- Email: [email protected]
Debating Organ Procurement Policy Without Illusions
Perspective Debating Organ Procurement Policy Without Illusions Benjamin Hippen, MD In this perspective, I review and critique claims that the transplant waiting list overstates the demand for kidneys and correct a few mischaracterizations of some structural barriers to increasing rates of transplantation. The solutions to the shortage of organs proffered by opponents of financial incentives fail to account for a panoply of clinical, regulatory, and financial realities of transplantation centers in the United States in ways that undermine the thesis that a trial of financial incentives for organ procurement is not warranted at this time. I conclude with some personal pessimistic reflections on the progress of this debate. Am J Kidney Dis. 66(4):577-582. 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.
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he authors of a Perspective in last month’s issue of AJKD argue that a core premise underlying arguments in favor of financial incentives for organ procurement is false, or at any rate, “rarely challenged by market opponents.”1 Specifically, the authors contend that advocates of financial incentives assume there is an extant and growing organ supply/demand disparity unable to be met by the current system of organ procurement, and that these advocates then exploit this (alleged) disparity and system failure to create a sense of urgency among clinicians and policy makers to permit a trial of financial incentives. Though not referenced, the authors go on to recapitulate many of the arguments and conclusions of the 2006 Institute of Medicine report on the organ shortage, ratifying its conclusion that a trial of financial incentives was not warranted “at this time” (Recommendation 8.1 from2). A decade later, and in the face of 20 years of discussion and concerted efforts, a general sense that the transplantation community has not exhausted conventional organ procurement strategies still remains influential, as does the conclusion that a trial of incentives is (still) not justified. In this article, I argue that the authors misinterpret waitlist data, incompletely account for other evidence of “unseen” demand for organs, and fail to account for extant clinical, regulatory, and financial realities that govern dialysis facilities and transplantation centers in ways that undermine their theses. Regardless of whether a trial of financial incentives is morally defensible or even capable of garnering broad moral support, further debates over the shortage of organs and the success of organ procurement strategies should proceed free of illusions and rooted in current clinical, regulatory, and financial realities.
MEASURING DEMAND The Waiting List—The Seen The authors worry that the magnitude of need represented by the waiting list may overstate the true Am J Kidney Dis. 2015;66(4):577-582
demand for organs, highlighting the observation that one-third of the patients added to the waiting list are listed as inactive (hereafter “status 7”) within a week of listing. Historically, candidates were listed as status 7 for a variety of reasons, the salient one being that accrued time on the waiting list was the chief means of achieving priority. In regions where median waiting times to transplantation were more than 5 years for some blood groups, a delay in listing until remediable barriers to candidacy were surmounted put candidates at an unjustifiable disadvantage. This use of status 7 listing is just a feature of how transplantation centers strategically coped with the long waiting times associated with the organ shortage. In support of their thesis, the authors relate results of a few studies that showed that 50% of status 7 candidates became active within 12 months of listing, one-third remained inactive, and 40% of those who died on the inactive list did so within 2 years of listing, implying that these patients were not candidates to begin with. From these data, they conclude that the waiting list “may therefore result in overstatement of the gap between supply and effective demand for kidneys....”1 A closer examination of the data indicates otherwise. Approximately 10,500 candidates were listed as status 7 in 2012, of whom 5,250 became active within 12 months of listing and one-third (w3,100) remained inactive.
From Metrolina Nephrology Associates, PA, and The Carolinas Medical Center, Charlotte, NC. Received March 21, 2015. Accepted in revised form May 1, 2015. Originally published online June 19, 2015. Address correspondence to Benjamin Hippen, MD, Metrolina Nephrology Associates, PA, and The Carolinas Medical Center, 2711 Randolph Rd, Bldg 400, Charlotte, NC 28207. E-mail: [email protected] 2015 by the National Kidney Foundation, Inc. 0272-6386 http://dx.doi.org/10.1053/j.ajkd.2015.05.013 577
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Which is to say that in 2012, a total of 57,903 candidates were listed as active and another 5,250 candidates listed as status 7 became active within 12 months, a total of about 63,000 candidates. From the observation that 3,100 candidates listed as status 7 in the same time frame remained inactive at 24 months and may not have been viable candidates at all, the authors conclude that the demand for transplantable kidneys “may” be overstated, but the data they cite put that overstatement of demand at a mere 5%. In 2008, the same trend was represented in a respected newspaper of record as a 30% overstatement of organ demand, replete with baseless charges of false advertising leveled against the transplantation community by media-favored bioethicists.3 However, there is a different reason why the waiting list will become a less reliable surrogate for demand: A key change in the US kidney allocation system4 implemented in January 2015 will change when patients are listed for a transplant. The salient change involves shifting how candidate waiting time is calculated from the date of listing (old system) to the date of end-stage renal disease (ESRD) on the Centers for Medicare & Medicaid (CMS) 2728 form. This means that a candidate with 5 years of ESRD who is listed will immediately accrue 5 “points,” and so on. This change renders obsolete the old use of status 7 to accrue waiting time. Now, status 7 listing only confers an advantage to those listed pre-ESRD, a small proportion of new referrals. In 2011, only 12.4% of all patients received a deceased donor transplant within 1 year of initiating dialysis therapy.5 A key component of sound waitlist management is ensuring that listed candidates are evaluated on a regular basis and that screening tests are up to date. With few exceptions (patients who are young or who have high calculated panel-reactive antibody), candidates who come to the list with very little ESRD time are very unlikely to receive an organ offer from a deceased donor until they accrue enough points (read: waiting time) to near the top of the list. Candidates with less ESRD time will be competing on a rolling basis with newly referred candidates with many years of ESRD, who once listed will immediately jump ahead of those with less ESRD time in the queue. From a transplantation center perspective, if a candidate with little ESRD time does not have an available living donor, it is poor stewardship to expend the time and resources to even evaluate and list the candidate. Because candidates with fewer points will not get offers, listing them early in their ESRD course will mean their testing would have to be repeated over multiple years. Instead, rational centers will likely delay evaluation until the candidate identifies a living donor or accrues enough ESRD time to approach the top of the list, ensuring that testing is current and not unnecessarily redundant. Putting off the evaluation of candidates until they 578
accrue sufficient points will contract the size of the active waiting list, which will appear to show an overall reduction in the demand for kidneys. However, in actuality, there is no overall reduction in demand, only the demand that is seen as a number on the waiting list, a false and misleading perception that is just an artifact of the current listing process and allocation system. Many otherwise viable transplant candidates whose evaluations are put off, perhaps for years, will simply join the ranks of the unseen.6 Prevalent Kidney Disease and the Unseen Behind the cohort of listed candidates are legions of patients who appear on no lists, and the benefit they might derive from transplantation and the loss they experience by being deprived of transplantation are largely unappreciated. Schold et al7 estimated that there are between 80,000 and 130,000 additional patients with ESRD who have an “overlapping risk profile” with listed transplant candidates, but who are never referred, a number that could conceivably double the current waiting list for kidneys. Also, the study by Schold et al7 did not include the potential transplant candidates among the much larger group of those who are projected to develop chronic kidney disease stage 4 or worse in their lifetimes (9%-11% and 16%-18% of the white and African American US population, respectively).8 Were even a fraction of the patients in these groups added to the list without proportionate growth in the number of available organs, median waiting times for deceased donor kidneys would exceed the expected life span of all but the heartiest of candidates, and with physiologic toll on the survivors. However, being unseen, these patients do not “count”; if they did, the inadequacies of current organ procurement regimens in the United States would be even more conspicuous, and the need for reforms, even more pressing. As a moral asterisk to the focus on first-world problems, a recent study published in Lancet conservatively estimated that in 2010, more than 2.3 million people worldwide who clinically warranted renal replacement therapy did not receive it,9 which in countries lacking health care resources amounts to a lack of access to transplantation. Even if meaningful solutions to the organ shortage that can garner broad moral support are lacking, perhaps the least we can do is acknowledge the reality of the plight of the seen and the unseen who bear the true costs of inadequate organ procurement strategies.
STRUCTURAL BARRIERS TO TRANSPLANTATION In their AJKD Perspective, the authors list a series of structural barriers facing these unseen patients, but draw unfounded conclusions. Two are worth examining in detail. Am J Kidney Dis. 2015;66(4):577-582
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“Financial Disincentives at the Dialysis Facility Level” The authors repeat an argument that enjoys currency in the transplantation community,10 namely that dialysis facilities have a powerful pecuniary interest in not referring patients for transplantation. However, this is a misunderstanding of the extant regulatory obligations and finances of dialysis facilities, a correct understanding of which supports the opposite conclusion. Patient education regarding transplantation as a therapeutic option and documentation of an evaluation of transplantation candidacy for each patient at a dialysis facility is a requirement of the CMS Conditions for Coverage (see11; {494.70 and {494.80). Dialysis facilities that fail to perform and document this activity risk regulatory jeopardy. For poor patients, the primary payor for dialysis is Medicare, Medicaid, or some hybrid, unless they are ineligible for these programs. The profit margins of dialysis facilities with an average payor mix of Medicare, Medicaid, and commercial insurance is 3% to 4%.12 Crucially, a facility composed entirely of patients with Medicare and/or Medicaid as the primary payor is financially unsustainable because payments to facilities on a per-treatment basis are, depending on local labor and other overhead costs to the facility, frequently less than the cost to the facility to provide the treatment. Although a dialysis facility requires a minimum number of patients to cover labor and operational overhead costs, the total net margin of a typical facility is achieved through cross-subsidization from collections from commercially insured patients. The import of all this is that patients whose primary payor is either Medicare or Medicaid, once referred and (probably many years later) having undergone transplantation, would not affect the net margin of a dialysis facility with an average payor mix. Furthermore, the financial landscape for facilities is about to change dramatically. A 9.5% cut in ESRD Medicare reimbursement, phased in annually through 2018, is already ensconced in federal legislation.12 Recalling that the average facility margin with an average payor mix is 3% to 4%, this cut means that serving patients with Medicare as the primary payor will become even less financially sustainable in the future and will require further cross-subsidization from commercially insured patients, regardless of a facility’s for-profit or not-for-profit status. If these cuts are realized, a center that has to more aggressively cross-subsidize the cost of care for most of its patients will be better off financially if more of these patients successfully undergo transplantation. Impecuniosity and Patient Access The authors argue that “without separate reforms to address the underlying bases of these access disparities, suitable candidates currently unable to access the Am J Kidney Dis. 2015;66(4):577-582
waiting list would be unlikely to benefit from the introduction of financial incentives (or other strategies to increase donor rates).”1 To be sure, if patients are unable to afford the costs of transplantation (immunosuppressants and posttransplantation visits/testing), increasing the number of available organs will be of little help. However, the proper comparison for the cost of financial incentives for organ procurement is the cost of providing maintenance dialysis. Therefore, unlike any other strategy to increase organ procurement rates, a comprehensive set of financial incentives that successfully increases the number of transplantable kidneys from living donors and that also covers the cost of transplantation, immunosuppression, and donor and recipient aftercare makes obvious financial sense to state-based and commercial payors compared to covering the costs associated with maintenance dialysis.13
STOP WASTING KIDNEYS! A staple of opponents of financial incentives is that incentive proposals would not even bear consideration if transplantation professionals would just stop wasting perfectly good kidneys. Citing a 19% rate of organ discard in the United States, the authors argue that if only we biopsied more kidneys before turndown, made more use of organs with a Kidney Donor Profile Index . 85% (previously known as expanded criteria donors), and increased use rates of organ donation after circulatory death just like many European centers, we would be a long way toward solving the problem. These arguments betray a lack of understanding of the extant regulatory burdens and financial constraints on US transplantation centers. In the United States, the expected risk-adjusted rate of death-uncensored transplant survival for a deceased donor kidney at 1 year is 96% (14; Fig 6.2), and 1-year expected patient survival is 98% to 99%. These outcomes represent the expectations of transplantation centers by CMS regulators, and failure to achieve these outcomes invites intense regulatory scrutiny under threat of involuntary closure.15 In the last several years, nearly 100 transplantation programs in the United States have gone through expensive stressful “mitigating factors” applications with CMS to avoid involuntary closure because of reported outcomes that were below riskadjusted expected outcomes, although the data and veracity of the methodology used to calculate risk adjustment has been heavily criticized.16 With some frequency, scrutinized centers are required to enter into a Systems Improvement Agreement, essentially a contract with CMS to put oversight of the transplantation program into a multiyear third-party receivership, at extravagant expense to the transplantation center, until reported outcomes improve. Regulatory scrutiny of programs that fall below expected outcomes is typically accompanied by denial 579
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of Center of Excellence status by CMS. Loss of this designation often causes commercial insurers to cancel insurance contracts and direct referrals to other programs. This is a profound incentive to embrace risk aversion.16,17 Refashioning insurance agreements and changing ingrained referral patterns is a slow process and can pose significant medium-term challenges to the financial stability of a transplantation program long after the quality issues have been resolved to a regulator’s satisfaction. Bearing this daunting regulatory reality in mind, consider the European experience with organs from donation after cardiac death (DCD) donors, which is highlighted by opponents of financial incentivization as exemplary of what the US centers should be doing. Reporting on 2,343 kidneys from controlled-DCD donors from 2000 to 2008, Dominguez-Gil et al18 reported a primary nonfunction rate of 5%, a delayed transplant function rate of 50%, and 1-year death-uncensored transplant survival of 85.1%. As the most recent Organ Procurement and Transplantation Network/Scientific Registry of Transplant Recipients report on kidney transplantation outcomes shows, the rate in the United States of primary nonfunction with kidneys from DCD donors decreased from just .6% in 2003 to just .2% in 2013 (14; Fig 6.1). Ostensibly this trend would suggest improvements in the ability to successfully transplant kidneys from DCD donors, but it is not an accident that the rate of decline in rates of primary nonfunction corresponds to a leveling off of the rate of DCD kidney procurement at 15% of all deceased donor organs over the last few years (14; Fig 4.5). This flattening is indicative of deliberate cherry-picking and precautionary principle behavior.19,20 A US program that accepted DCD organs conferring the degree of risk reported from Europe and reported similar outcomes would have to make an existential choice: either risk accepting many DCD kidneys in order to achieve .85% one-year transplant survival in that donor cohort or accept nearly none. Using the European outcomes data, for every failed DCD kidney at 1 year, a center would have to successfully manage an additional 7 DCD kidneys to 1-year death-uncensored transplant survival (death with transplant function counts as a transplant failure) and have no other patient deaths or transplant failures that year or risk regulatory scrutiny and accompanying vicissitudes. At a medium-volume program, a single extra death or transplant failure can be the tipping point. The flattening of organ use rates from deceased donors is the operationalization of risk aversion in organ acceptance behaviors, in rational response to costly regulatory sanctions if a center chooses incorrectly. Furthermore, the current structure of reimbursement for transplantation does not adequately cover the 580
costs of expected posttransplantation complications in high-risk transplants. Researchers at the University of Michigan reported that delayed transplant function alone (reported in 50% and 40% of DCD kidneys in the European Union18 and United States13 experience, respectively) results in a net loss to the transplantation center of $4,937 per case, and extended criteria donor kidneys resulted in a net loss of $5,887 per case.21 As public and private payers move away from fee for service to paying for population health management, for which capitation and cost containment is becoming the norm, there is no indication that in the near future, transplantation centers will be paid more for higher-risk transplantations and be relieved from the need to shift costs from commercial payers to cover the costs of transplants with higher complication rates. Commentators removed from these pressures might aver that this is but one more structural barrier that requires reform, but this is an evasion, on par with the phrase “more study is needed.” Moralized exhortations to “stop wasting kidneys,” uninformed by the clinical, regulatory, and financial realities governing the practice of transplantation in the United States, are unhelpful.
A CODA ON THE PROMISE OF FINANCIAL INCENTIVES Much ink has been spilled on the defensibility of financial incentives and interested readers can read and judge for themselves comprehensively argued briefs for financial incentives for organ procurement,22-27 consensus recommendations for a pilot trial,28 a canvassing of the data and arguments surrounding crowding-out concerns,29 or the vagaries of the Iranian system,30,31 just as a start. I conclude with a few points. The shortage of kidneys has long been with us. Too many patients with kidney disease will never have the benefits of transplantation in our current “successful” system, and their existence is barely acknowledged in the literature. Many of them are poor, live in a state of precarity, and are of minority race or ethnicity, and their plight causes insomnia for (too) few. There is no shortage of meetings, public debates, consensus statements, position papers, custodial groups, press releases, point-counterpoints, and op-eds. An embedded ethnographer at a meeting to address the shortage can count on enthusiastic endorsements of margin-tweaking practice changes and imperatives for further study, with the promise to meet again and maybe publish a paper. To take a recent example, we all should hope that the Consensus Conference on Best Practices in Live Kidney Donation,32 endorsed by the authors as a means of reducing financial disincentives to living donation, is successful because it is beneath argument that past and current living Am J Kidney Dis. 2015;66(4):577-582
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donors should not experience financial penalty for giving the gift of life. However, there is little evidence that reducing financial disincentives will increase rates of living donation. While the emerging moral consensus around eliminating disincentives is heartening,33 it strikes me as just the latest in a series of well-intentioned but largely ineffectual policy improvisations over the last 2 decades. Conceivably, I and those who share my perspective are wrong, and the opponents of a pilot trial of financial incentives are correct that a trial of financial incentives is just morally indefensible on its face. If so, perhaps we might all be spared another round of enthusiasms that pin the hopes of a dramatic improvement in organ procurement on the work of another task force, promising tangibly different results from the litany of similar that have been conducted in the last 2 decades, the wages of which have yielded, after a brief increase, flat rates of deceased donor organ procurement and flat-tofalling rates of living organ donation. Instead, perhaps we can be honest with ourselves and one another that the organ shortage is simply a tragedy that our society has not been able to solve in a manner that most of our citizens can morally abide, the real costs of which are disproportionately borne by the unseen, who are often also those most vulnerable and least capable of bearing them. If so, rather than succumb to despair, this may be the opportune occasion for transplantation physicians and surgeons to refocus on older professional virtues such as Humean sympathy34 and equanimity,35 to ameliorate suffering borne of a system problem that admits of no workable solution.
ACKNOWLEDGEMENTS This article includes data collected by the Scientific Registry of Transplant Recipients and the Organ Procurement and Transplantation Network. The interpretation and reporting of these data are the responsibility of the author and in no way should be seen as an official policy or interpretation of the US government. I thank Arthur Matas, MD, and Lisa Rasmussen, PhD, for comments on the manuscript. Errors of fact, reasoning, and interpretation are mine alone. Support: None. Financial Disclosure: The author declares that he has no relevant financial interests.
REFERENCES 1. Martin DE, White SL. Financial incentives for living kidney donors: are they necessary? [published online ahead of print June 6, 2015]. Am J Kidney Dis. 2015;65(6):826-832. 2. Childress JF, Liverman CT. Organ Donation: Opportunities for Action. Washington, DC: National Academies Press; 2006. https://www.iom.edu/Reports/2006/Organ-Donation-Opportunitiesfor-Action.aspx. Accessed March 15, 2015. 3. Stein R. A third of patients on transplant lists are not eligible. Washington Post. March 22, 2008. http://www.washingtonpost.
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com/wp-dyn/content/article/2008/03/21/AR2008032102981.html? sid5ST2011022308018. Accessed March 15, 2015. 4. Organ Procurement and Transplantation Network (OPTN) Policy 8: Allocation of Kidneys. http://optn.transplant.hrsa.gov/ ContentDocuments/OPTN_Policies.pdf#nameddest5Policy_08. Accessed March 15, 2015. 5. US Renal Data System. Table E5.2: Percent of patients either wait-listed or receiving a deceased-donor kidney within one year of ESRD initiation. In: USRDS 2014 Annual Data Report. http://www.usrds.org/reference.aspx. Accessed March 15, 2015. 6. Bastiat F. That which is seen, and that which is not seen. 1850. http://bastiat.org/en/twisatwins.html. Accessed March 15, 2015. 7. Schold JD, Srinivas TR, Kayler LK, Meier-Kriesche HU. The overlapping risk profile between dialysis patients listed and not listed for renal transplantation. Am J Transplant. 2008;8(1):58-68. 8. Grams ME, Chow EKH, Segev DL, Coresh J. Lifetime incidence of CKD stages 3-5 in the United States. Am J Kidney Dis. 2013;62(2):245-252. 9. Liyanage T, Ninomiya T, Jha V, et al. Worldwide access to treatment for end-stage kidney disease: a systematic review [published online ahead of print March 13, 2015]. Lancet. http:// dx.doi.org/10.1016/S0140-6736(14)61601-9. http://www.thelancet. com/pdfs/journals/lancet/PIIS0140-6736(14)61601-9.pdf Accessed March 15, 2015. 10. Zhang Y, Thamer M, Kshirsagar O, et al. Dialysis chains and placement on the waiting list for a cadaveric kidney transplant. Transplantation. 2014;98(5):543-551. 11. Department of Health and Human Services. Conditions for coverage for end-stage renal disease facilities. Federal Register. Part 494: April 15, 2008. https://www.cms.gov/Regulations-andGuidance/Legislation/CFCsAndCoPs/downloads/esrdfinalrule0415. pdf. Accessed March 15, 2015. 12. Wish D, Johnson D, Wish J. Rebasing the Medicare payment for dialysis: rationale, challenges, and opportunities. Clin J Am Soc Nephrol. 2014;9(12):2195-2202. 13. Matas AJ, Schnitzler M. Payment for living donor (vendor) kidneys: a cost-effectiveness analysis. Am J Transplant. 2003;4(2): 216-221. 14. Matas AJ, Smith JM, Skeans MA, et al. OPTN/SRTR 2013 Annual Data Report: Kidney. Am J Transplant. 2015;15(2):1-34. 15. Hawryluk M. Transplant center pull back to avoid sanctions. The Bulletin. January 3, 2014. http://www.bendbulletin.com/ health/organtransplants/1371249-151/transplant-centers-pullback-to-avoid-sanctions. Accessed March 15, 2015. 16. Abecassis MM, Burke R, Klintmalm GB, et al. American Society of Transplant Surgeons: transplant center outcomes requirements—a threat to innovation. Am J Transplant. 2009;9(6): 1279-1286. 17. Schold JD, Arrington CJ, Levine G. Significant alterations in reported clinical practice associated with increased oversight of organ transplant center performance. Prog Transplant. 2010;20(3):279-287. 18. 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. 19. Hawryluk M. Transplantable organs go to waste. The Bulletin. January 3, 2014. http://www.bendbulletin.com/health/ organtransplants/1375026-151/transplantable-organs-go-to-waste. Accessed March 15, 2015. 20. VanWagner LB, Skaro AI. Program-specific reports: implications and impact on program behavior. Curr Opin Organ Transplant. 2013;18(2):210-215. http://www.ncbi.nlm.nih.gov/ pmc/articles/PMC3725805/#R19. Accessed March 15, 2015.
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Benjamin Hippen 21. Englesbe MJ, Ads Y, Cohn JA, et al. The effects of donor and recipient practices on transplant center finances. Am J Transplant. 2008;8(3):586-592. 22. Hippen BE. In defense of a regulated market in kidneys from living vendors. J Med Philos. 2005;30(6):593-626. 23. Satel S, ed. When Altruism Isn’t Enough: The Case for Compensating Kidney Donors. Washington, DC: AEI Press; 2008. 24. Taylor JS. Stakes and Kidneys: Why Markets in Human Body Parts Are Morally Imperative. Hampshire, England: Ashgate Pub Ltd; 2005. 25. Cherry MJ. Kidney for Sale by Owner: Human Organs, Transplantation and the Market. Washington, DC: Georgetown University Press; 2005. 26. Goodwin M. Black Markets: The Supply and Demand of Body Parts. Cambridge: Cambridge University Press; 2006. 27. Beard TR, Leitzel J. Designing a compensated-kidney donation system. Law Contemporary Problems. 2014;77(3):253-288. 28. Working Group on Incentives for Living Donation. Incentives for organ donation: proposed standards for an internationally acceptable system. Am J Transplant. 2012;12(2):306-312. 29. Hippen BE, Satel S. Crowding out, crowding in and financial incentives for organ procurement. In: Satel S, ed. When
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Altruism Isn’t Enough: The Case for Compensating Kidney Donors. Washington, DC: AEI Press; 2008:96-110. 30. Hippen BE. Organ sales and moral travails: lessons from the living kidney vendor program in Iran. Cato Policy Analysis No 614. March 20, 2008. http://www.cato.org/publications/policyanalysis/organ-sales-moral-travails-lessons-living-kidney-vendorprogram-iran. Accessed March 15, 2015. 31. Mahdavi-Mazdeh M. The Iranian model of living renal transplantation. Kidney Int. 2012;82(6):627-634. 32. 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. http://onlinelibrary.wiley.com/enhanced/doi/ 10.1111/ajt.13173/. Accessed March 15, 2015. 33. Delmonico FD, Danovitch GM, Capron AM, et al. An open letter to HHS Secretary Burwell on ethically increasing organ donation. Transplantation Direct. 2015;1(1):1-19. 34. Gregory J. Lectures on the Duties and Qualifications of a Physician. Philadelphia: M. Carey & Son; 1817. 35. Osler W. Aequanimitas. In: Aequanimitas, With Other Addresses to Medical Students, Nurses, and Practitioners of Medicine. 3rd ed. New York: McGraw-Hill, Inc; 1932:1-12.
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T
he authors of a Perspective in last month’s issue of AJKD argue that a core premise underlying arguments in favor of financial incentives for organ procurement is false, or at any rate, “rarely challenged by market opponents.”1 Specifically, the authors contend that advocates of financial incentives assume there is an extant and growing organ supply/demand disparity unable to be met by the current system of organ procurement, and that these advocates then exploit this (alleged) disparity and system failure to create a sense of urgency among clinicians and policy makers to permit a trial of financial incentives. Though not referenced, the authors go on to recapitulate many of the arguments and conclusions of the 2006 Institute of Medicine report on the organ shortage, ratifying its conclusion that a trial of financial incentives was not warranted “at this time” (Recommendation 8.1 from2). A decade later, and in the face of 20 years of discussion and concerted efforts, a general sense that the transplantation community has not exhausted conventional organ procurement strategies still remains influential, as does the conclusion that a trial of incentives is (still) not justified. In this article, I argue that the authors misinterpret waitlist data, incompletely account for other evidence of “unseen” demand for organs, and fail to account for extant clinical, regulatory, and financial realities that govern dialysis facilities and transplantation centers in ways that undermine their theses. Regardless of whether a trial of financial incentives is morally defensible or even capable of garnering broad moral support, further debates over the shortage of organs and the success of organ procurement strategies should proceed free of illusions and rooted in current clinical, regulatory, and financial realities.
MEASURING DEMAND The Waiting List—The Seen The authors worry that the magnitude of need represented by the waiting list may overstate the true Am J Kidney Dis. 2015;66(4):577-582
demand for organs, highlighting the observation that one-third of the patients added to the waiting list are listed as inactive (hereafter “status 7”) within a week of listing. Historically, candidates were listed as status 7 for a variety of reasons, the salient one being that accrued time on the waiting list was the chief means of achieving priority. In regions where median waiting times to transplantation were more than 5 years for some blood groups, a delay in listing until remediable barriers to candidacy were surmounted put candidates at an unjustifiable disadvantage. This use of status 7 listing is just a feature of how transplantation centers strategically coped with the long waiting times associated with the organ shortage. In support of their thesis, the authors relate results of a few studies that showed that 50% of status 7 candidates became active within 12 months of listing, one-third remained inactive, and 40% of those who died on the inactive list did so within 2 years of listing, implying that these patients were not candidates to begin with. From these data, they conclude that the waiting list “may therefore result in overstatement of the gap between supply and effective demand for kidneys....”1 A closer examination of the data indicates otherwise. Approximately 10,500 candidates were listed as status 7 in 2012, of whom 5,250 became active within 12 months of listing and one-third (w3,100) remained inactive.
From Metrolina Nephrology Associates, PA, and The Carolinas Medical Center, Charlotte, NC. Received March 21, 2015. Accepted in revised form May 1, 2015. Originally published online June 19, 2015. Address correspondence to Benjamin Hippen, MD, Metrolina Nephrology Associates, PA, and The Carolinas Medical Center, 2711 Randolph Rd, Bldg 400, Charlotte, NC 28207. E-mail: [email protected] 2015 by the National Kidney Foundation, Inc. 0272-6386 http://dx.doi.org/10.1053/j.ajkd.2015.05.013 577
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Which is to say that in 2012, a total of 57,903 candidates were listed as active and another 5,250 candidates listed as status 7 became active within 12 months, a total of about 63,000 candidates. From the observation that 3,100 candidates listed as status 7 in the same time frame remained inactive at 24 months and may not have been viable candidates at all, the authors conclude that the demand for transplantable kidneys “may” be overstated, but the data they cite put that overstatement of demand at a mere 5%. In 2008, the same trend was represented in a respected newspaper of record as a 30% overstatement of organ demand, replete with baseless charges of false advertising leveled against the transplantation community by media-favored bioethicists.3 However, there is a different reason why the waiting list will become a less reliable surrogate for demand: A key change in the US kidney allocation system4 implemented in January 2015 will change when patients are listed for a transplant. The salient change involves shifting how candidate waiting time is calculated from the date of listing (old system) to the date of end-stage renal disease (ESRD) on the Centers for Medicare & Medicaid (CMS) 2728 form. This means that a candidate with 5 years of ESRD who is listed will immediately accrue 5 “points,” and so on. This change renders obsolete the old use of status 7 to accrue waiting time. Now, status 7 listing only confers an advantage to those listed pre-ESRD, a small proportion of new referrals. In 2011, only 12.4% of all patients received a deceased donor transplant within 1 year of initiating dialysis therapy.5 A key component of sound waitlist management is ensuring that listed candidates are evaluated on a regular basis and that screening tests are up to date. With few exceptions (patients who are young or who have high calculated panel-reactive antibody), candidates who come to the list with very little ESRD time are very unlikely to receive an organ offer from a deceased donor until they accrue enough points (read: waiting time) to near the top of the list. Candidates with less ESRD time will be competing on a rolling basis with newly referred candidates with many years of ESRD, who once listed will immediately jump ahead of those with less ESRD time in the queue. From a transplantation center perspective, if a candidate with little ESRD time does not have an available living donor, it is poor stewardship to expend the time and resources to even evaluate and list the candidate. Because candidates with fewer points will not get offers, listing them early in their ESRD course will mean their testing would have to be repeated over multiple years. Instead, rational centers will likely delay evaluation until the candidate identifies a living donor or accrues enough ESRD time to approach the top of the list, ensuring that testing is current and not unnecessarily redundant. Putting off the evaluation of candidates until they 578
accrue sufficient points will contract the size of the active waiting list, which will appear to show an overall reduction in the demand for kidneys. However, in actuality, there is no overall reduction in demand, only the demand that is seen as a number on the waiting list, a false and misleading perception that is just an artifact of the current listing process and allocation system. Many otherwise viable transplant candidates whose evaluations are put off, perhaps for years, will simply join the ranks of the unseen.6 Prevalent Kidney Disease and the Unseen Behind the cohort of listed candidates are legions of patients who appear on no lists, and the benefit they might derive from transplantation and the loss they experience by being deprived of transplantation are largely unappreciated. Schold et al7 estimated that there are between 80,000 and 130,000 additional patients with ESRD who have an “overlapping risk profile” with listed transplant candidates, but who are never referred, a number that could conceivably double the current waiting list for kidneys. Also, the study by Schold et al7 did not include the potential transplant candidates among the much larger group of those who are projected to develop chronic kidney disease stage 4 or worse in their lifetimes (9%-11% and 16%-18% of the white and African American US population, respectively).8 Were even a fraction of the patients in these groups added to the list without proportionate growth in the number of available organs, median waiting times for deceased donor kidneys would exceed the expected life span of all but the heartiest of candidates, and with physiologic toll on the survivors. However, being unseen, these patients do not “count”; if they did, the inadequacies of current organ procurement regimens in the United States would be even more conspicuous, and the need for reforms, even more pressing. As a moral asterisk to the focus on first-world problems, a recent study published in Lancet conservatively estimated that in 2010, more than 2.3 million people worldwide who clinically warranted renal replacement therapy did not receive it,9 which in countries lacking health care resources amounts to a lack of access to transplantation. Even if meaningful solutions to the organ shortage that can garner broad moral support are lacking, perhaps the least we can do is acknowledge the reality of the plight of the seen and the unseen who bear the true costs of inadequate organ procurement strategies.
STRUCTURAL BARRIERS TO TRANSPLANTATION In their AJKD Perspective, the authors list a series of structural barriers facing these unseen patients, but draw unfounded conclusions. Two are worth examining in detail. Am J Kidney Dis. 2015;66(4):577-582
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“Financial Disincentives at the Dialysis Facility Level” The authors repeat an argument that enjoys currency in the transplantation community,10 namely that dialysis facilities have a powerful pecuniary interest in not referring patients for transplantation. However, this is a misunderstanding of the extant regulatory obligations and finances of dialysis facilities, a correct understanding of which supports the opposite conclusion. Patient education regarding transplantation as a therapeutic option and documentation of an evaluation of transplantation candidacy for each patient at a dialysis facility is a requirement of the CMS Conditions for Coverage (see11; {494.70 and {494.80). Dialysis facilities that fail to perform and document this activity risk regulatory jeopardy. For poor patients, the primary payor for dialysis is Medicare, Medicaid, or some hybrid, unless they are ineligible for these programs. The profit margins of dialysis facilities with an average payor mix of Medicare, Medicaid, and commercial insurance is 3% to 4%.12 Crucially, a facility composed entirely of patients with Medicare and/or Medicaid as the primary payor is financially unsustainable because payments to facilities on a per-treatment basis are, depending on local labor and other overhead costs to the facility, frequently less than the cost to the facility to provide the treatment. Although a dialysis facility requires a minimum number of patients to cover labor and operational overhead costs, the total net margin of a typical facility is achieved through cross-subsidization from collections from commercially insured patients. The import of all this is that patients whose primary payor is either Medicare or Medicaid, once referred and (probably many years later) having undergone transplantation, would not affect the net margin of a dialysis facility with an average payor mix. Furthermore, the financial landscape for facilities is about to change dramatically. A 9.5% cut in ESRD Medicare reimbursement, phased in annually through 2018, is already ensconced in federal legislation.12 Recalling that the average facility margin with an average payor mix is 3% to 4%, this cut means that serving patients with Medicare as the primary payor will become even less financially sustainable in the future and will require further cross-subsidization from commercially insured patients, regardless of a facility’s for-profit or not-for-profit status. If these cuts are realized, a center that has to more aggressively cross-subsidize the cost of care for most of its patients will be better off financially if more of these patients successfully undergo transplantation. Impecuniosity and Patient Access The authors argue that “without separate reforms to address the underlying bases of these access disparities, suitable candidates currently unable to access the Am J Kidney Dis. 2015;66(4):577-582
waiting list would be unlikely to benefit from the introduction of financial incentives (or other strategies to increase donor rates).”1 To be sure, if patients are unable to afford the costs of transplantation (immunosuppressants and posttransplantation visits/testing), increasing the number of available organs will be of little help. However, the proper comparison for the cost of financial incentives for organ procurement is the cost of providing maintenance dialysis. Therefore, unlike any other strategy to increase organ procurement rates, a comprehensive set of financial incentives that successfully increases the number of transplantable kidneys from living donors and that also covers the cost of transplantation, immunosuppression, and donor and recipient aftercare makes obvious financial sense to state-based and commercial payors compared to covering the costs associated with maintenance dialysis.13
STOP WASTING KIDNEYS! A staple of opponents of financial incentives is that incentive proposals would not even bear consideration if transplantation professionals would just stop wasting perfectly good kidneys. Citing a 19% rate of organ discard in the United States, the authors argue that if only we biopsied more kidneys before turndown, made more use of organs with a Kidney Donor Profile Index . 85% (previously known as expanded criteria donors), and increased use rates of organ donation after circulatory death just like many European centers, we would be a long way toward solving the problem. These arguments betray a lack of understanding of the extant regulatory burdens and financial constraints on US transplantation centers. In the United States, the expected risk-adjusted rate of death-uncensored transplant survival for a deceased donor kidney at 1 year is 96% (14; Fig 6.2), and 1-year expected patient survival is 98% to 99%. These outcomes represent the expectations of transplantation centers by CMS regulators, and failure to achieve these outcomes invites intense regulatory scrutiny under threat of involuntary closure.15 In the last several years, nearly 100 transplantation programs in the United States have gone through expensive stressful “mitigating factors” applications with CMS to avoid involuntary closure because of reported outcomes that were below riskadjusted expected outcomes, although the data and veracity of the methodology used to calculate risk adjustment has been heavily criticized.16 With some frequency, scrutinized centers are required to enter into a Systems Improvement Agreement, essentially a contract with CMS to put oversight of the transplantation program into a multiyear third-party receivership, at extravagant expense to the transplantation center, until reported outcomes improve. Regulatory scrutiny of programs that fall below expected outcomes is typically accompanied by denial 579
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of Center of Excellence status by CMS. Loss of this designation often causes commercial insurers to cancel insurance contracts and direct referrals to other programs. This is a profound incentive to embrace risk aversion.16,17 Refashioning insurance agreements and changing ingrained referral patterns is a slow process and can pose significant medium-term challenges to the financial stability of a transplantation program long after the quality issues have been resolved to a regulator’s satisfaction. Bearing this daunting regulatory reality in mind, consider the European experience with organs from donation after cardiac death (DCD) donors, which is highlighted by opponents of financial incentivization as exemplary of what the US centers should be doing. Reporting on 2,343 kidneys from controlled-DCD donors from 2000 to 2008, Dominguez-Gil et al18 reported a primary nonfunction rate of 5%, a delayed transplant function rate of 50%, and 1-year death-uncensored transplant survival of 85.1%. As the most recent Organ Procurement and Transplantation Network/Scientific Registry of Transplant Recipients report on kidney transplantation outcomes shows, the rate in the United States of primary nonfunction with kidneys from DCD donors decreased from just .6% in 2003 to just .2% in 2013 (14; Fig 6.1). Ostensibly this trend would suggest improvements in the ability to successfully transplant kidneys from DCD donors, but it is not an accident that the rate of decline in rates of primary nonfunction corresponds to a leveling off of the rate of DCD kidney procurement at 15% of all deceased donor organs over the last few years (14; Fig 4.5). This flattening is indicative of deliberate cherry-picking and precautionary principle behavior.19,20 A US program that accepted DCD organs conferring the degree of risk reported from Europe and reported similar outcomes would have to make an existential choice: either risk accepting many DCD kidneys in order to achieve .85% one-year transplant survival in that donor cohort or accept nearly none. Using the European outcomes data, for every failed DCD kidney at 1 year, a center would have to successfully manage an additional 7 DCD kidneys to 1-year death-uncensored transplant survival (death with transplant function counts as a transplant failure) and have no other patient deaths or transplant failures that year or risk regulatory scrutiny and accompanying vicissitudes. At a medium-volume program, a single extra death or transplant failure can be the tipping point. The flattening of organ use rates from deceased donors is the operationalization of risk aversion in organ acceptance behaviors, in rational response to costly regulatory sanctions if a center chooses incorrectly. Furthermore, the current structure of reimbursement for transplantation does not adequately cover the 580
costs of expected posttransplantation complications in high-risk transplants. Researchers at the University of Michigan reported that delayed transplant function alone (reported in 50% and 40% of DCD kidneys in the European Union18 and United States13 experience, respectively) results in a net loss to the transplantation center of $4,937 per case, and extended criteria donor kidneys resulted in a net loss of $5,887 per case.21 As public and private payers move away from fee for service to paying for population health management, for which capitation and cost containment is becoming the norm, there is no indication that in the near future, transplantation centers will be paid more for higher-risk transplantations and be relieved from the need to shift costs from commercial payers to cover the costs of transplants with higher complication rates. Commentators removed from these pressures might aver that this is but one more structural barrier that requires reform, but this is an evasion, on par with the phrase “more study is needed.” Moralized exhortations to “stop wasting kidneys,” uninformed by the clinical, regulatory, and financial realities governing the practice of transplantation in the United States, are unhelpful.
A CODA ON THE PROMISE OF FINANCIAL INCENTIVES Much ink has been spilled on the defensibility of financial incentives and interested readers can read and judge for themselves comprehensively argued briefs for financial incentives for organ procurement,22-27 consensus recommendations for a pilot trial,28 a canvassing of the data and arguments surrounding crowding-out concerns,29 or the vagaries of the Iranian system,30,31 just as a start. I conclude with a few points. The shortage of kidneys has long been with us. Too many patients with kidney disease will never have the benefits of transplantation in our current “successful” system, and their existence is barely acknowledged in the literature. Many of them are poor, live in a state of precarity, and are of minority race or ethnicity, and their plight causes insomnia for (too) few. There is no shortage of meetings, public debates, consensus statements, position papers, custodial groups, press releases, point-counterpoints, and op-eds. An embedded ethnographer at a meeting to address the shortage can count on enthusiastic endorsements of margin-tweaking practice changes and imperatives for further study, with the promise to meet again and maybe publish a paper. To take a recent example, we all should hope that the Consensus Conference on Best Practices in Live Kidney Donation,32 endorsed by the authors as a means of reducing financial disincentives to living donation, is successful because it is beneath argument that past and current living Am J Kidney Dis. 2015;66(4):577-582
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donors should not experience financial penalty for giving the gift of life. However, there is little evidence that reducing financial disincentives will increase rates of living donation. While the emerging moral consensus around eliminating disincentives is heartening,33 it strikes me as just the latest in a series of well-intentioned but largely ineffectual policy improvisations over the last 2 decades. Conceivably, I and those who share my perspective are wrong, and the opponents of a pilot trial of financial incentives are correct that a trial of financial incentives is just morally indefensible on its face. If so, perhaps we might all be spared another round of enthusiasms that pin the hopes of a dramatic improvement in organ procurement on the work of another task force, promising tangibly different results from the litany of similar that have been conducted in the last 2 decades, the wages of which have yielded, after a brief increase, flat rates of deceased donor organ procurement and flat-tofalling rates of living organ donation. Instead, perhaps we can be honest with ourselves and one another that the organ shortage is simply a tragedy that our society has not been able to solve in a manner that most of our citizens can morally abide, the real costs of which are disproportionately borne by the unseen, who are often also those most vulnerable and least capable of bearing them. If so, rather than succumb to despair, this may be the opportune occasion for transplantation physicians and surgeons to refocus on older professional virtues such as Humean sympathy34 and equanimity,35 to ameliorate suffering borne of a system problem that admits of no workable solution.
ACKNOWLEDGEMENTS This article includes data collected by the Scientific Registry of Transplant Recipients and the Organ Procurement and Transplantation Network. The interpretation and reporting of these data are the responsibility of the author and in no way should be seen as an official policy or interpretation of the US government. I thank Arthur Matas, MD, and Lisa Rasmussen, PhD, for comments on the manuscript. Errors of fact, reasoning, and interpretation are mine alone. Support: None. Financial Disclosure: The author declares that he has no relevant financial interests.
REFERENCES 1. Martin DE, White SL. Financial incentives for living kidney donors: are they necessary? [published online ahead of print June 6, 2015]. Am J Kidney Dis. 2015;65(6):826-832. 2. Childress JF, Liverman CT. Organ Donation: Opportunities for Action. Washington, DC: National Academies Press; 2006. https://www.iom.edu/Reports/2006/Organ-Donation-Opportunitiesfor-Action.aspx. Accessed March 15, 2015. 3. Stein R. A third of patients on transplant lists are not eligible. Washington Post. March 22, 2008. http://www.washingtonpost.
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com/wp-dyn/content/article/2008/03/21/AR2008032102981.html? sid5ST2011022308018. Accessed March 15, 2015. 4. Organ Procurement and Transplantation Network (OPTN) Policy 8: Allocation of Kidneys. http://optn.transplant.hrsa.gov/ ContentDocuments/OPTN_Policies.pdf#nameddest5Policy_08. Accessed March 15, 2015. 5. US Renal Data System. Table E5.2: Percent of patients either wait-listed or receiving a deceased-donor kidney within one year of ESRD initiation. In: USRDS 2014 Annual Data Report. http://www.usrds.org/reference.aspx. Accessed March 15, 2015. 6. Bastiat F. That which is seen, and that which is not seen. 1850. http://bastiat.org/en/twisatwins.html. Accessed March 15, 2015. 7. Schold JD, Srinivas TR, Kayler LK, Meier-Kriesche HU. The overlapping risk profile between dialysis patients listed and not listed for renal transplantation. Am J Transplant. 2008;8(1):58-68. 8. Grams ME, Chow EKH, Segev DL, Coresh J. Lifetime incidence of CKD stages 3-5 in the United States. Am J Kidney Dis. 2013;62(2):245-252. 9. Liyanage T, Ninomiya T, Jha V, et al. Worldwide access to treatment for end-stage kidney disease: a systematic review [published online ahead of print March 13, 2015]. Lancet. http:// dx.doi.org/10.1016/S0140-6736(14)61601-9. http://www.thelancet. com/pdfs/journals/lancet/PIIS0140-6736(14)61601-9.pdf Accessed March 15, 2015. 10. Zhang Y, Thamer M, Kshirsagar O, et al. Dialysis chains and placement on the waiting list for a cadaveric kidney transplant. Transplantation. 2014;98(5):543-551. 11. Department of Health and Human Services. Conditions for coverage for end-stage renal disease facilities. Federal Register. Part 494: April 15, 2008. https://www.cms.gov/Regulations-andGuidance/Legislation/CFCsAndCoPs/downloads/esrdfinalrule0415. pdf. Accessed March 15, 2015. 12. Wish D, Johnson D, Wish J. Rebasing the Medicare payment for dialysis: rationale, challenges, and opportunities. Clin J Am Soc Nephrol. 2014;9(12):2195-2202. 13. Matas AJ, Schnitzler M. Payment for living donor (vendor) kidneys: a cost-effectiveness analysis. Am J Transplant. 2003;4(2): 216-221. 14. Matas AJ, Smith JM, Skeans MA, et al. OPTN/SRTR 2013 Annual Data Report: Kidney. Am J Transplant. 2015;15(2):1-34. 15. Hawryluk M. Transplant center pull back to avoid sanctions. The Bulletin. January 3, 2014. http://www.bendbulletin.com/ health/organtransplants/1371249-151/transplant-centers-pullback-to-avoid-sanctions. Accessed March 15, 2015. 16. Abecassis MM, Burke R, Klintmalm GB, et al. American Society of Transplant Surgeons: transplant center outcomes requirements—a threat to innovation. Am J Transplant. 2009;9(6): 1279-1286. 17. Schold JD, Arrington CJ, Levine G. Significant alterations in reported clinical practice associated with increased oversight of organ transplant center performance. Prog Transplant. 2010;20(3):279-287. 18. 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. 19. Hawryluk M. Transplantable organs go to waste. The Bulletin. January 3, 2014. http://www.bendbulletin.com/health/ organtransplants/1375026-151/transplantable-organs-go-to-waste. Accessed March 15, 2015. 20. VanWagner LB, Skaro AI. Program-specific reports: implications and impact on program behavior. Curr Opin Organ Transplant. 2013;18(2):210-215. http://www.ncbi.nlm.nih.gov/ pmc/articles/PMC3725805/#R19. Accessed March 15, 2015.
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Benjamin Hippen 21. Englesbe MJ, Ads Y, Cohn JA, et al. The effects of donor and recipient practices on transplant center finances. Am J Transplant. 2008;8(3):586-592. 22. Hippen BE. In defense of a regulated market in kidneys from living vendors. J Med Philos. 2005;30(6):593-626. 23. Satel S, ed. When Altruism Isn’t Enough: The Case for Compensating Kidney Donors. Washington, DC: AEI Press; 2008. 24. Taylor JS. Stakes and Kidneys: Why Markets in Human Body Parts Are Morally Imperative. Hampshire, England: Ashgate Pub Ltd; 2005. 25. Cherry MJ. Kidney for Sale by Owner: Human Organs, Transplantation and the Market. Washington, DC: Georgetown University Press; 2005. 26. Goodwin M. Black Markets: The Supply and Demand of Body Parts. Cambridge: Cambridge University Press; 2006. 27. Beard TR, Leitzel J. Designing a compensated-kidney donation system. Law Contemporary Problems. 2014;77(3):253-288. 28. Working Group on Incentives for Living Donation. Incentives for organ donation: proposed standards for an internationally acceptable system. Am J Transplant. 2012;12(2):306-312. 29. Hippen BE, Satel S. Crowding out, crowding in and financial incentives for organ procurement. In: Satel S, ed. When
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Altruism Isn’t Enough: The Case for Compensating Kidney Donors. Washington, DC: AEI Press; 2008:96-110. 30. Hippen BE. Organ sales and moral travails: lessons from the living kidney vendor program in Iran. Cato Policy Analysis No 614. March 20, 2008. http://www.cato.org/publications/policyanalysis/organ-sales-moral-travails-lessons-living-kidney-vendorprogram-iran. Accessed March 15, 2015. 31. Mahdavi-Mazdeh M. The Iranian model of living renal transplantation. Kidney Int. 2012;82(6):627-634. 32. 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. http://onlinelibrary.wiley.com/enhanced/doi/ 10.1111/ajt.13173/. Accessed March 15, 2015. 33. Delmonico FD, Danovitch GM, Capron AM, et al. An open letter to HHS Secretary Burwell on ethically increasing organ donation. Transplantation Direct. 2015;1(1):1-19. 34. Gregory J. Lectures on the Duties and Qualifications of a Physician. Philadelphia: M. Carey & Son; 1817. 35. Osler W. Aequanimitas. In: Aequanimitas, With Other Addresses to Medical Students, Nurses, and Practitioners of Medicine. 3rd ed. New York: McGraw-Hill, Inc; 1932:1-12.
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