Secondary Listing for Deceased-Donor Kidney Transplantation Does Not Increase Likelihood of Engraftment at a Large Transplant Center
* Corresponding author: Vineeta Kumar, firstname.lastname@example.org
The supply of donor organs has not increased as fast as has the number of patients awaiting kidney transplantation. Few organs are shared outside the areas of recovery. This trend has caused some ESRD patients to seek listing at multiple centers. We examined UNOS registry data and transplant registry data at the University of Alabama at Birmingham (UAB) for the 576 patients listed at multiple centers over an 8-year span ending December 31, 2005. We identified 72 multilisted patients who received a deceased-donor renal allograft at UAB and reviewed their records for demographics, HLA matching and transfer of listing time. The only predictors for transplantation at UAB were initial listing at UAB or transfer of waiting time. Fifty-one of the 72 patients had listed at UAB first; the other 21 had transferred waiting time. None of the 176 patients who listed elsewhere first and did not transfer waiting time had been transplanted at UAB. Aggregate cost of listing and evaluation for the 176 patients listed elsewhere first who did not transfer waiting time was $1 254 528. Secondary listing at UAB, with a large cohort awaiting transplantation, without transfer of waiting time from another center was an expensive and futile process.
Transplantation is the best option for renal-replacement therapy (1). Unfortunately, in the last decade, the growth in the number of patients awaiting renal transplantation has far exceeded the increase in the number of available deceased-donor allografts (2). This fact has led some patients with end-stage renal failure to pursue transplantation at several centers connected with separate organ procurement organizations in an effort to increase the likelihood of undergoing transplantation. Persons advocating an egalitarian approach to the distribution of organs have considered this process unfair because patients with limited resources cannot afford the extra time and expense of traveling to multiple centers for evaluation of their candidacy. Nonetheless, the policies of the United Network of Organ Sharing (UNOS) have always, albeit with some reluctance, permitted potential recipients to join the waiting lists at more than one transplant center (3).
For many years, HLA matching was a more significant factor than duration of waiting time in the allocation of deceased-donor kidneys for transplantation. However, with the improvement of outcomes, due at least in part to better immunosuppressive regimens, the disadvantage of longer waiting times outweighs the advantage of a lesser HLA mismatch, particularly for African Americans (4,5). In response to the lessening impact of HLA matching on outcomes and the lengthening of waiting time, UNOS has changed the algorithm for OPO-based allocation of renal allografts to one driven more by waiting times than HLA matching. Despite this change in the allocation system, the practice of potential recipients listing at multiple centers has received only modest attention. After review of the UNOS registry data, Merion et al. concluded that, compared to patients listed at only one center, multilisted patients were younger and better educated, more commonly had private insurance and more frequently were Caucasian (6). While some patients and their personal nephrologists envision enhanced prospects for transplantation through expansion of the donor pool by listing with multiple organ procurement organizations, the purported benefit is difficult to define. In the current era that emphasizes waiting time for the allocation of organs, multiple listing appears to provide an 88% greater access to kidneys while reducing wait time by 50% (6). As a busy renal-transplant center with a large cohort of potential recipients referred from a five-state area, we reviewed our experience of engraftment of multilisted patients over an 8-year interval.
We reviewed the UNOS registry data at the Organ Procurement and Transplantation Network (OPTN) as of November 22, 2006. We determined the number of patients on the active waiting list for deceased-donor kidney transplantation at the University of Alabama at Birmingham (UAB) who were also listed at another center during the interval from January 1, 1998 to December 31, 2005. The data were without personal identifiers, except for the multilisted patients transplanted at UAB. We reviewed the records of each of the multilisted patients. If the date of listing with UNOS and date of listing at UAB with UNOS were identical, we assumed that the patient had been evaluated and listed at UAB before listing at another transplant center. If the date of first listing with UNOS was earlier than the date of evaluation at UAB or date of listing with UAB, we assumed that the patient had been listed earlier at another center. Additional information compiled during the review of medical records included demographic features, HLA matching and socioeconomic factors. The UAB Institutional Review Board approved this study.
In the 8 years prior to January 1, 2006, we wait-listed 5233 patients with UNOS for deceased-donor renal transplantation at UAB. Excluding adults listed for multiorgan transplantation and children, 576 (11%) patients wait-listed at UAB for a deceased-donor renal allograft were also listed by at least one other center. A subgroup of 325 patients had been listed first at UAB (Table 1). During the 8-year interval, 51 patients were transplanted at UAB (none of whom had transferred their wait time to another center), 115 patients were transplanted at another center and 159 patients did not undergo engraftment. A second subgroup of 251 patients had been listed first at another center. During the study interval, 21 patients in this subgroup were transplanted at UAB, 103 patients were transplanted at another center and 127 patients did not undergo engraftment. Thus, of the 576 multilisted patients, 72 (12%) underwent deceased-donor kidney transplantation at UAB during the 8-year interval (Table 1). Each patient had indicated UAB as the priority transplant center, either by primary listing (n = 51) or by transfer of waiting time (n = 21). For 17 of the 21 patients listed first at another center, we found the document for transfer of waiting time in the medical records. We contacted the remaining four patients and confirmed that each had transferred their waiting time from another center to UAB prior to transplantation. Therefore, no patient who had been listed elsewhere first and did not transfer waiting time had been transplanted at UAB in the 8-year interval. The median age of these 72 multilisted patients was 44 years (mean 43.2 years, range 19–66 years). There was a predominance of males (65%) and African Americans (58%); these demographic features were similar to those of the overall group of patients transplanted at UAB in the same interval. The span in wait–time interval ranged from less than a month to nearly 7 years (median wait time 779 days, range 24–2546 days). There was no pattern of HLA matching that predicted the likelihood of transplantation.
Table 1. Outcome for the 576 potential renal-transplant recipients at UAB who were also listed at another center from January 1, 1998 to December 31, 2005
|No. First listed at UAB|
| Center where transplanted|
| UAB|| || || 51|
| Other|| || ||115|
| None|| || ||159|
| Total|| || ||325|
|Yes. First listed at another center|
| Center where transplanted|
| UAB|| 0||21|| 21|
| Other|| 80||23||103|
| None|| 96||31||127|
Among the 325 patients who were listed first at UAB, 115 underwent kidney transplantation elsewhere. In the group of 251 patients who were listed first elsewhere and then secondarily at UAB, 103 received an allograft at a center other than UAB. Eighty of this subset had not transferred time to UAB, whereas 23 transferred time and thus reset the waiting time to zero at the outside center. Therefore, of the 576 multilisted patients, 218 patients (37.8%) received a renal allograft at a center other than UAB; this frequency was three-fold that at UAB (12.5%). In the group of 251 patients listed first at a center other than UAB, 176 patients did not transfer their waiting time to UAB. Eighty (45%) of these patients have been transplanted at another center and 96 have not yet undergone engraftment. During the 8-year interval, the Alabama Organ Procurement Center served the two transplant programs in Alabama: University of South Alabama (USA) and UAB; among the 576 multilisted patients, 86 (14%) patients were listed at USA.
The listing-fee charge to Medicare for UAB to list the 176 patients who did not transfer their waiting time was $96 272 ($547 per patient). The aggregate charge for their evaluation studies at UAB before the listings with UAB was $1 158 256. Thus, the total cost to Medicare for the secondary listing at UAB for these 176 candidates was $1 254 528.
Patients with severe chronic kidney disease seeking renal transplantation were not well served by a secondary listing at our busy center. This result is most likely due to our long waiting times. The size of our waiting list exceeds the number of deceased-donor renal allografts transplanted annually by about 18-fold. Such delays in transplantation likely apply to other centers with large waiting lists, but may not be encountered in centers with shorter waiting times. In the last few years, the number of patients requesting secondary listing at UAB has increased despite shorter expected waiting times at the primary center. Indeed, some nephrologists in our referral area have a care plan showing four or five regional transplantation programs and encourage the patients to be on the waiting list at each center. While waiting times are available on the UNOS web page, many patients and nephrologists are apparently unaware of the implications for the prospects for transplantation. Based on our findings, patients who secondarily list with centers with long expected waiting times will not improve their likelihood for renal transplantation. Indeed, the shortening of their listing time at an active center with a smaller waiting list may even delay the date of their engraftment.
While patients awaiting renal transplantation at centers with long waiting times might be transplanted more quickly at centers with shorter average waiting times, this approach to increasing access to transplantation has several important inherent barriers. Visiting other centers entails substantial inconvenience and travel expenses, particularly if the distance is several hundreds of miles. These outlays are often compounded by the costs of stays in local hotels or to the requirement for repetitive outpatient visits. Some transplant programs also require an up-front fee as much as $5000 before listing, to be used as a reserve to ensure that expensive immunosuppressive medications can be purchased once engraftment has been accomplished. Insurance coverage may vary substantially between centers. Medicaid in some states provides better coverage of expenses for in-state centers, even if out-of-state centers have better results or shorter waiting times. Furthermore, some private insurance programs restrict their coverage to transplant programs with better outcomes, regardless of geography or waiting times. Nonfinancial factors may also lead to a reluctance of personal nephrologists to send patients to some centers. These include a sense of familiarity with protocols of the nearby center and personal relationships with the transplant surgeons and nephrologists. Thus, while some internet-savvy, better educated patients with financial resources may increase the likelihood of engraftment by listing at centers with shorter waiting times, access for transplantation will not be equalized in most geographical regions. Nevertheless, centers with long waiting times should inform candidates for transplantation of the potential benefit of listing at multiple centers. This process should include centers served by separate organ procurement agencies, because listing with separate transplant programs within the same agency will have essentially no impact on the opportunity to receive an allograft.
Secondary listing at transplant centers with long expected waiting times is expensive for all participating parties. If the nil frequency of engraftment at UAB continues for the 96 patients awaiting transplantation at UAB as a secondary listing, the cost to Medicare for the 176 patients will be substantial. Ultimately, the taxpayers are responsible for these expenditures that will provide little in return. There is neither an increased number of patients transplanted nor any reason to anticipate better survival for the allograft. The process adds significant strain to already busy centers to provide administrative services, laboratory and diagnostic testing and physician/surgeon time. Furthermore, the prospective recipient must incur additional travel costs, frequently out of pocket.
In 1990, the state of New York banned multiple listing (7), but this approach had little effect on the practice, as patients went to out-of-state centers. The ban was soon dropped. Some health care advocates have favored multilisting as a means to equalize waiting times across the country; however, this effect has not been observed (6). There have been frequent changes in the kidney allocation policy of UNOS but few studies to assess the effect of these changes on the practice of multiple listing. Our findings indicate that the process of secondary listing at transplant centers with large waiting lists confers no benefit to the patient or Medicare.
We thank Katarina Anderson of the Department of Research, United Network for Organ Sharing and Wilma Marcum and Amy Spears for assistance in compiling the data.
Conflict of Interest Statement
The authors do not have any commercial associations that might pose a conflict of interest.