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Keywords:

  • Ethics;
  • HIV;
  • organ donation;
  • transplant

Abstract

  1. Top of page
  2. Abstract
  3. Background
  4. Sizing Up the Opportunity: Estimates of the Potential Number of Organs From HIV+ Individuals
  5. Ethical Considerations
  6. Legal and Operational Barriers to Promoting HIV+ Organ Donation and Transplantation
  7. Future Opportunities
  8. Acknowledgments
  9. Disclosures
  10. References

Case reports of kidney transplantation using HIV-positive (HIV+) donors in South Africa and advances in the clinical care of HIV+ transplant recipients have drawn attention to the legal prohibition of transplanting organs from HIV+ donors in the United States. For HIV+ transplant candidates, who face high barriers to transplant access, this prohibition violates beneficence by placing an unjustified limitation on the organ supply. However, transplanting HIV+ organs raises nonmaleficence concerns given limited data on recipient outcomes. Informed consent and careful monitoring of outcome data should mitigate these concerns, even in the rare circumstance when an HIV+ organ is intentionally transplanted into an HIV-negative recipient. For potential donors, the federal ban on transplanting HIV+ organs raises justice concerns. While in practice there are a number of medical criteria that preclude organ donation, only HIV+ status is singled out as a mandated exclusion to donation under the National Organ Transplant Act (NOTA). Operational objections could be addressed by adapting existing approaches used for organ donors with hepatitis. Center-specific outcomes should be adjusted for HIV donor and recipient status. In summary, transplant professionals should advocate for eliminating the ban on HIV+ organ donation and funding studies to determine outcomes after transplantation of these organs.


Abbreviations
ESRD

end-stage renal disease

HCV

hepatitis C virus

HIVRN

HIV Research Network

IRB

Institutional Review Board

KTR

kidney transplant recipient

NIS

Nationwide Inpatient Sample

NOTA

National Organ Transplant Act

OPO

organ procurement organizations

OPTN

Organ Procurement and Transplantation Network

UNOS

United Network of Organ Sharing.

Background

  1. Top of page
  2. Abstract
  3. Background
  4. Sizing Up the Opportunity: Estimates of the Potential Number of Organs From HIV+ Individuals
  5. Ethical Considerations
  6. Legal and Operational Barriers to Promoting HIV+ Organ Donation and Transplantation
  7. Future Opportunities
  8. Acknowledgments
  9. Disclosures
  10. References

HIV+ Americans with end-stage organ disease die each year despite estimates suggesting that hundreds of organs could be donated by HIV+ individuals with severe brain-injury. However, the transplantation of HIV+ donor organs has been barred since 1988 under an amendment to NOTA [1]. This federal statutory prohibition was promulgated in the context of legislation that placed diverse restrictions on HIV+ individuals and communities considered at risk for contracting the disease, including travel and immigration limitations. Since that time, however, advances in clinical care for HIV+ patients, rising waiting times and reports about transplantation using HIV+ kidneys in South Africa create new urgency to reconsider whether the ban on HIV+ organ donation in the United States is justified [2].

Organ transplantation for HIV+ kidney and liver recipients from non-HIV infected donors has shown good short-term outcomes and allayed ethical concerns about whether the risks of transplant outweighed benefits. The main concerns were that HIV+ recipients would be harmed by opportunistic infections or malignancies, and that poor transplant outcomes would waste the common resource of donated organs [3]. Stock et al. assembled a prospective cohort of 150 HIV+ kidney transplant recipients (KTRs) and reported survival rates of 94.6% and 88.2% at 1 and 3 years, respectively, similar to outcomes among non-HIV infected KTRs in national registry data. Graft-survival rates were 90.4% and 73.7% respectively, which were similar to those of higher-risk KTRs [4]. Similarly, a meta-analysis of 15 studies reporting outcomes after liver transplantation for 686 HIV+ patients showed a 12-month survival rate of 84.5%, which is comparable to rates among HIV-negative patients [5]. Notably, concerns about a high risk of opportunistic infections posttransplant have not manifested during medium-term follow-up of these cohorts.

Case reports from transplant centers inside and outside the United States have described positive outcomes among HIV+ heart, lung and kidney-pancreas transplant recipients of organs from HIV-negative donors [6-9]. It is plausible that carefully selected HIV+ patients with severe liver or thoracic disease could benefit from receiving an HIV+ organ versus waiting an uncertain duration for an HIV-negative organ. The risk-benefit analysis of accepting an organ from an HIV+ donor would differ for each type of organ.

An accurate needs assessment for organ transplantation among HIV+ patients is hindered by limited data, legal obstacles to reporting HIV status and disparities in access to the waiting list. A total of 198 organ transplants among HIV+ individuals were reported in 2011 [8]. However, because the Organ Procurement and Transplantation Network (OPTN) does not collect data on HIV infection among wait-listed candidates, and some states prohibit the reporting of HIV status, the actual number of HIV+ patients who received a transplant or who are on the waiting list is unknown. HIV infection is associated with elevated mortality rates for end-stage renal disease (ESRD) patients on dialysis and for patients listed for liver transplant [10, 11]. Unfortunately, HIV+ patients with ESRD face the same lack of available organs for transplant as other patients, but also confront their own unique barriers [10]. In a 2009 single center study, Sawinski et al. [12] reported that after initial transplant eligibility approval, only 20% of HIV+ patients were later activated on the kidney transplant waiting list versus 73% of HIV-negative patients. Some centers also require disclosure of a transplant candidate's HIV status to a potential living donor. The ethical justification is that the donor should know that the recipient's outcome may be worse and integrate that information into the donation decision [13]. However, in a single-center study by Rodrigue et al., only 36% of HIV+ respondents reported willingness to share their HIV status even if it meant they could get a live-donor kidney. HIV+ transplant candidates also had lower levels of knowledge about live donor kidney transplantation compared to HIV-negative candidates [14]. Collectively, these findings show challenging barriers to transplant for HIV patients, while restrictions on reporting HIV status make it extremely difficult to ascertain the number of HIV+ patients who would benefit from transplant or who have received a transplant in the United States.

Promising case reports of kidney transplantation involving HIV+ donors and recipients in South Africa suggest that concerns regarding the transplantation of HIV+ organs into HIV+ recipients should be reevaluated. HIV-associated nephropathy is the leading cause of ESRD in South Africa, the country with the world's largest population of people with HIV and limited resources to support dialysis [15]. Muller et al. reported outcomes from 14 HIV+ recipients in Cape Town [2, 16]. Before transplantation, the recipients had stable CD4 counts and viral loads, no opportunistic infections, and were on anti-retroviral therapy. Six to 12 months posttransplant, CD4 counts remained stable, viral loads undetectable, and for most patients, renal function was good [2]. The generalizability of these outcomes to the United States, where the prevalence of resistant HIV strains is higher (one study from the Centers from Disease Control estimated that 19% of new HIV infections are with virus resistant to at least one class of anti-retroviral therapies) yet resources to treat resistant HIV are greater, is unknown [17].

Sizing Up the Opportunity: Estimates of the Potential Number of Organs From HIV+ Individuals

  1. Top of page
  2. Abstract
  3. Background
  4. Sizing Up the Opportunity: Estimates of the Potential Number of Organs From HIV+ Individuals
  5. Ethical Considerations
  6. Legal and Operational Barriers to Promoting HIV+ Organ Donation and Transplantation
  7. Future Opportunities
  8. Acknowledgments
  9. Disclosures
  10. References

Enthusiasm for HIV+ organ donation may depend on the size of the potential organ pool. This pool consists of organs from donors who die of causes unrelated to their HIV infection, but also of organs currently being discarded due to false positive serologic testing for HIV in the donor. Currently available FDA approved NAT assays have false positive rates between 0.1% and 0.85% [18]. Boyarsky et al. aimed to quantify the number of potentially eligible HIV+ donors using three sources—the Nationwide Inpatient Sample (NIS), the HIV Research Network (HIVRN), and the OPTN/United Network of Organ Sharing (UNOS)—and used these data to extrapolate the potential number of donors nationwide. The authors estimated that 534 potential HIV+ deceased organ donors would be available per year using NIS data and 494 donors using HIVRN data. This group also reviewed OPTN records related to referrals of potential deceased donors and estimated that approximately 20 potential deceased donors per year are determined to have HIV infection that was not anticipated until medical screening for donation was undertaken [19].

Furthermore, allowing transplantation of organs from HIV+ donors might reduce the discard of organs due to false positive results from viral antibody and nucleic acid testing. Although limited data quantify the number of lost organs due to unconfirmed testing for HIV [20], it is plausible that some centers would be willing to accept high quality organs with possible HIV infection—particularly for their HIV+ candidates.

Ethical Considerations

  1. Top of page
  2. Abstract
  3. Background
  4. Sizing Up the Opportunity: Estimates of the Potential Number of Organs From HIV+ Individuals
  5. Ethical Considerations
  6. Legal and Operational Barriers to Promoting HIV+ Organ Donation and Transplantation
  7. Future Opportunities
  8. Acknowledgments
  9. Disclosures
  10. References

As shown in Table 1, the interests of HIV+ transplant candidates require that their clinicians balance the duties of beneficence and nonmaleficence [21]. The ever-growing disparity between the number of donated organs and the number of wait-listed patients has created an ethical imperative for transplant clinicians to seek novel methods of expanding transplant access. The duty of beneficence toward HIV+ wait-listed patients, particularly those individuals whose health is worsening on the waiting list, provides a strong rationale for the transplant community to advocate for repealing the ban on HIV+ organ donation and funding studies to determine outcomes with this practice. Notably, HIV+ patients would have access to organs donated by HIV-negative as well as HIV+ donors. Permitting HIV+ organ donation may particularly benefit African Americans, who are disproportionately impacted by HIV/AIDS and face persistent disparities in access to renal transplantation [22, 23]. HIV nephropathy is a disease that almost exclusively affects African Americans [24]. Indeed, of the 150 HIV+ KTRs in the Stock et al. [4] study, 69% were African American. It is likely that the majority of donated HIV+ kidneys would be transplanted into African American recipients.

Table 1. Ethical considerations in allowing HIV+ individuals to donate organs
PrincipleContextImplication
For transplant candidates
BeneficenceThe demand for transplant coupled with the lack of organs requires that the transplant community seek ways expand access to transplantTransplant providers should advocate to allow transplantation using organs from donors with HIV or initial HIV+ serologies
NonmaleficenceTransplant with an HIV+ organ could cause diverse complicationsInformed consent should be obtained prospectively at wait-listing and again at transplant. The practice should take place at experienced centers in an observational study to carefully assess outcomes
For donors
JusticeHIV+ individuals face unique stigma related to unique historical and legal context of HIV infection in the USTreating HIV similarly to other transmissible diseases such as HCV will reduce stigma and make HIV regulation less exceptional

The potential to harm transplant recipients through HIV transmission nonetheless remains a fundamental concern. Infecting an HIV+ recipient with a new strain of HIV could lead to uncontrolled viral replication, immune dysregulation, and opportunistic infections. An important dimension of the nonmaleficence concern is whether transplantation of HIV+ organs into HIV-negative recipients should be ethically acceptable under any circumstance. Indeed, such practice would run counter to extensive public health efforts to minimize HIV transmission and could also put intimate partners of an organ recipient at risk. We acknowledge that HIV+ to HIV-negative transplantation would be appropriate only in rare cases where the risks of transmitting HIV infection are clearly outweighed by the risks of continuing to wait for a transplant and with the recipient's informed consent. This scenario may exist when a candidate's medical urgency for transplant is so severe that the risks of waiting include imminent death.

Allowing HIV+ organs into the general organ supply will require significant efforts to ensure systems are in place to prevent accidental transmission into the wrong recipient. Such operational considerations can, however, be addressed through improvements to the current system. The potential for harm and the possibilities for treatment of an anticipated transmission with HIV+ to HIV-negative transplant are in some ways analogous to existing circumstances involving recipients of organs from donors who have known hepatitis C virus (HCV) or other serious infections.

If transplantation with HIV+ donor organs proceeds, important challenges related to the selection of HIV+ donors, the processes of recipient informed consent and clinical management must be addressed. The risk of accepting these organs is likely to exist along a spectrum corresponding to the characteristics of the particular strain of virus and the donor's HIV-related history. However, the medical workup of organ donors is time-limited. For example, transplant and organ procurement organization (OPO) teams will not have time to ascertain HIV genotype or other relevant features of HIV infection (such as history of opportunistic infections) for many donors. In addition, recipients of HIV+ kidneys—and perhaps other organs—may suffer elevated rates of organ rejection. Table 2 categorizes these challenges.

Table 2. Medical considerations that affect recipient risk
Management concernContextImplication
Risk-stratification of HIV+ donorsSome HIV+ donors will have viral resistance based on genotype mutations. Characterization of viral resistance will often be infeasible prior to organ procurementInitially, HIV+ donor organs should be accepted only under the lowest risk scenarios, e.g. among donors with well-controlled, nonresistant virus. Ideally documentation of genotypic testing should be obtained to confirm lack of resistance. Informed consent of the recipient should include discussion of the potential for acquisition of resistant HIV
 HIV+ donors will present at various stages of infection. Some HIV+ donors will have a history of opportunistic infection or reduced CD4 counts. Characterization of opportunistic infection history will often be infeasible however CD4 counts may be available as a surrogate marker for opportunistic infection riskThe risk of exposing the recipient to an opportunistic infection transmitted from the donor will be low, but present. This risk should be addressed during informed consent
 Some HIV+ donors will have coexisting infection with HCVHIV/HCV coinfection in a donor will be likely to increase the risk of poor recipient outcomes, including death. Until greater experience using organs from HIV+ donors provides guidance about effective management, transplant centers should not use organs from coinfected donors
Organ rejectionHIV+ organ recipients are at elevated risk of organ rejectionHIV+ to HIV+ organ donation may lead to even higher rates of acute rejection and, by extension, higher risk of organ failure. This risk should be addressed during informed consent
Viral impairment of organ functionHIV can injure organs such as kidneys (e.g. chronic kidney disease through HIV associated nephropathy [HIVAN])Transplant candidates with a history of HIV-related organ dysfunction, such as kidney transplant candidates with HIVAN, should be informed that accepting an HIV+ organ may lead to recurrent organ impairment
Unintended HIV+ organ transplantation into HIV-negative recipientsThe procurement of organs from donors with transmissible diseases such as HIV creates the small risk that these organs will misallocated and lead to unintended infection of seronegative recipientsClinicians and OPO staff will have a duty to ensure carefully developed, redundant precautions are taken to ensure that organs from HIV+ donors are allocated correctly
Medication side effects and interactionsAntiretroviral therapy is associated with diverse, challenging side effects. Many anti-retroviral medications (e.g. protease inhibitors) also interact with calcineurin inhibitors, raising the risk of out-of-range calcineurin trough levelsTransplant candidates considering these organs should be educated about the potential need for changes in their antiretroviral regimen and side effects

Given these risks, transplantation using HIV+ organs should first take place using organs from donors with well-controlled HIV and no history of opportunistic infections [25]. Ideally, the first HIV+ donors accepted would have had stable and well-characterized HIV infection for a substantial period prior to brain injury, so that transplant teams could obtain important information on the donor virus, such as historical genotype patterns and current viral load. These restricted criteria for HIV+ donors could be relaxed over time if outcomes among recipients were favorable, and/or better antiretroviral therapies became available.

Transplantation using organs from HIV+ donors should proceed in the context of well-resourced studies in which relevant outcomes including quality of life are collected with Institutional Review Board (IRB) oversight. When analyzing risks, IRB's should contrast the risk of transplantation using HIV+ organs with outcomes if candidates remained on the waiting list, rather than with transplant outcomes for recipients of non-HIV+ organs. Nonmaleficence concerns should also be addressed with the processes of informed consent and restriction of the use of HIV+ organs, at least initially, to experienced centers. Patients should be prospectively consented for HIV+ organ transplant eligibility while on the waiting list (similar to existing practice for transplantation with HCV+ organs), with candid discussion about the lack of outcome data for KTRs outside of South Africa. Through adaptation of existing disease transmission protocols, the OPTN will also need to investigate and confirm possible unintended transmission of HIV into recipients through allocation errors.

Eliminating the prohibition on transplanting HIV+ organs could have a positive impact on donors as well. The ethical analysis for donors is not, however, as simple as increasing the HIV+ donor's ability to exercise autonomy over disposition of organs after death. While any adult has the right to register as an organ donor, whether donation occurs is always subject to medical screening (to ensure viable organ function and reduce the risk of transmissions), logistical considerations, and the ability to find a suitable match. The Uniform Anatomical Gift Act recognizes these considerations by granting adults the right to make an anatomical gift for the purposes of transplant, while granting the recipient of the intended gift the right to accept or reject it [26]. Thus, the law recognizes the autonomy rights of donors and the autonomy rights of transplant candidates. Accordingly, HIV+ adults can authorize organ donation, but OPOs are currently prohibited from recovering those organs for transplant.

The primary ethical benefit for donors by eliminating the ban on recovering HIV+ organs for transplant relates to the principle of justice commonly understood as the fair distribution of benefits. The federal ban raises justice concerns because it singles out HIV+ status as the only medical criterion listed as an absolute ban to donation for transplant. Although other criteria are considered contraindications, such as certain cancers, none are codified in NOTA or enumerated in the implementing regulations [1]. Precluding the option of using HIV+ organs for transplant arbitrarily excludes the HIV+ population from the psychological benefit that accrues from knowing one might become a donor after death. This prohibition also impacts the families of HIV+ individuals given that donor families gain psychological relief that the donor's death helped others [27]. Allowing transplant using HIV+ organs can serve as an important example of abandoning the paradigm of placing unique restrictions around the conduct and care of individuals with HIV [28].

Legal and Operational Barriers to Promoting HIV+ Organ Donation and Transplantation

  1. Top of page
  2. Abstract
  3. Background
  4. Sizing Up the Opportunity: Estimates of the Potential Number of Organs From HIV+ Individuals
  5. Ethical Considerations
  6. Legal and Operational Barriers to Promoting HIV+ Organ Donation and Transplantation
  7. Future Opportunities
  8. Acknowledgments
  9. Disclosures
  10. References

The prohibition on recovering HIV+ organs for transplant is imbedded in three layers of federal law and regulation: NOTA at 42 USC 640, its implementing regulations known as the “final rule” at 42 CFR 121.6(b), and OPTN/UNOS policy on Screening Potential Organ Donors at Policy 2.2.3.3 [1, 29]. The first step to removing these barriers would be federal legislation to amend §628(2)(C) of NOTA. This provision currently requires OPOs to “arrange for the acquisition and preservation of donated organs … including arranging for testing with respect to preventing the acquisition of organs that are infected with the etiological agent for acquired immune deficiency syndrome [1]”.

There are several possible legislative pathways forward. NOTA could be amended to eliminate any reference to HIV. In the implementing regulations, the US Secretary of Health and Human Services would then determine the requirements for testing and use of HIV+ organs. This approach would allow for future flexibility as clinical management of HIV+ organ donation and transplantation evolves. An alternative option would be to amend the existing language to clarify that HIV+ organs may be recovered and transplanted only into HIV+ recipients. The regulations and/or OPTN policy could establish clinical criteria and informed consent standards for transplanting HIV+ organs. Indeed, the American Society of Transplantation, the American Society of Transplant Surgeons and a consortium of patient advocacy groups supported federal legislation to this effect (the HIV Organ Policy Equity Act) which was introduced in the Senate in February 2013 [30].

Some states have laws related to HIV+ organ donation and transplant that would need amendment to avoid issues of federal preemption. Illinois, for example, enacted a law in 2004 allowing the transplant of HIV+ organs [31]. Without a variance from the federal regulators, however, this attempt to use HIV+ organs for HIV+ recipients was largely thwarted. At the time Illinois passed the law, the most serious concern raised related to safety and ensuring that HIV+ organs were segregated from the general organ pool and allocated to the correct recipients [32]. Implementing such a system would require new OPTN policies and programming for the national computer database that matches donors to recipients. This task seems feasible given the current system that matches donor organs with the appropriate recipients based on medical criteria—such as ABO blood type—that carry substantial clinical risks if done incorrectly.

For health professionals, the use of HIV+ organs for transplantation creates additional concerns including the risks of infection during surgery and effects on center outcomes. Universal precautions around the handling of tissues and bodily fluids afford reasonable protection against needle sticks or other unanticipated exposure to HIV. Organ transplantation with HCV+ donors serves as an example of how viral positive-to-positive transplant can expand the organ pool without undue burdens to health providers [33, 34]. The use of HCV+ organs has enabled HCV+ renal transplant candidates to shorten waiting time and to improve survival compared to waiting longer for an HCV-negative organ [34]. However, given the substantial differences between HIV and HCV infection, and the unknown magnitude of risk associated with HIV+ organs, health professionals should continue to have discretion to select appropriate organs based on the specific risk/benefit analysis for each patient.

If HIV+ organs are transplanted, clinical complications such as infections and rejection are likely to worsen transplant center outcomes. Posttransplant survival rates are publicly reported for all transplant centers [35]. Poor outcomes can lead to audits by OPTN and CMS, loss of patient referrals or closure of the transplant program [36]. Risk adjustment models only include a limited number of relevant donor and recipient attributes—leading to a perception that these outcome reports act as a disincentive to innovation [36]. This disincentive could be addressed by either excluding transplants where HIV+ organs are used from risk-adjustment assessments or adjusting for the donor's HIV serostatus. Until there is resolution of these tensions between the valid interests of transplant professionals in maximizing patient access to organs versus their interests in protecting center outcomes, the acceptance of organs from HIV+ donors will likely remain limited.

Future Opportunities

  1. Top of page
  2. Abstract
  3. Background
  4. Sizing Up the Opportunity: Estimates of the Potential Number of Organs From HIV+ Individuals
  5. Ethical Considerations
  6. Legal and Operational Barriers to Promoting HIV+ Organ Donation and Transplantation
  7. Future Opportunities
  8. Acknowledgments
  9. Disclosures
  10. References

Lifting the prohibition on transplantation using HIV+ organs would promote beneficence for transplant candidates by expanding access to organs and address justice concerns for donors and their surrogates. If the practice of using HIV+ organs in transplantation proceeds, nonmaleficence concerns about harms to transplant recipients need to be diligently integrated into patient selection, processes of informed consent, shared decision making that incorporates risk/benefit analyses for individuals, and careful collection of relevant outcomes for recipients. There are also substantial opportunities for innovation that should be embraced by transplant leaders and funding agencies. These opportunities include (i) creating new regulatory mechanisms for accurate estimation of the number of HIV+ transplant candidates, (ii) determining the willingness of HIV+ and, in rare cases, HIV negative candidates to accept HIV+ organs, (iii) creating effective approaches to informed consent, (iv) characterizing the risks specific to different HIV+ donors, such as HIV resistance patterns, (v) assessing the rate of posttransplant infectious complications and (vi) determining optimal oversight for using HIV+ organs in transplantation.

References

  1. Top of page
  2. Abstract
  3. Background
  4. Sizing Up the Opportunity: Estimates of the Potential Number of Organs From HIV+ Individuals
  5. Ethical Considerations
  6. Legal and Operational Barriers to Promoting HIV+ Organ Donation and Transplantation
  7. Future Opportunities
  8. Acknowledgments
  9. Disclosures
  10. References
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