Version May 2024
INTRODUCTION — Most countries in the Western world prohibit compensated organ donation. Within the United States, the National Organ Transplant Act of 1972 states, "It shall be unlawful for any person to knowingly acquire, receive, or otherwise transfer any human organ for valuable consideration for use in human transplantation." Penalties include a fine of up to USD $50,000 and/or imprisonment for up to five years.
Although condemned by the international community, organ trafficking, transplant tourism, and commercial transplantation are likely here to stay. Patient desperation, which is driven by the disparity between organ supply and demand, finds an outlet in unregulated countries. It is important to remember that, compared with dialysis, transplantation is the best treatment for end-stage kidney disease (ESKD).
Evidence indicates that healthcare practitioners who support organ trafficking and transplant tourism often dispense substandard care. Another concern is the risk of morbidity and mortality experienced by the living donors who are preyed upon by unscrupulous centers.
This topic review will address some of the current issues affecting the international transplant community that threaten to undermine altruistic organ donation and transplantation. The discussion will include the related issues of organ trafficking, transplant tourism, and transplant commercialism (table 1).
EPIDEMIOLOGY — The actual number of transplants resulting from organ trafficking, transplant tourism, and transplant commercialism is largely unknown. Some estimate that organ trafficking may account for 5 and 10 percent of all kidney transplants [1]. In a systematic review that examined the published number of patients who purchased organs, 6002 patients were reported to travel for transplantation over a period of 42 years; of these, 1238 (21 percent) were reported to have paid for their transplants [2]. An additional unknown number of patients paid for transplants in their native countries.
Within the United States, the extent of transplant tourism was evaluated by examining United States national transplant waiting-list removals without a corresponding United States transplant recorded in the database [3]. Three hundred seventy-three foreign transplants were documented, 90 percent of which were kidneys.
Internationally, it appears that most such organs have been kidneys. One report suggested that kidney trafficking is "big business" in some of Europe's less affluent communities [4]. Another described the "mother of all scandals in human organ trafficking in India" [5]. It was estimated that up to 1500 transplants were performed and USD $31.4 million changed hands in a single center in northern India. The donors were paid approximately USD $523, with allegations of very poor postoperative care. It is thought that six such donors died, although the true number may be larger. In addition, it has been alleged that two-thirds of 2000 kidneys from transplants performed in Pakistan went to foreigners [6].
At least one model of compensated living kidney donation has been established in a regulated fashion. An Iranian model has apparently led to the elimination of their national kidney transplant waiting list [7]. Foreigners are neither permitted to undergo kidney transplantation from Iranian living donors nor are they permitted to volunteer as kidney donors for Iranian patients. In this report, 1881 kidney transplant recipients were described, all of whom were Iranian with the exception of 19 (1 percent) Afghani or Iraqi refugees, 11 (0.6 percent) other foreign nationals, and 18 (0.9 percent) Iranian immigrants.
There has been some increase in reporting of transplant tourism in the medical literature. As an example, an analysis of the Korean Network for Organ Sharing reported that a total of 2206 Korean patients underwent overseas organ transplantation (kidney transplantation, 977; liver transplantation, 1229) between 2000 and 2016 [8]. In 97 percent of overseas kidney transplantation cases and 98 percent of overseas liver transplantation cases, the transplants were performed in China. There was an inverse relationship between the annual number of deceased donors in Korea after 2006 and the number of overseas transplants.
RECIPIENT OUTCOMES — Stories of dreadful complications and poor outcomes have circulated about organ donors and recipients in unregulated countries [9-14]. A number of published single-center reports also describe poor outcomes experienced by recipients of commercial living-donor kidneys. As examples [10,14-17]:
●The outcomes of 115 patients who had been commercially transplanted in various countries and presented for follow-up care to a center in Turkey were reported [14]. Most had been transplanted in India, with smaller numbers transplanted in Iraq and Iran. At a mean follow-up of 65 months, there were numerous infections, and allograft survival was significantly worse at various time points compared with living-related transplantations performed locally. However, no difference in patient survival rates was noted.
●In a study of 10 patients with "surreptitious" overseas kidney transplantation, four experienced life-threatening infections. At a mean of two years, nine recipients were alive, and the mean serum creatinine concentration was 1.1 mg/dL (97.24 micromol/L) [16].
●In a third study of 33 kidney transplant patients who had received a kidney abroad, the one-year allograft survival was significantly lower compared with that of a matched University of California, Los Angeles (UCLA) cohort (89 versus 98 percent), while the acute rejection rate was markedly higher (30 versus 12 percent) [17]. Over one-half (17 patients) of those who had obtained a kidney abroad also had an infection.
●A study that compared records of 215 Taiwanese who received commercial cadaveric kidney transplants in China (tourism group) with those of 321 transplant recipients (domestic group) reported a higher 10-year cancer incidence in the tourism group (21.5 versus 6.8 percent, respectively) [18]. The same group provided a subsequent analysis of 307 transplant tourists compared with domestic patients between 2003 and 2009 [19]. The subjects in the tourist group were older at transplantation and had a shorter dialysis time before transplantation. There were significantly higher incidence rates of BK viruria, Pneumocystis jirovecii pneumonia, and malignancy (particularly urothelial carcinoma) in the tourist group. Graft and patient survival were superior in the domestic group.
Taken together, these reports suggest that transplant tourists have a more complex posttransplantation course, with a higher incidence of acute rejection, severe infectious complications, and malignancy [20]. The effect of transplant tourism on graft loss is not clear, since some [11,20], but not all [14,18], studies have shown acceptable graft function among transplant tourists.
Healthcare providers in regulated countries are responsible for caring for patients who have undergone surreptitious transplantation. Transplant is a treatment, not a cure, and requires long-term immunosuppression, prophylaxis, and care. Patients who receive a kidney outside of the United States are not eligible for government (Medicare or Medicaid) or pharmaceutical assistance. This can lead to enormous problems providing immunosuppression and antiviral agents when the patient returns to the United States. The fact that many patients live who have been transplanted under such circumstances is likely a reflection of the excellent care of horrendous complications that are provided after the event.
DECLARATION OF ISTANBUL — In 2004, the World Health Organization (WHO) called on member states "to take measures to protect the poorest and vulnerable groups from transplant tourism and the sale of tissues and organs, including attention to the wider problem of international trafficking in human tissues and organs." As a result, the Transplantation Society and the International Society of Nephrology held a consensus conference in Istanbul in April 2008. One hundred fifty-two participants from 78 countries attended. The result of these deliberations was the "Istanbul Declaration on Organ Trafficking and Transplant Tourism," subsequently published by a variety of high-impact-factor journals [6,21-25]. The document is divided into various sections that include a preamble, definitions, principles, and proposals, which are paraphrased in the following sections.
The Declaration of Istanbul was updated in 2019 with commentary that the strengthening of legislation addressing organ trafficking and the development of ethical programs in several countries suggest that progress has been made toward combating organ trafficking [26,27]. However, trafficking activities continue to pose a threat to both vulnerable populations and the success of transplant programs worldwide. Eradicating transplant tourism depends upon complex solutions that include efforts to progress toward self-sufficiency in transplantation.
Definitions — According to the declaration, organ trafficking was defined as "the recruitment, transport, transfer, harboring or receipt of living or deceased persons or their organs by means of the threat or use of force or other forms of coercion, of abduction, of fraud, of deception, of the abuse of power or of a position of vulnerability, or of the giving to, or the receiving by a third party of payments or benefits to achieve the transfer of control over the potential donor, for the purpose of exploitation by the removal of organs for transplantation." Transplant commercialism was defined as "a policy or practice in which an organ is treated as a commodity, including by being bought or sold or used for material gain." Travel for transplantation was defined as "the movement of organs, donors, and recipients or transplant professionals across jurisdictional borders for transplantation purposes" (table 1).
Principles — The details of the published principles are available in the source document. Briefly, these principles include the implementation of programs for preventing and treating organ failure, legislation governing organ recovery, equitable allocation, optimization of medical care of both donors and recipients, and prohibition of organ trafficking and transplant tourism. The World Health Assembly specifically called on countries to prevent the purchase and sale of human organs for transplantation by prohibiting advertising, soliciting, brokering, organ trafficking, and transplant tourism and to include penalties for such acts that encourage organ trafficking or transplant tourism.
To increase deceased organ donation, proposals included collaboration between governments and healthcare institutions to remove obstacles and disincentives; legislation to initiate donation programs and promote infrastructure development; maximization of "the therapeutic potential of deceased organ donation"; and sharing of information, expertise, and technology. To ensure the protection and safety of living donors, "the act of donation should be regarded as heroic and honored as such by representatives of the government and civil society representatives," and determination of donor suitability should be guided by the Amsterdam and Vancouver Forums.
The Istanbul group also recommended that organ donors be provided with the opportunity to participate in life and health insurance schemes. Unfortunately, being an organ donor may impact the likelihood of obtaining life, disability, and health insurance. A systematic review of the literature uncovered 23 studies between 1972 and 2006 that provided data on 2067 living organ donors, 385 potential donors, and 239 responses from insurance companies [28]. Almost all companies would provide life and health insurance to living organ donors, usually with no higher premiums. However, concern about insurability was still expressed by 2 to 14 percent of living organ donors in follow-up studies, and 3 to 11 percent of donors actually encountered difficulties with their insurance. In one study, donors whose insurance premiums increased were less likely to reaffirm their decision to donate. Based on this information, some living organ donors had difficulties with insurance despite companies reporting otherwise, a finding that has potential implications for public policy development.
Promulgation of the Declaration of Istanbul and the formation of the Declaration of Istanbul Custodian Group (DICG) have shown that strategic and collaborative actions by professionals can deliver changes [29]. Cooperation between professional organizations and relevant international, regional, and national governmental organizations has resulted in significant progress in combating organ trafficking and transplant tourism around the world.
Proposals — To increase transplantation, the Istanbul group made a number of proposals. Again, these are presented in full in the source documents. Briefly, the proposals include the following concepts:
●Governments should take appropriate action to increase living and deceased organ donation by establishing or maximizing donation practices.
●Donor suitability should adhere to the recommendations of the Amsterdam and Vancouver Forums. (See "Kidney transplantation in adults: Evaluation of the living kidney donor candidate".)
●The care of organ donors is the responsibility of jurisdictions that sanction organ trafficking, transplant commercialism, and transplant tourism.
●Provision of care includes medical and psychosocial care at the time of organ donor surgery and for the consequences related to donation.
●Cost reimbursement does not constitute payment for organ donation; it is due in part to the cost of treating the recipient.
Some of these recommendations may be at variance with United States living donation practices. As an example, living kidney donors are currently ineligible for the loss of earning reimbursement. However, such individuals are eligible for reimbursement for other expenses incurred as a consequence of organ donation (visit the National Living Donor Assistance Center website).
Most centers do not provide routine long-term medical follow-up of living donors, let alone psychosocial support in the event that their donated organ fails. However, there is much interest in developing a national living-donor registry based on longitudinal follow-up of such individuals after nephrectomy. There is no mechanism by which living donors can be provided with medical insurance beyond the resources of the individual concerned.
Joint statement: AST/ASTS — The American Society of Transplantation (AST) and American Society of Transplant Surgeons (ASTS) convened a workshop in June 2014 to explore increasing both living and deceased organ donation in the United States [30]. The joint position statement rejected transplant tourism in the strongest possible terms while acknowledging the potential in the United States for concerted action to remove all remaining financial disincentives for potential donors.
United Network for Organ Sharing — A policy proposal relating to transplantation of deceased-donor organs into nonresidents of the United States was jointly sponsored by the Organ Procurement and Transplantation Network (OPTN)/United Network for Organ Sharing (UNOS) International Relations and Ethics Committees and approved by the OPTN/UNOS Board in June 2012 [31].
The proposal followed prior acceptance by the Board of the definitions of "travel for transplantation" and "transplant tourism" and the introduction in March 2012 of revised data collection categories for transplant candidates who are neither citizens nor residents. The most important aspect of the policy concerned replacement of the previous "5 percent rule" with the review of all residency and citizenship data and the preparation of a public annual report. The policy and public data report are designed to ensure transparency and support transplant center responsibility to account for their practices. The new policy does not prohibit organ transplantation in nonresidents. Since the adoption of the policy, analysis of the first 19 months of data showed that less than 1 percent of new deceased-donor waitlist additions and less than 1 percent of transplantation recipients were non-US citizen/nonresidents candidates who traveled to the United States for purposes of transplantation.
SOCIETY GUIDELINE LINKS — Links to society and government-sponsored guidelines from selected countries and regions around the world are provided separately. (See "Society guideline links: Kidney transplantation".)
SUMMARY AND RECOMMENDATIONS
●Overview – Most countries in the Western world prohibit compensated organ donation. Despite this, organ trafficking, transplant tourism, and commercial transplantation, although condemned by the international community, are likely here to stay. (See 'Introduction' above.)
●Epidemiology – The actual number of transplants resulting from organ trafficking, transplant tourism, and transplant commercialism is largely unknown. Some estimate that organ trafficking may account for 5 and 10 percent of all kidney transplants. (See 'Epidemiology' above.)
●Recipient outcomes – Evidence suggests that adult transplant tourists have a more complex posttransplantation course, with a higher incidence of acute rejection and severe infectious complications; however, kidney function is acceptable. Similar outcomes have been reported in pediatric kidney transplant recipients. (See 'Recipient outcomes' above.)
●Declaration of Istanbul – A consensus conference in Istanbul in April 2008 resulted in the "Istanbul Declaration on Organ Trafficking and Transplant Tourism." Principles include institution of programs to prevent and treat organ failure, legislation governing organ recovery, equitable allocation, optimization of medical care of both donors and recipients, and prohibition of organ trafficking and transplant tourism. (See 'Declaration of Istanbul' above.)
Proposals from the Istanbul Conference include the following concepts:
•Governments should promote both deceased and living organ donation by establishing or maximizing donation practices.
•Donor suitability should adhere to the recommendations of the Amsterdam and Vancouver Forums.
•The care of organ donors is the responsibility of jurisdictions that sanction organ trafficking. Provision of care includes medical and psychosocial care at the time of surgery and for the consequences related to donation.
•Cost reimbursement does not constitute payment for organ donation; it is due in part to the cost of treating the recipient. (See 'Proposals' above.)
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