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Management of Patients Who Receive an Organ Transplant Abroad and Return Home for Follow-up Care

Recommendations From the Declaration of Istanbul Custodian Group

Domínguez-Gil, Beatriz MD, PhD1; Danovitch, Gabriel MD2; Martin, Dominique E. MBBD, PhD3; López-Fraga, Marta BS, PhD4; Van Assche, Kristof PhD5; Morris, Michele L. MD6; Lavee, Jacob MD7; Erlich, Gilad LLM8; Fadhil, Riadh MBChB, FRCS9; Busic, Mirela MD10; Rankin, Glynn11; Al-Rukhaimi, Mona MD12; O'Connell, Philip MD13; Chin, Jacqueline BA Hons (NUS), BPhil, DPhil (Oxon)14; Norman, Triona15; Massari, Pablo MD16; Kamel, Refaat MD17; Delmonico, Francis L.18 on behalf of the Declaration of Istanbul Custodian Group working group on ethical travel for transplantation.

Author Information
doi: 10.1097/TP.0000000000001963

Organ transplantation is the best and frequently the only lifesaving treatment for end-stage organ failure. However, although the number of transplants performed worldwide has steadily increased, organ shortages persist,1 leading some patients to explore opportunities for transplantation in foreign countries. Although some travel for transplantation is justifiable, foreign patients may knowingly or inadvertently contribute to transplant-related crimes, such as trafficking in human organs (THO) and human trafficking for organ removal (HTOR).2-8

The Declaration of Istanbul on Organ Trafficking and Transplant Tourism states that travel for transplantation becomes 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.”9

Transplant tourism most frequently occurs when a prospective recipient travels to a country where the laws against organ commercialism are marred by loopholes or are poorly enforced.10 The organs most readily available in such countries for foreigners are kidneys obtained from paid living, unrelated “donors,” often victims of exploitation and coercion. Executed prisoners have also been the source of organs for transplant tourists, a practice widely condemned by the international community.11-13 In addition, organs from deceased donors have sometimes been allocated to foreigners who are prioritized over residents, thus undermining a country´s ability to address the transplantation needs of its own population. The World Health Organization (WHO) has estimated that 5% to 10% of organ transplants performed annually takes place in the context of international organ trade.10 However, the true magnitude and the features of transplant tourism remain unknown in the absence of systematic efforts to compile solid evidence on this practice.14-16

Eradicating transplant tourism depends on complex solutions that include efforts by countries to ethically progress towards self-sufficiency in transplantation.9,17,18 Meanwhile, professionals and authorities confront the medical, legal, and ethical problems raised by patients who return home after receiving an organ transplant abroad, particularly when the organ has been illegally or unethically obtained. These patients often return with poor medical documentation. Some suffer postoperative complications and infectious diseases which endanger their own well-being and may pose a public health threat.19-21 The care of these patients can be complex and may impose burdens on their national health system beyond those inherent to organ failure and its treatment in normative transplantation. Issues related to reimbursement of expenses for the procedure abroad and to access to follow-up care and immunosuppression are further matters of concern.

Transplant tourism usually entails criminal activities committed abroad, and on occasion even in the recipient's home country. Combatting THO and HTOR requires international and interagency cooperation in criminal investigations that might be triggered by information provided by patients returning home for care after having undergone an illicit transplantation abroad. Reporting of these cases by health professionals to the relevant authorities is, however, a subject of intense debate.22

Despite the challenges outlined above, there is little guidance for professionals, health systems, and other authorities concerned with the management of transplant travelers. With the support of The Transplantation Society and the International Society of Nephrology, the Declaration of Istanbul Custodian Group convened an international, multidisciplinary workshop comprising 35 participants in Madrid, Spain, on April 4 to 5, 2016, to address these challenges and produce recommendations for the management of these patients (see Supplementary Material, SDC,https://links.lww.com/TP/B496). These recommendations are presented in this article.

CORE PRINCIPLES AND RECOMMENDATIONS FOR MANAGING PATIENTS WHO RECEIVE AN ORGAN TRANSPLANT ABROAD AND RETURN HOME FOR FOLLOW-UP CARE

  • Recommendation 1: Governments and health professionals should implement the necessary measures to ensure that traceability, transparency and continuity of care are guaranteed also for patients who receive a transplant in a foreign country.
  • Organ transplantation differs in many respects from other sophisticated medical interventions. Organs are required from other human beings who may be living or deceased. Successful transplant programs hence require the full engagement of the public who are, perforce, the source of the organs. The success of transplantation is measured not only in the recovery from surgery itself but also in the long-term function of the organ and in the well-being of the living donor. There are also major safety concerns relating to the dangers of transmission of infection, malignancy and other diseases. Health authorities have a responsibility to regulate and monitor the practice of organ transplantation, to protect living donors and transplant recipients from harm, and to assure the equitable distribution of organs from deceased donors.23
  • To achieve these ends, transparency and traceability are required. Both principles have been enshrined in international standards. The WHO Guiding Principles on human cell, tissue and organ transplantation call for all organ donors and recipients to be reported by health professionals to the relevant authority and to be registered, with traceability ensured and results monitored.23 The Council of Europe Additional Protocol to the Convention on Human Rights and Biomedicine concerning Transplantation reaffirms the principle of transparency and the obligation to ensure traceability of organs.24 In the European Union, these principles are laid down as mandatory requirements through Directive 2010/53/EU.25 Moreover, Directive 2012/25/EU describes procedures for transmitting the information required for traceability and vigilance where organs are exchanged across borders.26
  • Transparency requires that data on all transplants performed in each jurisdiction be available to the public through a governmental organization or a dedicated organization designated by a governmental authority. Such transparency reassures the public that organs donated are allocated fairly, per verifiable, equitable, and medically sound criteria. Traceability, with ease of identification of the organ source, is necessary for the safety of living donors, recipients, and of the public in the event of transmission of diseases. For these reasons, countries with a developed transplant infrastructure should maintain a waiting list for organs and all transplants, performed exclusively in authorized institutions, should be notified to a central authority, that will record all data and ensure that organs can be traced from donor to recipient and vice versa.
  • Transfer of care of a recent transplant recipient from one transplant program to another requires a detailed description of the donor, the surgical procedure, the posttransplant course, the immunosuppressive regimen, and the adjunctive infection prophylactic regimen. Gaps in the continuity of care can result in unnecessary hospital admissions and diagnostic tests, as well as in otherwise avoidable complications.
  • The principles of transparency, traceability and continuity of care, which apply to patients who undergo transplantation domestically, should also apply to patients who receive—by legitimate or illegitimate means—an organ transplant abroad. To achieve these goals, governments and health professionals should implement the necessary measures, such as those proposed in the present manuscript.
  • Recommendation 2: Patients who receive a transplant abroad should be promptly referred for evaluation at a transplant center to ensure appropriate screening and care of these patients, particularly addressing infectious diseases.
  • Ideally, all transplants performed in a foreign country will take place in a coordinated manner with prospective communication between professionals in the destination and the home country of the transplant candidate. Currently, however, health professionals frequently receive transplant recipients on their return home in unexpected and acute circumstances. The primary duty of health professionals in any circumstance is to ensure provision of care.
  • Patients who receive a transplant abroad incur unique risks, particularly when the transplant is obtained at unofficial or unrecognized transplant centers or is performed in breach of clinical, ethical, and legal standards.27,28 The screening of “donors” in circumstances of organ commercialism is inconsistent with best practice, as the financial interests of those involved, including health professionals, often conflict with the health interests of donors and recipients. Most commercial living donors belong to medically underserved, socioeconomically disadvantaged groups with high risks of exposure to tuberculosis, human immunodeficiency virus, and hepatitis viruses.10 Some patients who seek transplantation abroad may be higher risk candidates for transplantation because of age and medical comorbidities. Patients returning from transplantation at a foreign destination may present with acute surgical complications and infectious diseases due to opportunistic pathogens or multidrug resistant organisms not previously seen in their home country.29,30 They may also present with subtle and delayed infectious syndromes that may be difficult to diagnose due to their atypical presentation and their rarity in the recipient’s home country.
  • As a consequence, specific knowledge and expertise are required to evaluate and care for patients who receive an organ transplant abroad, particularly in circumstances consistent with THO or HTOR. Professionals at transplant centers should oversee such evaluation and care, and require specific guidance and training for the screening and evaluation of transplant travelers. Guidelines should be produced by the community of transplant professionals, drawing on international experience and expertise. Guidelines may require tailoring in the context of local healthcare and legal systems, and training should be provided as part of ongoing professional development in transplant centers.
  • Recommendation 3: National health authorities and/or insurance providers should not cover the costs of transplant procedures performed abroad when they involve THO and/or HTOR. However, patients who receive a transplant abroad should always be provided necessary care upon their return, and costs of follow-up treatment should be covered as for any other transplant patient, subject to the registration of relevant information at official transplant registries.
  • Travel for transplantation may be appropriate and necessary, for example, when transplantation is performed in the context of bilateral or multilateral agreements, or when migration separates potential-related donors and recipients in different jurisdictions. Thus, health authorities or insurers may provide financial support to enable travel by transplant candidates or potential living donors that meets the standards established within the domestic jurisdiction. However, when patients undergo transplantation abroad in conditions that entail THO and/or HTOR, then the health system and/or the insurance provider at the home country should not reimburse the costs of that procedure.23 It is for individual jurisdictions to determine how this recommendation may be applied. In practice, this measure has proven to be an effective deterrent of transplant tourism. In Israel, transplant legislation enacted in 2008 specified that the reimbursement of transplantation abroad would be limited to procedures performed in compliance with the legislation of the country of destination and of the principles of the Israeli Law against organ trade.31 A progressive decline in the number of Israeli patients receiving an organ transplant abroad has since been observed.
  • A different approach should be taken with regards to the care of transplant travelers upon their return. All these patients should be provided with necessary healthcare, regardless of whether they are suspected of engagement in illicit activities. Healthcare should not be withheld as a punitive measure, especially when doing so might endanger lives. It is not the responsibility of health professionals or authorities to sanction patients suspected of criminal activity, which is a matter for legislators and law enforcement authorities (LEA). However, some professionals may be reluctant to care for patients whom they suspect or know to have obtained a transplant through illegal or unethical means. Professionals must always provide care to any patient in emergent need, including patients who may have obtained an organ through transplant tourism.32 In nonemergent situations, individual physicians may elect to defer the care of these patients to another physician.32
  • In countries that routinely provide whole or partial coverage for posttransplant care, the same coverage should be provided to patients who have undergone a transplant abroad. However, these patients should also be held to the same standards of traceability and transparency applied to those receiving transplants domestically, such that coverage of posttransplant care should be made conditional on the routine registration of the patient and the transplant-related data in the official registries managed by governmental authorities or delegated agencies, as indicated in recommendation 4.
  • Recommendation 4: Data routinely collected by health professionals and recorded at national transplant registries on patients who receive a transplant domestically, including long-term follow-up information, should also be routinely collected for patients who receive a transplant abroad.
  • Systems of international support and cooperation between health authorities should be established to assist in the timely communication of information about patients who receive transplants abroad to facilitate transparency, continuity of care and transnational traceability and vigilance.
  • Consolidated and anonymized data on patients who receive organ transplants abroad should be regularly reported by health authorities to relevant international organizations.
  • Routine and standardized data collection from patients who return from transplantation at a foreign destination offers significant benefits for health authorities and those responsible for the prevention of transnational transplant-related crimes. At present, there is little information available regarding the magnitude of travel for transplantation, the countries involved, and the factors influencing travel. There is only sporadic and nongeneralizable information regarding “donor” and recipient demographics, quality of care, and the impact of traveling for transplantation on posttransplant outcomes. This makes it difficult to provide guidance to patients, health professionals and authorities responsible for prospectively and retrospectively managing travel for transplantation. Furthermore, specific data collection is required to enable traceability of organs, and hence to assure the safety of donors, recipients and their respective communities. Specific knowledge is particularly required about the frequency and type of infectious diseases that patients might import. The cross-border transit of infectious pathogens that often results from commercial (and on occasion also from noncommercial) transplantation not only strains the medical and financial resources of the countries when transplant travelers return with infection-related complications, but also negatively impacts public health, potentially even being the source of infectious disease outbreaks.29,30,33
  • In accordance with the abovementioned international legal framework,23-26 countries with transplantation systems should establish registries with information on donors and recipients that ensure transparency, guarantee traceability, and allow for the appropriate follow-up of living donors and recipients. These registries should be managed by a governmental authority or by a delegated body. Registries should be subject to quality control measures and auditing, and comply with patient confidentiality and data protection measures that apply in the relevant jurisdictions.
  • We propose that the same data routinely recorded from patients who receive a transplant domestically should also be recorded from patients who receive a transplant abroad. When a recipient returns home to receive posttransplant care, the treating physician should provide information to the transplant registry in the same manner as they would for patients who receive an organ transplant within the country. Some additional information may be required due to the unique characteristics of travel for transplantation. Table 1 proposes a set of variables to collect from patients returning from transplantation abroad which should be part of existing data collections and transplant registries.
  • To facilitate continuity of care and transnational traceability and vigilance, we further propose that systems of international cooperation should also be established to assist in the timely communication of information about patients who receive transplants in foreign destinations. This would require that, when a national health authority receives information about a resident having received a transplant abroad, they should inform the parallel authority of the country where the transplant took place. The exchange of information would allow for authorities in destination countries to cross-check that the transplant procedure is also registered within their national registry. This data exchange would also allow transnational traceability, which is of importance when safety problems arise in either the donor or the recipient.
  • Because of the global dimension of travel for transplantation, and the need for concerted efforts to combat THO and HTOR, data regularly collected by national health authorities should be shared internationally.34 National data on patients who travel abroad for transplantation could be reported by health authorities to international organizations and communicated using existing data collection mechanisms, that is, the Council of Europe Newsletter Transplant35 and the WHO Global Observatory on Organ Donation and Transplantation.1 Under the framework of Resolution CM/Res(2013)55, the Council of Europe is already piloting this type of data collection by a network of national focal points designated by Council of Europe member states.36Table 2 lists key information to be shared internationally for a given year. Sharing such information would allow a better understanding of travel for transplantation and identification of possible hotspots of transplant tourism that merit investigation by the countries concerned.
  • Figure 1 summarizes the proposed flow of information between professionals, national agencies, and international organizations.
  • Recommendation 5: Health professionals and health authorities should be provided with guidance and training to assist them in the identification of patients who may have received an organ transplant abroad in circumstances consistent with THO and/or HTOR.
T1-13
TABLE 1:
Proposed data set to collect and register from patients who return after transplantation in a foreign destination
T2-13
TABLE 2:
Proposed set of aggregated data to be shared by National Health Authorities with the Council of Europe and the World Health Organization
F1-13
FIGURE 1:
Flow of information for registration of data in national transplant registries on patients who receive an organ domestically and those who receive an organ transplant abroad and return home for follow-up care. DD, deceased donor; LD, living donor.

Governments should provide a clear legal and ethical framework and should develop mechanisms to allow health professionals and/or health authorities to communicate information about these cases to national and/or international law enforcement agencies.

Law enforcement agencies should receive training and guidance on the nature and characteristics of transplant-related crimes, particularly those of THO and HTOR.

Health professionals and authorities should be provided with guidance and training to assist them in identifying cases of travel for transplantation that may involve criminal activity.37 They should become familiar with possible indicators (“red flags”) of illegitimate travel for transplantation, such as those proposed in Table 3. Importantly, by identifying potential cases of transplant tourism through these indicators, clinicians will also be able to provide better care to these patients through tailored evaluation and management, informed by the risks associated with illicit transplantation.

T3-13
TABLE 3:
Indicators that can help health professionals and authorities to retrospectively identify illegitimate travel for transplantationa

To effectively combat transplant-related crimes and prevent established criminal rings from committing further crimes, national LEA should duly be made aware of all potential illicit activities, including those detected or suspected by health professionals. This requires governmental legislative action and the development by professional organizations of clear ethical frameworks for reporting or providing information about detected or suspected cases.

There are several potential concerns about reporting or providing this information to LEA in particular, where there is a potential breach of legal and ethical duties to protect patient privacy and medical confidentiality. In some jurisdictions, statutory provisions permit or mandate that physicians breach these duties only when there is an imminent risk to public health, or when vulnerable individuals, such as children, are at risk of sexual abuse or violence.38,39 Although information about donation and transplantation is routinely collected from patients and reported to health authorities in many countries, reporting information to LEA that relates to potential criminal activity is a different matter. Issues may be complicated further by the transnational scope of these activities involving jurisdictions with nonharmonized legislation.40

Case law indicates that, where cases of transplant tourism are presented to LEA, this generally is not the result of reporting by health professionals or health authorities. Indeed, criminal investigations have been instigated after exposure by investigative journalists, inquiries by customs and border police, and allegations by informants or (prospective) donors who were threatened.8,41 By contrast, direct reporting by health professionals of suspected cases is very uncommon. To our knowledge, only in Israel has a system been developed for the reporting of identified or suspected cases of illegitimate travel for transplantation by health professionals (Table 4).

T4-13
TABLE 4:
Summary of the Israeli system for the reporting of suspected or confirmed cases of illegitimate travel for transplantation by health professionals to law enforcement authorities

In the absence of mechanisms to report cases of transplant tourism to LEA, countries seeking to combat transplant-related crimes may explore different approaches. Jurisdictions may develop a system that provides for (voluntary or mandatory) nonanonymized reporting of detected or suspicious cases to LEA by health professionals, even without the patient´s consent. Here, inspiration could be drawn from statutory frameworks requiring disclosure of potential child abuse. Transplant hospitals could establish protocols to identify and report suspected cases like protocols in place on child abuse. The latter protocols stipulate the obligations (either voluntary or mandatory) to identify and report child abuse, specify indicators of abuse and thresholds of risk that activate the reporting duty, set out procedures of consultation with colleagues or specialists and indicate what and how evidence should be documented and to whom the referral should be made.42-44 Just as is the case for reporting child abuse, health professionals who report suspected cases of transplant tourism should be granted immunity from criminal and civil liability for breaching medical confidentiality and their identity as well as the contents of their reports should be kept confidential.

Considering that the system for reporting cases of child abuse might not readily be transposable, an alternative could be a system of (voluntary or mandatory) reporting of anonymized data that reveals information on entities, hospitals, or professionals engaged in illegitimate transplantation, but not the identity of the patient concerned. Legislative provisions that protect patients from the consequences of identity disclosure may facilitate reporting of information that would be most effective in prosecuting those who regularly engage in THO or HTOR, such as transplant professionals or brokers, while protecting those who may be deemed vulnerable, such as recipients or “donors.” In any circumstance, patients who receive an illegitimate transplant abroad should be encouraged to report their case on a voluntary basis and cooperate with LEA during criminal investigations, provided they are suitably protected, and in accordance with the law.

Reporting systems may also vary. Instead of direct case reports by individual professionals to LEA, health professionals may delegate this task to authorities coordinating national transplantation activities. Such authorities may be responsible for forwarding this information to the national LEA and for facilitating the collection of evidence from their counterparts in other countries. Where necessary, the national LEA would communicate with their counterparts or liaison officers in other countries to ensure the progress of the criminal investigations.

It is essential that national authorities develop clear legislations and ethical frameworks and protocols to encourage, or potentially even mandate, the reporting of these cases to LEA. When such systems are established, patients should be routinely informed about reporting practices, use of data, and potential legal consequences of travel for transplantation. LEA will require training and guidance concerning the diverse and subtle manifestations of THO and HTOR. Health authorities and LEA should work on effective ways of ensuring interagency cooperation in the identification, prevention, and combat of these crimes.

CONCLUSIONS

Although progress has been made since the Declaration of Istanbul was published in 2008,21 transplant tourism remains a global problem against which no consistent and harmonized response has been formulated. Preventing and combatting transnational transplant-related crimes require a firm and coordinated response from health professionals, health authorities, LEA, and international health and prosecuting organizations.

The principles of transparency, traceability and continuity of care that apply to patients who receive an organ domestically should also apply to patients who return from transplantation abroad. Furthermore, governments and professional organizations must develop legal and ethical frameworks for the communication of identified or suspected cases of illegitimate travel for transplantation by health professionals to LEA. Without such actions, the perils of transplant tourism will persist.

ACKNOWLEDGMENTS

Other participants in the DICG Workshop on Ethical Travel for Transplantation: Curie Ahn (South Korea), Nancy Ascher (United States), Alireza Bagheri (Iran), Jeremy Chapman (Australia), Somchai Eiam-Omg (Thailand), Rudolf García-Gallont (Guatemala), John Gill (Canada), Vivekanand Jha (India), Adeera Levin (Canada), Rafael Matesanz (Spain), Elmi Muller (South Africa), Alejandro Niño Murcia (Colombia), José R. Núñez (World Health Organization), Axel Rahmel (Germany), Rafael Reyes (Mexico), Faissal Shaheen (Saudi Arabia), Haibo Wang (People's Republic of China).

The authors wish to thank The Transplantation Society and the International Society of Nephrology for their support in the organization of this workshop. The authors are appreciative of participation by representatives of the Council of Europe and the World Health Organization. The authors wish to thank Piero Segantini of the International Society of Nephrology for his administrative support of the meeting.

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