At the 2 transplant centers performing the largest (most) number of NC/NR deceased donor liver transplants, the quality of these liver allografts (donor age, >70 years and DCD) transplanted to NC/NR patients was not inferior to donor livers transplanted into all other recipients (Table 5).
NC/NR Waitlist Registrations
During the period of 2013 to 2016, 2806 NC/NR candidates were registered with 1149 declared as patients traveling to the United States specifically for the purpose of transplantation (TFT). Regions 5 and 9 (mainly California and New York) have the highest percentage of NC/NR candidates and transplants, representing approximately 2.5% of all candidate listings and deceased donor transplants in their respective regions. UNOS region 3 (Southeast United States inclusive of Louisiana and Florida) had the most registrations and deceased donor transplants for NC/NR-TFT candidates in 2016 (kidney, 20 registrations, 10 transplants; liver, 23 registrations; 19 transplants).
In 2016, all NC/NR patients comprised 1.3% of all waitlist additions, with the number (TFT and TFO) increasing steadily between 2013 and 2016 (Figure 1).
During the period of 2014 to 2016, there were 5 high-volume NC/NR centers that listed more than 5% of their kidney candidates as NC/NR. Three of these 5 centers overlapped with listing greater than 5% of their candidates as NC/NR and performing greater than 5% of the deceased donor kidney transplants to NC/NR patients.
During the period of 2014 to 2016, there were 7 high-volume NC/NR centers that listed more than 5% of their liver candidates as NC/NR, 6 of these 7 centers with listing more than 5% of their candidates as NC/NR and performing greater than 5% of the deceased donor liver transplants to NC/NR patients.
The majority of NC/NR patients undergoing deceased donor liver transplantation and being listed for liver transplantation are residing in a Middle East Country (Table 2).
Time to Transplantation and Waitlist Mortality for Kidney and Liver Registrants
To evaluate access for transplantation at the centers performing the most NC/NR transplants the percent of candidates who underwent organ transplantation within 1 and 3 years was compared with other centers in their respective UNOS Regions. Data were available between 2013 and 2015. Four of the 7 kidney transplant centers performing the most NC/NR transplants had a noticeably lower percentage of registrations undergoing kidney transplantation within 1 year, and 5 of 7 had a lower percentage at 3 years, when compared with their respective Region (Figure 2). There were no noticeable differences for liver registrants waiting transplantation.
The waitlist mortality was evaluated for the transplant centers performing the most NC/NR transplants between 2013 and 2015. Two kidney centers had a noticeably higher waitlist mortality within 3 years of listing for kidney transplantation, when compared with their respective UNOS Region (Figure 3). There were no observable differences for liver waitlist mortality in this period of 2013 to 2015.
NC/NR Countries of Origin
Candidates from the Gulf Countries of the Middle East, particularly Saudi Arabia and Kuwait comprised the largest number of NC/NR-TFT registrations and transplants of organs (Table 2).
In 2016, there were 36 heart, 20 lung, 100 liver and 65 kidney registrations of NC/NR added to the waitlist. The most NC/NR TFT registrations for kidney and liver combined were from Saudi Arabia (47 total; 13 kidney and 34 liver) and Kuwait (40 total; 15 kidney and 25 liver). During 2013, 2014, and 2015, 31 of 971 heart, 33 of 1468 lung, 90 of 1642 liver, and 21 of 1701 kidney transplants were performed from deceased donors to NC/NR candidates. Forty-nine percent of the NC/NR patients undergoing liver and kidney transplantation were from Saudi Arabia and Kuwait.
The largest proportion of NC/NR TFT candidates coming to the United States for deceased donor transplantation were for liver and kidney allografts; in 2016, totaling 165 registrations (100 liver and 65 kidney).
In 2016, 47 residents of Saudi Arabia (34 liver, 13 kidney) were listed for liver or kidney and 26 (21 liver, 5 kidney) received deceased donor transplant. The second highest volumes were from Kuwait with 40 listings (25 liver, 15 kidney) and 15 transplants (11 liver, 4 kidney).
The largest number of TFO was from Central America (notably Mexico). These data are presented in Table 2.
A policy of transparency has emerged from the OPTN/UNOS that fulfills a Guiding Principle by the World Health Organization (WHO) for member states to make evident a registry of organ transplants that is transparent and available to the public—as the accountable source of donor organs (both living and deceased). Such a registry should identify the relationship of the donor and recipient, the country of origin from which transplants are being performed and the survival outcome of recipients and living donors.5
The WHO has encouraged countries to achieve self-sufficiency in organ donation and transplantation providing organs for patients within their governmental jurisdiction,3,4 consistent with the Declaration of Istanbul.6 The WHO has also emphasized that the practice of organ transplantation requires this policy of transparency, maintaining public trust and to provide regularly updated data on the allocation of organs that assures their equitable distribution and an assessment of self-sufficiency performance.7,8
We performed an analysis of the data available from OPTN/UNOS for public review that has substantive limitations but accomplishes (as comprehensively possible at this time), the purpose of the OPTN/UNOS to collect such data—fulfilling the WHO transparency principle. These data have been the subject of review by the OPTN/UNOS Ad Hoc International Relations Committee who has been charged with this responsibility.
The limitations of the data available currently from UNOS are evident. The data have not been validated after the submission by transplant centers (self-reported), and the data have a categorical distinction of NC/NR undergoing transplantation by intention or purpose of travel (TFT vs TFO) that also is not validated. Our review involved the retrieval of data with inconsistent time frames of analysis of NC/NR transplants and registrations; these are the data that were accessible. Finally, we recognize that the review of waitlist mortality and time to transplantation are not precise metrics of access to transplantation, but it is a reflection of NC/NR experience at certain centers that should elicit their review of accepting NC/NR patients.
Despite these limitations, this detailed report is useful not only in deriving summary observations of the NC/NR experience and a conclusion to suggest transplant center monitoring, but also in shaping recommendations for the improvement of such analyses in the future.
There are a substantial number of NC/NR being listed and undergoing organ transplantation in the United States, irrespective of whether they travel to the US for the purpose of transplantation (TFT) or not (TFO) as evident in Tables 1 and 2. The categorical distinction of TFT versus TFO was understandably developed in its intent to distinguish those NC/NR who were residing in the United States at the time of unexpectedly developing organ failure that required transplantation. However, that categorical separation elicits skepticism with the large number of TFO undergoing transplantation and no data regarding how long they had resided in the United States before transplantation. The increasing trend of TFO as illustrated in Figure 1 also underscores our concern regarding NC/NR transplants, with a skepticism that these patients are correctly categorized. The availability of organs for NC/NR transplants in the United States is not matched by the availability of organs for US patients to undergo transplantation in NC/NR countries, especially those who have not satisfactorily or responsibly addressed their self-sufficiency for organ donation. Finally, there was no (speculated) equivalency of NC/NR transplants with the number of NC/NR deceased organ donors in the United States (Table 6).
The Declaration of Istanbul defines travel for transplantation to be transplant tourism if it involves organ trafficking and/or transplant commercialism or if the resources (organs, professionals and transplant centers) devoted to providing transplants to patients from outside a country undermine the country’s ability to provide transplant services for its own population.1 Because few countries are currently able to meet the needs of all the patients awaiting transplantation, virtually any transplants performed in individuals from other countries could fall under the definition of tourism unless there are reciprocal arrangements of providing deceased donor organs between countries, as in Eastern Europe. There are no deterrents in countries that are systematically sending their patients to the United States for deceased organ donor transplants because of inadequate programs of deceased donation in their own countries. That reality is the basis of providing the transparency evident in this report.
The percentage of organs transplanted to NC/NR annually is certainly small (<1% of the total transplants performed) for the United States to be perceived as a site of transplant tourism. Nevertheless, the waitlist registrations of NC/NR have been increasing, especially for liver transplantation (Figure 1 and Table 2). These registrations are concentrated at a few transplant centers that overlap but are not identical to the specific centers that are performing the most NC/NR organ transplants.
Noteworthy also are the data of Figure 2, which reveal kidney transplant centers whose percentage of candidates undergoing transplantation within 1 and 3 years after listing were less than other centers in their UNOS respective regions. If they are performing noticeably less transplants than other centers in the region, and have a higher rate of registrants removed from the list because of death (Figure 3), these centers should reckon with such data when contemplating the acceptance of NC/NR candidates—especially listing NC/NR from countries that have not fulfilled a WHO direction of addressing self-sufficiency and otherwise maybe denying the opportunity of transplantation for US residents.
The disproportionate percentage of waitlist registrations from countries in the Middle East that have done little to establish successful programs of deceased donation (Table 2) should be a concern for the United States and international community. There should be no cultural basis for the inadequacy of these countries to establish programs of deceased donation, especially because the governments of these countries do not object to such NC/NR patients undergoing deceased donor transplantation in the United States.
The data also make clear that the organs provided for NC/NR patients are of comparable quality to those organs transplanted to US recipients. NC/NR patients are not being disadvantaged or only assigned organs of marginal quality (Table 5). Moreover, the data also surprisingly reveal lower MELD scores for NC/NR patients at the time of transplant than for US recipients undergoing transplantation at the same center (Tables 3A, 3B and 4A, 4B).
Our analysis excludes NC/NR pediatric transplantation recognizing the inability of some countries to provide organ transplants for this patient population and the history of US transplant centers providing compassionate care for patients, irrespective of their country of origin. Between 2013 and 2015, there were 32 pediatric NC/NR heart transplants, 9 pediatric lung transplants, 62 pediatric liver transplants, and 31 pediatric kidney transplants.
The relatively large number of NC/NR patients undergoing kidney transplantation designated from Mexico (Table 2) may reflect compassionate care of undocumented individuals laboring in the United States. This report also does not address living donor NC/NR transplants in the United States, and it also has the self-reporting inadequacy of either not reporting the country of origin or the NC/NR patient listed from “other” countries of origin.
Finally, a relatively small number high-volume centers for liver7 and kidney3 transplantation would seem to require proper monitoring to assess whether these centers are soliciting NC/NR patients or have developed a systematic referral pattern for NC/NR candidates when the percentage of transplants performed exceeds 5%. We used the 5% metric to define a high-volume NC/NR center recalling the previous threshold based on the prevailing UNOS policy at the time that would have triggered a center review of such transplant activity. Such a review should include heart and lung registrations and transplants as well.
There are no sanctions that are contemplated for centers with high rates of NC/NR registrations or transplants; nevertheless, those centers will be exposed transparently to attention regarding the practices that we anticipate a responsibility of centers to address the concerns of their patient population as to the time waiting for transplantation and mortality on the list.
We commend OPTN/UNOS for collecting and providing the data to present the analysis of this report. However, the transparency of this report, when viewed with a public awareness of deceased donor organ shortages, suggests the need for a more comprehensive understanding of current NC/NR activity in the United States. Patterns of organ-specific NC/NR registrations and transplantations at high-volume centers should prompt a review of transplant center practices to determine whether the deceased donor and center resources may be compromised for their US patients.
The authors thank Eric Beeson and Sarah Taranto of UNOS Research Department for their contribution in the provision of data for this report.
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