be taken seriously. Iran has been cited as a counterexample to fears of deceased donation crowding out, given its recent development of an unpaid deceased donation system in parallel with a market in living donor kidneys. However, a 2011 Iranian study found that of the 58% of families who declined to authorize donation in one organ procurement organization, Am J Kidney Dis. 2015;-(-):---
15% did so due to concerns about potential gossip that they had donated for money.59 Even a small decline in deceased donor numbers in the United States would mean fewer life-saving heart, lung, and liver transplants.
ARE INCENTIVE TRIALS JUSTIFIED AT THIS TIME? Proponents of the necessity argument point to the deaths of individuals awaiting kidney transplantation as the consequence of prohibition of financial incentives2-7 and thus contend there is a moral imperative to reduce waitlist mortality by the introduction of regulated markets for kidneys.3-5,12 Although the consequentialist rhetoric of the necessity argument has exerted a powerful influence on debate, the actual potential of a regulated market to increase the overall supply of kidneys for transplantation is at present entirely speculative. In contrast, we argue that the capacity of the existing altruistic donation system has not been exhausted. Disappointment in current organ procurement organization performance should stimulate renewed and repeated efforts to diagnose and address system failures. Action should be informed by formal review of best practices and knowledge gaps, as undertaken during the 2014 Consensus Conference on Best Practices in Live Kidney Donation.60 To save lives, it is also necessary to reduce the need for kidney transplantation. Pursuit of an everincreasing supply of organs for transplantation is not only unsustainable for health systems, but is also unduly burdensome for potential donor populations and neglects equally critical responsibilities with respect to disease prevention. The obligation incumbent on health systems to prevent unnecessary loss of life from ESRD would therefore best be met through intervention in the modifiable causes of ESRD while simultaneously optimizing rates of kidney donation. Even if altruism-based strategies were proved to yield overall more kidneys for transplantation than an incentive-based system, this would not in itself preclude the use of incentives in conjunction with other strategies to increase donor rates unless there are reasonable grounds to expect that introducing incentive-based strategies would decrease the overall supply of kidneys for transplantation. We have argued that this risk must be taken seriously. However, retention of the prohibition would also be justified if the fifth premise of the necessity argument were proven false: that is, if it were shown that ethical concerns about the use of incentives are sufficient to outweigh the overriding ethical obligation to save lives when possible. Although we have deferred discussion of this latter point to another forum, we note that advocates of incentives have recently called for “pilot studies” on the grounds that these would assist 5
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in evaluating not only the efficacy of incentives, but also potential ethical concerns.33,34 Prior to any such trials, we contend that more robust incentive proposals should be presented. These should be subject to critical analysis and detailed impact assessment so that any decision to revoke the National Organ Transplant Act may be well informed and that the design of a clinical trial of incentives may be subject to rigorous scientific and ethical review before implementation. Detailed proposals specifying the mode(s) of delivery and magnitude of incentive(s) to be offered in designated populations will facilitate estimation of the likely efficacy of incentives in recruitment, the potential risks to vendor populations, and the potential impact on the existing altruistic system. The apparent simplicity of incentive proposals— merely recruit more living donors by offering payment—contrasts with the inherent complexities and costs associated with increasing the efficiency of the existing system. However, the introduction of incentives would also necessarily increase the operational and regulatory complexity of kidney transplantation and likely lead to unintended consequences.11 In conclusion, we note simply that the best-performing organ donation programs in the world currently rely on altruistic donors. Disincentives and barriers to participation in living donation and to the procurement of deceased donor organs, rather than insufficient public motivation to donate, constrain the availability of kidneys for transplantation. Financial incentives may threaten the success of established altruistic programs and ultimately lead to greater loss of lives.
ACKNOWLEDGEMENTS Both authors are members of the Declaration of Istanbul Custodian Group, and Dr Martin is co-chair of The Transplantation Society Ethics Committee. The views presented in this paper are the authors’ own and do not represent the opinions or positions of either organization. This commentary uses data from annual reports of the US Renal Data System (USRDS) and the Organ Procurement and Transplantation Network/Scientific Registry of Transplant Recipients (OPTN/SRTR; produced by the Minneapolis Medical Research Foundation and United Network for Organ Sharing under contract with HHS/HRSA). The interpretation and reporting of these data are the responsibility of the author(s) and in no way should be seen as an official policy or interpretation of the US government. We thank the 3 anonymous reviewers who provided very helpful feedback on an earlier draft of this manuscript. Support: None. Financial Disclosure: The authors declare that they have no relevant financial interests.
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