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Transplant Tourism - Patients Travel Around the U.S. for their Best Transplant Options

Transplant tourism: a growing phenomenon

David J Cohen 1

Nature Reviews Nephrology volume 5 , pages 128–129 ( 2009 ) Cite this article

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Medical tourism is increasing owing to high costs of care, lack of availability or long waits for procedures, and improvements in technology and standards of care in many countries. Transplant tourism is one example of medical tourism that has been attracting increasing attention because of concerns over poor treatment and outcomes of both donors and recipients. Most such cases involve vended kidneys obtained from vulnerable populations, and both donors and recipients receive inferior care by US standards. This commentary discusses a paper by Gill et al . that compared outcomes of 33 transplant tourists with those of patients transplanted at a US center. Fewer complications and better outcomes were seen in patients transplanted in the US center than among transplant tourists. Large transplant centers with long waiting times are increasingly likely to see patients return newly transplanted from overseas; such patients require urgent attention, with particular consideration to infectious complications.

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Presbyterian Hospital, Room 4-124, 622 West 168th Street, New York, NY 10032, USA [email protected]

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DJ Cohen is a Professor of Clinical Medicine at Columbia University Medical Center, New York, NY, USA.,

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Cohen, D. Transplant tourism: a growing phenomenon. Nat Rev Nephrol 5 , 128–129 (2009). https://doi.org/10.1038/ncpneph1039

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Received : 27 November 2008

Accepted : 17 December 2008

Published : 27 January 2009

Issue Date : March 2009

DOI : https://doi.org/10.1038/ncpneph1039

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Transplant Tourism: Understanding the Risks

Transplant and Oncology (M Ison and N Theodoropoulos, Section Editors)
Published: 14 April 2015
Volume 17 , article number 18 , ( 2015 )

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Jennifer M. Babik 1 &
Peter Chin-Hong 1

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Transplant tourism is commonly defined as travel abroad for the purpose of transplantation, but the term evokes ethical and legal concerns about commercial transplantation. Due to the mismatch in supply and demand for organs, transplant tourism has increased over the last several decades and now accounts for 10 % of transplants worldwide. Patients from the USA who pursue transplantation abroad do so most commonly for renal transplantation, and travel mostly to China, the Philippines, and India. Transplant tourism puts the organ recipient at risk for surgical complications, poor graft outcome, increased mortality, and a variety of infectious complications. Bacterial, viral, fungal, and parasitic infections have all been described, and most concerning are the high rates of blood-borne viral infections and invasive, often fatal, fungal infections. Transplant and infectious diseases physicians should have a high degree of suspicion for infectious complications in patients returning from transplantation abroad.

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Transplant Tourism and the Traveling Transplant Recipient: Infection Mitigation and Treatment Strategies

Transplant Tourism

Papers of particular interest, published recently, have been highlighted as: • of importance •• of major importance.

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Acknowledgments

The authors would like to thank Ban Hock Tan for his assistance. Dr. Chin-Hong is supported by the National Center for Advancing Translational Sciences, National Institutes of Health, through UCSF-CTSI Grant Numbers UL1 TR000004 and TL1 TR000144. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIH.

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Jennifer Babik and Peter Chin-Hong have no conflicts of interest.

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This article does not contain any studies with human or animal subjects performed by the author.

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Babik, J.M., Chin-Hong, P. Transplant Tourism: Understanding the Risks. Curr Infect Dis Rep 17 , 18 (2015). https://doi.org/10.1007/s11908-015-0473-x

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Transplant Tourism: The Shadow World of Medicine

Recently, Pakistani police raided an apartment in Islamabad and released 24 men and women who had beenheld up against their will. Brought there through threats and deceit, these people were scheduled to go to a clinic where one kidney would be removed from each of them for commercial transplant purposes. This phenomenon has been growing gradually, permeating different countries and transforming into what has become the shadow world of medicine.

According to the World Health Organization (WHO), about 100,800 solid organ transplants are done every year, most of which are liver and kidney transplants. About 30% of these transplant procedures are performed in the United States, making the country a major destination for helping people in need of organ donation.

However, the country has a system in which organs are allocated in a fair way; based on the severity and nature of illness of the prospective recipient, the chances of survival of the patient without a timely transplant, and the availability of the organs. This means some patients may have to wait for a long time, sometimes as long as 7 years, to have a transplant.

Even in countries with efficient organ donation systems, the available organs are either inadequate to meet the growing demands for it or its donation are hampered by serious legal and sociocultural problems.

These various impediments open the door to transplant tourism, seeing patients from the US and other developed countries travel to countries – mostly China, India, Philippines, and Pakistan – where they can have the procedure done faster and at affordable rates. However, there is a dark side to this.

The Burden of International Organ Trade

Illegal organ trafficking has penetrated transplant medicine for more than a decade now, with several individuals and groups illegally harvesting organs from living donors and facilitating such activities. A case in point is China: A 2019 study published in the British Medical Journal (BMJ) in January called for the retraction of more than 400 research papers covering more than 85,000 organ transplants performed in China over concerns that the organs may not have been voluntarily donated but harvested forcefully and unethically from Chinese Prisoners.

The study, which was conducted by Australian researchers led by Wendy Rodgers, Ph.D, a professor of clinical ethics at Macquarie University in Australia, found that 90 percent of these studies did not report how the organs were sourced.

While the Chinese authorities maintained that organs for transplant have been provided by voluntary donors or from executed convicts on death rows, there is fresh evidence to the contrary. A detailed 2016 report by International Coalition to End Transplant Abuse in China, a transplant ethics group, found some inconsistencies between the number of organ transplants the Chinese government reported were performed in the country and the actual number – more than 70,000 organs were unaccounted for.

Investigations show that many of these organs were forcefully harvested from prisoners of conscience, such as those who practiced Falun Dafa, a religious practice that has been banned in the country. In addition, several of those Chinese organ transplants were performed before 2010, when China did not have an organized organ donation system. So this begs the question of how and from where the organs were obtained.

Forms of International Organ Trade

Today, there are several agencies and facilitators abetting illegal purchase and sale of organs for transplant. Some of these facilitators are even healthcare providers. In Taiwan, China, of 118 patients who underwent organ transplants with illegally harvested organs, 69 reported that the procedures were facilitated by doctors. There have also been several allegations of embassy personnel of some Middle Eastern countries facilitating illegal kidney trade in the Philippines.

In some instances, live donors are flown from their home countries to the recipient’s country and in others, both recipients and donors are transferred to another country to have the transplant surgery done. And the majority of the recipients are foreigners from developing countries.

More than 100 illegal kidney transplant surgeries were performed in South Africa between 2001 and 2002, with most of the recipients traveling from Israel and donors coming from Brazil and parts of eastern Europe. Police investigations of these transplants revealed that there was an international organ trafficking syndicate involved in facilitating most of the transplants. The case is even more concerning in the Islamic Republic of Iran, where paid kidney donation is legal but restricted to foreigners.

According to Peter Chin-Hong, MD, professor of medicine and director of the University of California’s transplant infectious disease program, poverty is what fuels this illegal organ trade. In agreement with this, Voluntary Health Association reports that about 2000 Indians sell a kidney every year, with donors paid about $6,000 to harvest their kidneys.

Although reports estimate that transplant tourism comprises only 10% of all transplants performed worldwide, Chin-Hong believes this figure might just be an underestimate, as several of these illegal activities are underground and underreported.

Risks of Transplant Tourism

This illegal commercialization of organs comes with one of many problems – an increased risk of diseases and deaths from the transplanted organs. Unlike what is obtainable in the United States, most of the harvested organs do not pass through the standard screening procedures before transplant is performed and, in other cases, the procedure is performed in terribly nonsterile conditions.

This exposes the recipient to several, often fatal, infectious diseases including tuberculosis, HIV/AIDS, hepatitis, cytomegalovirus (CMV) infection, and other blood-borne infections. Some studies have shown that the risk of these diseases in commercial transplantation could be as high as 7.1% for hepatitis B, 4.1% for HIV, and 30% for CMV, much higher than in traditional transplantation. However, these risks may just be underestimated, as most organ recipients do not report their transplant tourism.

Even worse are the potential risks to these organ donors. Less empirical research has been done for the paid or coerced donors from whom these organs are harvested. Some of the harvesting procedures may be performed under aseptic conditions, increasing the risk of severe surgical infections and complications. In addition to this, coerced donors run the risk of developing severe psychological problems and disabilities.

The Way Out

The international organ trade thrives on the growing demand for organ transplantation, as well as the lack of and discrepancies in regulations and policies guiding organ transplant between countries. This global inequity has to be addressed with appropriate policies and ethical guidelines that respect and protect human dignity.

Countries must also address the problem of organ shortage by exploiting ethically acceptable sources of donor organs and developing appropriate organ donation programs across the world. The Transplantation Society also urges that ethical organizations must review studies and journals that report data on organ transplants, rejecting those that do not adhere to ethical practices on organ transplant.

Furthermore, health practitioners should continue to educate patients and citizens about the dangers of transplant tourism and emphasize the need for standard practices regarding screening and procedural settings for an organ transplant.

Bottom Line

In what has been aptly described by Chin-Hong as “the shadow world of medicine,” transplant tourism poses great health and ethical burden, with attendant risks of severe infectious diseases and the dehumanizing nature of the act. The need, therefore, arises for healthcare providers, health organizations, and governments to take this seriously, establishing policies to avert transplant tourism and creating programs to address organ shortage.

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The Medical Tourism Magazine (MTM), known as the “voice” of the medical tourism industry, provides members and key industry experts with the opportunity to share important developments, initiatives, themes, topics and trends that make the medical tourism industry the booming market it is today.

Transplant tourism

Affiliation.

1 Division of Liver Diseases, The Mount Sinai School of Medicine, New York, New York 10029, USA. [email protected]
PMID: 20364454
DOI: 10.1097/mot.0b013e328337353e

Purpose of review: Because of the ongoing organ donor shortage, transplant tourism is occurring at an increasing rate both in the USA and abroad. To date, there have been little published data to help guide the programmatic philosophy of the USA transplant centers regarding transplant tourism.

Recent findings: We summarize position statements from several transplant societies regarding transplant tourism and specifically transplantation occurring in China (because of the use of executed prisoners as organ donors). Transplant tourism is ever increasing and patients may be at risk for greater post-transplant morbidity as well as inadequate follow up care. Transplant centers require some guidance with regard of how to deal with these patients.

Summary: Transplant tourism is an increasing reality facing the USA transplant centers. Most professional societies do not condone it yet cannot abrogate a physician's right to care for such patients. Ethical principles mandate transplant physicians provide adequate care for returning transplant tourists. Better ways of assessing the scope of the problem are necessary. Transplant tourism may exist because of the disparity between the need for organ donors and their availability and is thus is likely to continue into the future.

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Attitude of Health Personnel
Health Knowledge, Attitudes, Practice
Health Services Accessibility
Medical Tourism* / ethics
Medical Tourism* / psychology
Organ Transplantation* / adverse effects
Organ Transplantation* / ethics
Organ Transplantation* / psychology
Patient Education as Topic
Practice Guidelines as Topic
Public Opinion
Risk Assessment
Tissue Donors / ethics
Tissue Donors / psychology
Tissue Donors / supply & distribution*
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Research Article

The outcomes and controversies of transplant tourism—Lessons of an 11-year retrospective cohort study from Taiwan

Contributed equally to this work with: Daniel Fu-Chang Tsai, Shi-Wei Huang

¶ ‡ These authors are co-first authors on this work.

Affiliation Graduate Institute of Medical Education and Bioethics, National Taiwan University College of Medicine; Department of Medical Research, National Taiwan University Hospital; and Centre of Biomedical Ethics, National Taiwan University, Taipei, Taiwan

Affiliation Department of Urology, National Taiwan University Hospital Yunlin Branch, Yunlin, Taiwan

Affiliation School of Law, University of Manchester, Manchester, United Kingdom

Affiliation Office of Health Care Policy Research, Koo Foundation Sun Yat-Sen Cancer Center, Taipei, Taiwan

Affiliations Institute of Population Health Sciences, National Health Research Institutes, Zhunan, Taiwan, Department of Medical Research, Tungs’ Taichung Metro Harbor Hospital, Taichung, Taiwan

* E-mail: [email protected]

Affiliations Institute of Population Health Sciences, National Health Research Institutes, Zhunan, Taiwan, Department of Health Services Administration, China Medical University, Taichung, Taiwan

Daniel Fu-Chang Tsai,
Shi-Wei Huang,
Soren Holm,
Yi-Ping Lin,
Yu-Kang Chang,
Chih-Cheng Hsu

Published: June 2, 2017
https://doi.org/10.1371/journal.pone.0178569
Reader Comments

Transplant tourism has increased rapidly in the past two decades, accounting for about 10% of world organ transplants. However it is ethically controversial and discouraged by professional guidelines. We conducted this study to investigate the outcomes and trends of overseas kidney and liver transplantation in Taiwan to provide a sound basis for ethical reflection.

Methods and findings

The Taiwanese National Health Insurance Research Database was used to identify 2381 domestic and 2518 overseas kidney transplant (KT) recipients from 1998 to 2009 and 1758 domestic and 540 overseas liver transplantation (LT) recipients from 1999 to 2009. Cox proportional hazards models were used to assess the risks of mortality and graft failure. The numbers of overseas transplantation increased after 2000, reached a peak in 2005 and decreased after 2007. Compared to their domestic counterparts, the overseas KT recipients were older, male predominant, with shorter pre-op dialysis period and more comorbidities. Similarly, the overseas LT recipients were older, male predominant and had more hepatocellular carcinoma cases. The 1-, 5-, and 10-year patient survival rates were 96.9%, 91.7% and 83.0% respectively for domestic KT and 95.8%, 87.8% and 73.1% for overseas KT (p<0.001). The 1-, 5-, and 10-year patient survival rates were 89.2%, 79.5%, 75.2% for domestic LT and 79.8%, 54.7%, 49.9% for overseas LT (p<0.001).

The poorer outcomes of the overseas groups may be due to more older patients, more comorbidities (KT), or more hepatocellular carcinoma recurrences (LT). After domestic reform and international ethical challenges, the numbers of organ tourism decreased but the practice still persisted surreptitiously. Compulsory registration policies for overseas transplantation with international conventions to sanction organ trafficking and transplant tourism should be considered to stop these controversial practices.

Citation: Tsai DF-C, Huang S-W, Holm S, Lin Y-P, Chang Y-K, Hsu C-C (2017) The outcomes and controversies of transplant tourism—Lessons of an 11-year retrospective cohort study from Taiwan. PLoS ONE 12(6): e0178569. https://doi.org/10.1371/journal.pone.0178569

Editor: Stanislaw Stepkowski, University of Toledo, UNITED STATES

Received: February 3, 2017; Accepted: May 15, 2017; Published: June 2, 2017

Copyright: © 2017 Tsai et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: The Data used for this manuscript are available from the National Health Insurance Research Database (NHIRD). Due to legal restrictions imposed by the government of Taiwan in relation to the “Personal Information Protection Act”, the data cannot be made publicly available. Requests for data can be sent as a formal proposal to the NHIRD ( http://nhird.nhri.org.tw/index1.php ).

Funding: This work was supported by the National Health Research Institutes, Ministry of Science and Technology, and Ministry of Health and Welfare of Taiwan. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Abbreviations: KT, kidney transplant; LT, liver transplant; TORSC, Taiwan organ registry and sharing center; NHI, national health insurance; NHIRD, NHI Research Database; SD, standard deviation; CCI, Charlson comorbidity index; HR, hazard ratio; IRR, incidence rate ratio

Introduction

The advancement of organ transplantation has saved numerous human lives and created enormous welfare gains. However, in the past two decades, the global organ shortage has led to the development of transplant tourism: the practice of traveling outside one’s own country to obtain organ transplantation, which often involves organ trade or trafficking [ 1 ]. Transplant tourism was estimated to account for 10% of organ transplants performed around the world in 2007 [ 2 ]. Such practice, though saving lives, has been discouraged by many international organizations because it involves the exploitation of vulnerable groups and the poor [ 1 , 3 ].

Taiwan’s hepatitis B carrier rate and the country’s prevalence and incidence of renal dialysis are among the world’s highest [ 4 , 5 ]. Even though Taiwan was one of the first Asian countries to perform renal transplant surgery in 1968, it has suffered from a severe shortage of transplantable organs for more than four decades due to a low organ donation rate. As a result, transplant tourism from Taiwan to China began in the early 1990s and has progressed rapidly as social and economic interaction between the two countries have increased [ 6 , 7 ]. According to a survey in 2006 by Taiwan’s Department of Health, only 2 of 400 overseas kidney transplant (KT) recipients and 3 of 222 overseas liver transplant (LT) recipients had organ transplantation performed outside of China [ 8 ]. Due to a growing awareness of the ethical controversies and human rights issues, measures were taken to discourage transplant tourism. For example, in 2006, the Taiwanese government announced a guideline prohibiting doctors’ participation in any form of organ brokering [ 9 ], and in 2007, requested physicians’ voluntary reporting of overseas transplant patient information to the Taiwan Organ Registry and Sharing Center (TORSC). Meanwhile, China introduced its Human Organ Transplant Act in 2007 [ 10 ]; and in 2008, the Declaration of Istanbul prohibited transplant tourism [ 1 ].

However, the practices and the outcomes of international organ tourism have not been well understood. Nationally-integrated and comprehensive medical and social research concerning transplant tourism is still scant. Questions to be answered include “How are patients who engaged in transplant tourism different from other patients?” and “Are there differences in the outcomes for overseas and domestic transplants?” Since Taiwan’s National Health Insurance (NHI) is a compulsory and universal health insurance program that covers over 99% of the general population and keeps comprehensive healthcare records, an overview of the overseas transplant patient population and the outcomes of the transplants are available [ 11 ]. Therefore, we investigated trends over the past decade in the numbers and outcomes of overseas kidney and liver transplants and in transplant-related policies in order to create an evidence base for reflection upon ethical/legal implications leading to specific proposals for policy initiatives in the Asian region that may help to resolve relevant important global health, ethics, and human rights issues.

Subjects and methods

Data source.

All patients in Taiwan who need organ transplantation and/or post-transplantation immunosuppressive therapies are registered in the NHI program so that their costs of treatment can be covered. Therefore, all transplant recipients (both domestic and overseas) in Taiwan can be identified from the NHI Research Database (NHIRD), which is derived from NHI reimbursement claims since 1996.

Study subjects

Those who received KT or LT were divided into two groups: “domestic recipients” (Taiwanese receiving a transplant in Taiwan) and “overseas recipients” (Taiwanese receiving a transplant abroad). From the NHIRD, we identified 2381 domestic KT via NHI records for the KT procedure between January 1998 and June 2009. A total of 68 transplants were excluded because of a second KT or with a simultaneous LT. To make domestic and overseas KT comparable, we further excluded 63 subjects who died or resumed dialysis within 1 month after the domestic KT operation, because only the successful overseas transplantation patients who returned to Taiwan and received anti-rejection therapies could be included in our study. Therefore, the remaining 2250 domestic KT recipients were selected for further analysis.

We defined overseas KT recipients as patients who were prescribed immunosuppressive medication by Taiwan physicians for kidney transplants (ICD9 = V42.0) but did not have an NHI record for a KT operation. The overseas KT recipients were validated with the NHI-based registry of catastrophic illness to exempt co-payment, and transplantation, cancer and dialysis were all included in the designated categories of catastrophic illness. The transplant-related immunosuppressive drugs recognized in this study include cyclosporine, tacrolimus, mycophenolate mofetil, sirolimus, rapamune, and cytotect. Among the 2518 overseas KT identified between January 1998 and June 2009, 114 transplants were excluded because of a second KT or with a simultaneous LT. The remaining 2404 overseas KT recipients were selected for further analysis. By applying similar criteria in selecting domestic and overseas LT recipients from the NHIRD, we identified 1658 domestic LT recipients (excluding 84 patients who died within one month after LT and 16 secondary LT) and 540 overseas LT recipients for further analysis between January 1999 and December 2009. We further contacted the TORSC to get the number of overseas and domestic (including deceased and living) transplants beyond the study period.

Statistical analysis

The distributions of demographic and clinical characteristics of the study subjects were described and compared using mean ± standard deviation (SD) and Student’s t-tests for continuous variables, and counts/proportions and chi-square tests for categorical variables. The comorbidity was measured by the D’Hoore’s Charlson comorbidity index (CCI) score [ 12 ] using the subjects’ NHI records a year prior to transplantation. The trends of overseas and domestic transplants were compared using Cochran-Armitage trend test.

Associations between domestic and overseas KT recipients and mortality/graft failure (or association between LT groups and mortality) were analyzed using Kaplan–Meier survival curves and log-rank tests. Multivariable Cox proportional hazards models were further conducted to estimate their adjusted associations. The proportional hazards assumption was evaluated by plotting Kaplan–Meier survival curves for investigated covariates against follow-up time. Study entry was defined as the date of transplantation. For domestic KT and LT recipients, the date of transplantation was as shown in the NHIRD. For overseas KT and LT recipients, the date of transplantation was defined as 14 days and 35 days, respectively, prior to the date the patients took the first prescription of post-transplant immunosuppressant drugs, because the average postoperative hospital stays for overseas KT and LT were 14 days and 35 days, respectively, according to a previous questionnaire survey (8). As determined by database availability, the KT and LT cohorts were followed up through the ends of 2009 and 2010, respectively. In the models estimating the hazard ratio (HR) of mortality, observations were censored on December 31, 2009, for kidney transplants and December 31, 2010, for liver transplants, or on the date that the patients died, whichever occurred first. In the models estimating the hazard ratio of kidney graft failure, observations were censored on December 31, 2009, on the date that the patients died, or the date on which the subjects resumed persistent dialysis, whichever came first. The pre-transplant characteristics adjusted in the multivariable Cox proportional hazards models for KT recipients included gender, age at KT, CCI score, and time interval between initiation of dialysis and KT. To assess mortality risk for LT recipients, age, gender, CCI score, and hepatocellular carcinoma, were adjusted in the multivariable models.

Analyses were performed using SAS software, version 9.3 (SAS Institute, Cary, North Carolina, USA). A two-sided P value < 0.05 was considered statistically significant. This study was approved by the Institutional Review Board of the National Health Research Institutes.

Numbers of transplants and trends

The number of patients receiving KT overseas has increased since 2000 and first peaked in 2002 (n = 354) before a decrease in 2003 ( Fig 1 ), the year of the severe acute respiratory syndrome (SARS) epidemic in Southeast Asia [ 13 ]. After a second peak in 2005 (n = 374), cases of overseas KT decreased in 2007–2014 (P<0.001). Meanwhile, the number of overseas LT started to increase in 2000, peaking in 2005 as well (n = 117), and then decreased (P<0.001). The steady decrease of overseas LT after 2012 coincided with an increase of domestic LT, which was mainly from related living donations ( S1 Table ).

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(A) Kidney transplants, 1998–2014 (Cochran-Armitage trend test P < 0.0001). (B) Liver transplants, 1999–2014 (Cochran-Armitage trend test P < 0.0001). KT = kidney transplant. LT = liver transplant. The numbers from 1998–2009 and 2010–2014 were obtained from NHIRD and TORSC, respectively. The numbers in 2009 would be incomplete since some recipient data were not available until in 2010 NHIRD.

https://doi.org/10.1371/journal.pone.0178569.g001

Demographic comparison

Table 1 shows that, compared to the domestic KT recipients, the overseas KT recipients were older (47.9 vs 41.2 years, p<0.001), male-dominant (54.8% vs 49.0%, p<0.001), and had a shorter dialysis duration before KT (p<0.001). The overseas KT recipients also suffered from more comorbidities: they had a higher CCI score (1.01 vs 0.73, p<0.001), as well as higher percentages of diabetes (14.2% vs 8.0%, p<0.001) and hypertension (38.6% vs 26.5%, p<0.001).

https://doi.org/10.1371/journal.pone.0178569.t001

As shown in Table 2 , overseas LT recipients were older (50.3 vs 43.0 years, p<0.001), mainly adult (97.4% vs 83.5%, p<0.001), and male-dominant (82.0% vs 69.0%, p<0.001). In addition, more of them had hepatocellular carcinoma compared to their domestic counterparts (64.1% vs 39.9%, p<0.001).

https://doi.org/10.1371/journal.pone.0178569.t002

Clinical outcome

Table 1 and Fig 2 show the domestic KT recipients had a significantly better crude patient survival rate than the overseas recipients (log rank test p<0.001) but a similar graft survival rate (log rank test p = 0.649). In Cox proportional hazards model ( Table 3 ), the risk factors of mortality for KT recipients were older age (>65 y/o vs ≤35 y/o, aHR = 5.00 [3.39–7.36], p<0.001), male (aHR = 1.35 [1.14–1.61], p<0.001), higher CCI score (≥3 vs 0, aHR = 1.53 [1.20–1.94], p<0.001), and longer pre-transplantation dialysis time (≥1 yr vs no dialysis, aHR = 1.36 [1.01–1.81], p = 0.040). Regarding kidney graft failure, there was no difference between domestic or overseas kidney recipients (aHR = 0.88 [0.77–1.01], p = 0.068), but older age (>65 y/0 vs <35 y/o, aHR = 2.15 [1.57–2.94], p<0.001), male (aHR = 1.15 [1.02–1.31], p = 0.029), higher CCI score (≥3 vs 0, aHR = 1.41 [1.16–1.70], p = 0.001) and longer pre-transplantation dialysis time (>1yr vs no dialysis, aHR = 1.46 [CI 1.16–1.82], p = 0.001) were still considered risk factors for graft failure ( Table 3 ).

(A) Patient survival for kidney transplant recipients, log-rank test P < 0.001; (B) graft survival for kidney transplant recipients, log-rank test P = 0.649; (C) patient survival for liver transplant recipients, log-rank test P < 0.001; (D) patient survival for liver transplant recipients, categorized by location and whether the patient had hepatocellular carcinoma, log-rank test P < 0.001.

https://doi.org/10.1371/journal.pone.0178569.g002

https://doi.org/10.1371/journal.pone.0178569.t003

Regarding liver transplants, the domestic LT recipients had significantly better survival probabilities than those of the overseas LT recipients in the crude rate (log-rank test p<0.001, Table 2 and Fig 2 ). Overseas LT recipients with prior hepatocellular carcinoma had the lowest survival rate ( Fig 2 ). In Cox proportional hazards models, due to significant interaction between location of transplantation and history of hepatocellular carcinoma (p<0.001), we separated the subjects into two groups according to their history of hepatocellular carcinoma ( Table 4 ). In the hepatocellular carcinoma group, overseas LT had a significantly higher hazard ratio for patient mortality (aHR = 2.65 [2.08–3.38], p<0.001) after adjusting for age, sex, and CCI score. On the other hand, in the non-hepatocellular carcinoma group, the mortality rate of overseas LT was not different from that of domestic LT (aHR = 1.31 [0.94–1.82], p = 0.107). Older age (>60 y/o vs ≤18 y/o, aHR = 2.32 [1.37–3.93], p = 0.001) was another risk factor for patient mortality.

https://doi.org/10.1371/journal.pone.0178569.t004

We further identified that post-KT malignancy and liver disease were the two main causes of death for overseas KT recipients compared to those for the domestic KT recipients. On the other hand, hepatocellular carcinoma was the major cause of death for overseas LT recipients (69.0 per 1000 person-years; IRR = 6.58 [4.69–9.23], p<0.001) compared to their domestic counterparts (8.2 per 1000 person-years) ( Table 5 ).

https://doi.org/10.1371/journal.pone.0178569.t005

Features of transplant tourism from Taiwan to China

Our results showed that the overseas transplant group had the following characteristics: male predominant, older, having more comorbidities, having a shorter pre-operative dialysis time in kidney transplant, and more hepatocellular carcinoma cases in liver transplant. The outcomes of overseas transplant were inferior to domestic transplants in crude rate. After adjusting for covariates, no difference was noted in overseas and domestic kidney transplant. However, overseas liver transplant is much worse than domestic liver transplant in the hepatocellular carcinoma group.

There were several reasons that created the different characteristics between domestic and overseas transplant. Taiwan is still a relatively paternalistic society, and males commonly play a dominant role in family finance and income disposition. Older people generally have greater financial and social resources; yet they might have more health problems and comorbidities, which put them at a disadvantage in rank on the transplant-waiting lists and may even lead to them being excluded for surgery. Hence, they are more likely to grasp an opportunity for overseas transplantation. The pre-transplantation dialysis period is shorter in the overseas group, which indicates a shorter waiting period and the commercial nature of overseas transplantation. The same reason applies to overseas liver transplants, with more recipients being older and male.

Patient and graft survivals.

Two previous studies show that the clinical outcomes of overseas KTs were comparable to those of domestic KTs after 2000 [ 7 , 14 ]; however, those studies had brief follow-up periods (< 5 years) and used only one institution with limited case numbers. In our study, the crude patient survival rate was better for domestic KT recipients, but there was no difference in graft survival. The higher mortality rate in overseas KT recipients might have been reduced by a low kidney graft failure rate (overseas vs. domestic: 33.2% vs. 54.5%, Table 1 ). This is consistent with the general conception that organs procured from executed prisoners (especially young males) in China are similar to organs from living donors, and hence, have better “quality” than the domestic deceased organs which are mainly from brain-dead patients. However, after adjusting for covariates, the mortality rate was similar between domestic and overseas KT patients. The poor survival rate in overseas patients is attributed to the characteristics of overseas patients (old age, more comorbidity, and male).

Malignancy.

We found that the main causes of death for KT, especially in overseas transplants, were malignancy and liver disease. The most common malignancies in overseas KT recipients were genitourinary malignancy (kidney or bladder cancer) and hepatocellular carcinoma. Tsai et al.[ 15 ] also reported a high de novo malignancy rate in renal transplant tourism compared to that of domestic renal transplant recipients. The 10-year cumulative cancer incidence of the tourism group (21.5%) was significantly higher than that of the domestic group (6.8%), and the most common cancers were urothelium carcinoma and hepatocellular carcinoma. The high cancer incidence in the tourism group might be related to older age, more depleting antibody induction therapy, and omitted pre-transplant cancer screening procedures.

In liver transplants, patient survival was remarkably worse among overseas recipients. Overseas hepatocellular carcinoma patients had the worst prognosis compared with other groups. In Taiwan, to ensure standard quality, the NHI program reimburses live LT according to UCSF criteria [ 16 ] and cadaver LT according to Milan criteria [ 17 ]. In overseas LT, 64.1% had hepatocellular carcinoma before operation compared to 39.9% in domestic groups; but the hepatocellular carcinoma mortality rate was 69.0 compared to 8.2 per 1000 person-years (p<0.001), which implies that most overseas LT recipients were not suitable candidates for LT and inevitably had a high hepatocellular carcinoma recurrence rate and high mortality. Similar to our findings, Allam et al. also reported poor outcomes for LT patients who received transplantation in China, showing one- and three-year cumulative patient survival rates of 83% and 62%, respectively, compared to 92% and 84% in domestic hospitals [ 18 ]. The main reason for this discrepancy may be less prudent selection criteria for transplantation in China because 41 (55%) of the patients who received overseas transplantation had been denied liver transplantation at domestic hospitals due to multiple comorbidities, exceeding the age limit, or advanced hepatocellular carcinoma. In other words, some LT cases might not be medically indicated and some KT cases were clinically suboptimal for transplantation in the overseas groups, which might contribute to the poorer outcome of the overseas groups.

Transplant tourism in Asia and organs from executed prisoners

Surveys show that a remarkable number of people from many Asian countries in addition to Taiwan also traveled to China for transplantation: there were 462 KT and 504 LT cases from South Korea to China between 2001 and 2006 (19); 801 cases of KTs from Malaysia to China, which accounted for half of the country’s total KTs between 2002 and 2011 (20); and 752 cases of KT from Israel to the Philippines and China between 2001 and 2007 (21). Saudi Arabia also had 650 overseas KT, though not specifically mentioning which countries they went to (22). [ 19 – 22 ]. Although China is reforming its transplantation policy and has announced that it is no longer using organs from executed prisoners, critics have continued to question whether this practice has remained [ 23 ]. The WMA Statement on Organ and Tissue Donation (2012) indicates that “in jurisdictions where the death penalty is practised, executed prisoners must not be considered as organ and/or tissue donors. While there may be individual cases where prisoners are acting voluntarily and free from pressure, it is impossible to put in place adequate safeguards to protect against coercion in all cases” [ 24 ]. In relation to the commercial aspects of transplant tourism, the Declaration of Istanbul contains prohibitions against a range of practices, including “a ban on all types of advertising (including electronic and print media), soliciting, or brokering for the purpose of transplant commercialism, organ trafficking, or transplant tourism.” And the recently adopted “Convention against Trafficking in Human Organs” (2014) by the Council of Europe obligates ratifying states to criminalize “ trafficking in human organs” [ 25 ].

Taiwan and transplant tourism trends.

Overseas transplants increased rapidly after 2000, perhaps due to improved surgical techniques and transplantation outcomes, as well as to increased organ supply and brokering activity in China. In 2006, China admitted using organs from executed prisoners [ 10 ]—a practice prohibited by international professional societies and condemned by human rights groups. As the public, the media, and NGOs began to better understand the unethical nature of transplant tourism, pressure started to grow in Taiwan. While international organizations were exercising pressure on China and requesting legal reform on transplantation policy, Taiwan’s government prohibited medical personnel from involvement in any form of organ brokering. China passed its Human Organ Transplant Act in 2007. Since these policy changes, the number of transplant tourists from Taiwan to China has decreased remarkably. This might be due to an increased awareness of related ethical/legal controversies, but also due to the escalated expense of organ trafficking resulting from outlawing the organ trade, which led to reduced availability of organs (prices nearly doubled and even tripled according to the authors’ local survey).

In June 2015, Taiwan passed amendments to the Human Organ Transplantation Act. Organ brokers and patients receiving illegal organ transplants no matter domestically or overseas could face a maximum of five years imprisonment and a fine of up to USD 50,000. Criminalizing “patients” for illegal transplantation was disputed during the law amendment discussions (2013–2015). Some transplantation professionals, patient groups and Ministry of Health & Welfare expressed sympathy for patients who receive such transplantation and raised opposing opinion because patients might be desperate and hopeless while so doing. Yet the Ministry of Justice and human right organization supported such amendment based on the principle that human rights protection and punishment should be applied equally to brokers and buyers in an illegal organ trade [ 26 , 27 ]. After the Act passed, compulsory registration for overseas transplantation is required, which will promote transparency in transplant tourism and therefore may serve as a deterrent. Prohibiting using executed prisoners as organ donors to follow international guideline was implemented. Increased domestic organ donation strategies including “mandatory choice” and “required request” in deceased organ procurement policy, promoting “donation after circulatory death,” and allowing “paired exchange” were all included in the amended law [ 28 ]. Although it will take time to observe the amendments’ actual effects on transplant tourism, the overall trend has shown a reduction in numbers.

Policy suggestion for regulating transplant tourism in Asia

International guidelines concerning organ transplantation all call for adoption of a paradigm that involves governments taking national-level responsibility for fulfilling patients’ needs for organ donation and transplantation, and for ending unethical/illegal organ trafficking and commercialization [ 29 ]. In 2007, the Philippines prohibited foreigners from travelling to that country for transplantation, which quickly led to a remarkable decrease in such cases [ 30 ]. In 2008, Israel passed a law banning the sale, purchase, and brokerage of organs, both in Israel and abroad; and it has arrested brokers. As a result, transplant tourism to China from there seems to have ceased [ 31 ]. Despite these regulatory efforts in reducing organ tourism, the issue remains a complex, conflicting, ethical/legal challenge in many Asian countries. Politicians, patients, doctors, brokers, and other stakeholders have engaged in a power struggle to protect their respective interests, which in turn has made ethical and effective legislation difficult to accomplish. Comprehensive and enforceable national and international regulatory frameworks within Asian regions, which could be similar to the Convention against Trafficking in Human Organs (2014) by the Council of Europe, are indeed needed yet lacking. The WHO Guiding Principles on Human Cell, Tissue and Organ Transplantation (2010)—requiring relevant transplantation information to be open, accessible, and monitored—could serve as a reference, with enacting principles 10 and 11 (“traceability” and “transparency,” respectively) serving as the first step [ 32 ].

We therefore propose that Asian countries, as well as other countries involved with transplant tourism, adopt practical strategies and legislation so as to effectively reduce transplant tourism and organ trafficking. For example, they should:

Set up compulsory registration policies for overseas transplantation for monitoring this practice.
Sanction and punish all parties involved in organ trade and brokering.
Develop international and national legislation to criminalize and prevent all activities involving organ trafficking.
Develop an effective national organ procurement and donation policy so as to reduce the organ shortage and achieve national self-sufficiency in transplant organs.
Continue efforts to stop the use of organs from executed prisoners in China.

Strengths and limitations of this research

A strength of our study is that all the overseas transplant patients were identified and the results can be generalized. Additionally, the cohort is larger and with longer follow-up times (an 11-year cohort) than previous studies on transplant tourism (7,18). However, this study has several limitations. This is a retrospective study and recruited only overseas transplantation patients who survived, returned to Taiwan, and received anti-rejection therapies. Early intra-hospital mortality cases, in which the patients died after transplantation and failed to return to Taiwan, were not available in our research. This problem is common to all similar studies investigating the outcome of transplant tourism. To avoid overestimating the outcome of overseas transplants, we excluded domestic recipients who died within one month or who resumed dialysis within one month after the transplant operation to make the overseas and domestic groups more comparable. In addition to donor quality, some key variables in the LT models that had affected post-LT survival were not available, including various aspects of donor quality, pre-operative laboratory data, and the characteristics of hepatocellular carcinoma. Therefore, these confounding factors were not exclusively adjusted in the multivariable models. Due to the unethical nature of the transplant tourism sector, overseas transplant patients usually lack such clinical data and return home with only limited medical information, which hinders fair comparison and comprehensive research. However, the purpose of our study is not to find all the covariates affecting post-transplant survival in order to improve overseas transplants; rather, our study seeks to provide a picture of overseas transplants (trends, patient characteristics, and outcomes) in transplant tourism over the past decade in order to propose possible solutions to this important global health issue.

Our study gives a basic overview and describes problems of transplant tourism from Taiwan to China. The overseas transplant group had different demographic and clinical compositions than those of the domestic one; hence, the overseas group’s outcome is inferior. Although transplant tourism has decreased after the increased ethical awareness and establishment of relevant professional guidelines and policies, it still exists in many countries. We have reflected upon the ethical controversies of transplant tourism and proposed strategies for policy and legal reform based on recent professional and governmental efforts, as well as developments in Taiwan; these could be useful references for other Asian countries.

Supporting information

S1 table. numbers of domestic kidney and liver transplants, stratified by living and deceased status, april 2005–2015..

https://doi.org/10.1371/journal.pone.0178569.s001

Acknowledgments

This study was supported by the National Health Research Institutes, the Ministry of Science and Technology, and the Ministry of Health and Welfare of Taiwan. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author Contributions

Conceptualization: DFCT SWH CCH.
Data curation: SWH YPL YKC.
Formal analysis: SWH CCH YPL YKC.
Funding acquisition: DFCT SWH CCH.
Investigation: SWH CCH.
Methodology: DFCT SWH CCH.
Project administration: DFCT SWH CCH.
Resources: DFCT SWH CCH.
Software: SWH CCH.
Supervision: DFCT CCH.
Validation: DFCT SWH CCH.
Visualization: DFCT SWH CCH.
Writing – original draft: DFCT SWH.
Writing – review & editing: CCH SH.
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Clin J Am Soc Nephrol
v.3(6); 2008 Nov

Transplant Tourism in the United States: A Single-Center Experience

Jagbir gill.

* Division of Nephrology and § Department of Surgery, David Geffen School of Medicine at University of California, Los Angeles, and ‡ UCLA Immunogenetics Center, Los Angeles, California; and † Division of Nephrology, St. Paul's Hospital, University of British Columbia, Vancouver, British Columbia, Canada

Bhaskara R. Madhira

David gjertson, gerald lipshutz, j. michael cecka, phuong-thu pham, alan wilkinson, suphamai bunnapradist, gabriel m. danovitch.

Background and objectives: Transplant “tourism” typically refers to the practice of traveling outside the country of residence to obtain organ transplantation. This study describes the characteristics and outcomes of 33 kidney transplant recipients who traveled abroad for transplant and returned to University of California, Los Angeles (UCLA) for follow-up.

Design, settings, participants, & measurements: Posttransplantation outcomes were compared between tourists and a matched cohort of patients who underwent transplantation at UCLA (matched for age, race, transplant year, dialysis time, previous transplantation, and donor type). Median follow-up time was 487 d (range 68 to 3056).

Results: Compared with all patients who underwent transplantation at UCLA, tourists included more Asians and had shorter dialysis times. Most patients traveled to their region of ethnicity with the majority undergoing transplantation in China (44%), Iran (16%), and the Philippines (13%). Living unrelated transplants were most common. Tourists presented to UCLA a median of 35 d after transplantation. Four patients required urgent hospitalization, three of whom lost their grafts. Seventeen (52%) patients had infections, with nine requiring hospitalization. One patient lost her graft and subsequently died from complications related to donor-contracted hepatitis B. One-year graft survival was 89% for tourists and 98% for the matched UCLA cohort ( P = 0.75). The rate of acute rejection at 1 yr was 30% in tourists and 12% in the matched cohort.

Conclusions: Tourists had a more complex posttransplantation course with a higher incidence of acute rejection and severe infectious complications.

The demand for kidney transplantation continues to increase ( 1 , 2 ). Some patients opt to explore the option of kidney transplantation outside their country of residence ( 3 ). In the United States, the implications of this practice, often termed “transplant tourism,” remain largely unknown.

The observation of an increasing trend of patients who return from transplantations that are performed abroad led us to review the experience and outcomes with transplant tourism among patients who were followed in the UCLA Kidney Transplant program. We describe the characteristics and posttransplantation outcomes of patients who sought a transplant abroad and then returned to be followed at UCLA.

Materials and Methods

Study population.

We identified all living- and deceased-donor kidney transplant recipients who were followed at UCLA and underwent transplantation outside the United States as of April 2007 using the UCLA kidney transplant database. Patients who had moved to the United States after having a kidney transplant and nonkidney transplant recipients were excluded. One recipient of a kidney-pancreas transplant was identified.

Definitions

We used the term “tourist” to describe residents of the United States who underwent transplantation outside the United States and then returned to the United States for follow-up care, keeping in mind that we did not know all of the circumstances surrounding the recipients’ reason to pursue a transplant abroad.

Recipient race was categorized as per the Organ Procurement Transplant Network/United Network for Organ Sharing candidate and recipient registration forms ( 4 ). Overall allograft survival was determined from the date of transplantation until death or return to dialysis; patients were censored at the end of follow-up.

Study Design

Demographic recipient data; donor data (when available); transplant data (when available); and clinical events and outcomes including graft loss, patient death, acute rejection, serum creatinine measurements after transplantation, and infectious events were obtained using chart review. Patient data were verified with transplant staff and physicians, but patients were not directly questioned with regard to their transplants for the purpose of this study.

We first compared recipient and known transplant characteristics between tourists and all adult patients who underwent transplantation at UCLA during the study period. Overall graft survival, patient survival, incidence of acute rejection at 1 yr, and serum creatinine 1 yr after transplantation were compared between patients who underwent transplantation at UCLA and tourists.

Using the UCLA transplant database, we then identified a matched cohort of 66 adult patients (>21 yr) patients who underwent transplantation at UCLA during the study period, matched 2:1 with tourists for the following characteristics: Recipient age, race (Asian versus non-Asian), transplant year, previous transplantation, dialysis time, and donor type (living versus deceased). Overall graft loss, patient death, acute rejection, renal function, and infectious events were compared between tourists and the matched control subjects.

Statistical Analysis

Donor, recipient, and transplant characteristics were described using means ± SD or frequencies. Comparisons between groups were made using the t , Kruskal-Wallis, χ 2 , or Fisher exact test, as appropriate. Graft survival rates were estimated by the Kaplan-Meier product limit method, and the test for equality of survival curves was performed using the log-rank test. Propensity scores were calculated using logistic regression and were used to match the 33 tourists to 66 patients who underwent transplantation at UCLA. Comparisons with matched control subjects were performed using conditional logistic regression (using the clogit command). All P values were two-tailed. All analyses were conducted using Stata 9.0 (Stata Corp., College Station, TX).

Demographic Data

We identified 44 patients who underwent transplantation outside the United States and were subsequently followed at UCLA. Nine had immigrated to the United States after undergoing transplantation in their native country; therefore, 33 patients who had obtained a transplant abroad were residents of the United States. Twenty-nine of these individuals had been evaluated at UCLA before obtaining a transplant abroad. No pretransplantation data were available for two patients.

Transplant tourism was more common in recent years, with 67% of tourists having undergone transplantation between 2003 and 2007 ( Figure 1 ). Demographic data for tourists and all adult patients who underwent transplantation at UCLA during the study period are outlined in Table 1 . Tourists included mostly patients of Asian ethnicity and had a shorter median dialysis time before transplantation compared with patients who underwent transplantation at UCLA. Characteristics of the matched cohort are also outlined in Table 1 , demonstrating that the tourists and the matched group were well matched.

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Numbers of transplants tourism cases over time.

Characteristics of tourists, adult UCLA transplant recipients, and matched cohort of UCLA transplant recipients a

Country of Transplantation

Table 2 outlines the number of transplants performed in each country and the reported ethnicity of the transplant recipients. Most patients underwent transplantation in China, Iran, the Philippines, and India. Pakistan, Peru, Egypt, Turkey, Mexico, and Thailand accounted for a single transplant each. All but five patients traveled to regions of their ethnicity for transplantation.

Number of transplants and recipient ethnicity by transplanting country

Donor Information

Donor information beyond that of donor source was provided for only five patients, with donor age provided in three instances and HLA matching provided in two instances. Figure 2 illustrates donor type by transplanting country. With the exception of nine (27%) deceased-donor transplants performed in China, all transplants were living-donor transplants. The majority of these were reported as living unrelated donor transplants (61%), but the nature of the relationship between the donor and the recipient was unknown in most cases. Four (12%) living-related donor transplants were performed in India, Mexico, and Thailand. Of the living-related donors, two were cousins, one was a sibling, and one was unknown.

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Number of transplants by donor type and transplanting country. LURD, living-unrelated donor; LRD, living-related donor. Pakistan, Turkey, Peru, and Egypt all had a single LURD. Thailand and Mexico each had a single LRD.

Transplant Characteristics and Discharge Medications ( Table 3 )

Transplant immunosuppression: Tourists and UCLA transplants a

The median duration of hospitalization was 15 d; however, duration of hospitalization was unavailable for 15 (47%) patients. All patients were discharged on a calcineurin inhibitor; prednisone; and mycophenolate mofetil (90%), azathioprine (7%), or rapamycin (3%). Eight patients received induction therapy, and only 12 patients were reported to have received prophylaxis with sulfasoxazole/trimethoprim and four patients received cytomegalovirus (CMV) prophylaxis. Donor CMV status was unavailable for all patients.

Posttransplantation Outcomes

Outcomes after transplant for tourists and patients who underwent transplantation at UCLA are outlined in Table 4 .

Graft and patient outcomes of tourists and all patients who underwent transplantation at UCLA a

Condition on Arrival to UCLA

The median time after transplantation to initial visit at our center was 35 d (range 13 to 2769), and the median follow-up time was 487 d (range 68 to 3056). Three patients required immediate hospitalization, two of whom ultimately lost their grafts and required a transplant nephrectomy. The third patient had a complicated course with Gram-negative sepsis but retained allograft function. A fourth patient was first seen on admission to the intensive care unit (ICU) at UCLA 5 mo after transplantation with renal failure and fulminant hepatic failure.

Graft and Patient Survival among Tourists

Overall 1-yr graft survival (GS) and patient survival (PS) were not statistically different between tourists (GS 89.3%; PS 100%) and patients who underwent transplantation at UCLA (GS 94%; PS 96.4%); however, among the cohort of 66 matched UCLA patients, only a single graft loss and no deaths were reported during the follow-up period. Meanwhile, four tourists had allograft failure, and one of these patients died. The median time to graft loss for these patients was 132 d. The circumstances surrounding these four cases are outlined in Table 5 .

Graft losses among tourists a

Rejection, Primary Nonfunction, and Delayed Graft Function

Tourists had a higher cumulative incidence of acute rejection in the first year after transplantation (30%; n = 10) compared with patients who underwent transplantation at UCLA (15%; P = 0.02) and the matched cohort (12%; P = 0.2). No episodes of hyperacute rejection or primary nonfunction were reported. Three patients were reported to have an early acute rejection (before discharge from hospital after transplantation) and were all treated at the transplanting center. One of these patients ( Table 5 , patient 2) did not regain renal function and subsequently returned to the United States, where he was initiated on hemodialysis and underwent allograft nephrectomy.

Five patients had an acute rejection within the first 6 mo of transplantation after discharge, with one patient not regaining renal function (patient 1). Three additional patients had an episode of acute rejection between 6 mo and 1 yr.

One patient (who received a deceased-donor kidney in China) was reported to have experienced delayed graft function and required dialysis for 3 wk after transplantation. This patient had a prolonged hospitalization in China as a result of anemia but ultimately regained and retained stable renal function.

The mean serum creatinine levels at 1 mo, 6 mo, and 1 yr after transplantation were not significantly different in tourists compared with all patients who underwent transplantation at UCLA and the matched cohort.

Infectious Complications

Infectious complications are outlined in Table 6 . The overall incidence of an infectious event was not different in tourists compared with the matched cohort of UCLA patients; however, the severity and types of infections were markedly different. Seventeen (52%) tourists had at least one infectious complication, with three patients having had two or more infectious episodes. Twelve (36%) patients were hospitalized, and an infectious cause was listed as the primary cause of hospitalization in nine (27%) cases. By comparison, only six (9%) of the 66 matched control subjects required hospitalization for infectious complications after transplantation. The median duration of hospitalization among tourists was 12.5 d (range 1 to 744), with two patients requiring multiple hospitalizations for recurrent infections. Three patients required ICU admission: One was admitted to a hospital in Iran a short period after transplantation for CMV pneumonia and consequently developed respiratory failure; another was hospitalized with Gram-negative sepsis and acute respiratory distress syndrome (patient 1); the third patient ultimately died as result of fulminant hepatic failure after presumably contracting hepatitis B from her donor (patient 4).

Infectious complications after transplantation a

Viral Infections

Ten (30%) patients developed CMV infection after transplantation, and six of these patients were hospitalized as a result. Of the 10 patients with CMV infection, six had CMV viremia alone that responded well to treatment, and they retained stable renal function. A seventh patient developed CMV viremia after a course of lymphocyte-depleting therapy for acute rejection. An eighth patient had mild disease limited to the urinary tract. CMV was considered a contributory cause of interstitial nephritis and resultant graft loss in one case (patient 2). One additional patient developed CMV pneumonia along with bacterial sepsis and ultimately lost his graft (patient 1).

None of the 10 patients who developed CMV infection had received prophylaxis at the time of transplantation. Donor CMV status was not provided in any of these cases. In the matched cohort, a markedly lower proportion of patients had reported CMV infections (12%), one of whom developed severe disease that required ICU admission for respiratory failure secondary to CMV pneumonitis.

Bacterial Infections

Compared with the matched cohort, there seemed to be a lower incidence of bacterial infections among the tourists; however, many bacterial infections in the matched cohort occurred within the first month after transplantation, and we did not have sufficient data in the first month after transplantation for the tourists.

Among the tourists, four (12%) patients developed a bacterial urinary tract infection (UTI). UTI was the primary cause of hospitalization for one of these patients and may have contributed to the development of Gram-negative sepsis in two additional cases. One of these patients subsequently developed a vancomycin-resistant enterococcal perinephric abscess that required surgical intervention. In the matched cohort, there was a higher proportion of UTI (21%), but bacteremia secondary to UTI was seen in only one case and did not result in hemodynamic compromise.

There was a single case of pneumonia in the tourist group, reported to occur at the time of transplantation in Iran. The lone kidney-pancreas transplant recipient developed a peripancreatic abscess that required surgical drainage and a prolonged hospitalization.

Surgical Complications

Surgical complications were generally uncommon. Four (12%) tourists had one or more surgically related complications, including lymphocele, ureteric stricture, transplant renal artery stenosis, and a perinephric abscess. There were no reported episodes of urine leaks or acute surgical complications.

The disparity between the supply and demand for kidney transplantation remains a preeminent issue in transplantation. The dire implications of this disparity on patient outcomes are clear to both members of the transplant community and the thousands of patients who are waiting for kidney transplantation. As the transplant community struggles to meet the increasing demand for transplantation, some patients have turned to countries outside their country of residence to obtain an organ transplant ( 3 , 5 – 9 ). The risks and implications of this practice, often termed “transplant tourism,” have been difficult to assess in the United States because of the variable experiences and limited numbers of patients at a single center. In recent years we have noticed an increase in the number of tourists who present for follow-up care at our center after having obtained a transplant abroad, and we were concerned by the seemingly high rate of complications that we observed. We identified 33 California residents during a 10-yr span, most of whom had been evaluated for transplantation at our center, who underwent transplantation abroad and then returned to our center after transplantation for medical follow-up. More than two thirds of tourists whom we identified had received a transplant in the preceding 4 yr, representing a significant increase in recent years. This supports recent data by Merion et al. ( 8 ) that indicated a tripling in the number of identified tourists who returned to the United States from 2000 to 2006. We were unable to identify recipients’ reasons for traveling abroad, making it difficult to determine whether longer wait times for transplantation, a reluctance or an inability to pursue living-related donors, or a combination of these and other factors are driving this phenomenon.

Who Are Tourists, and Where Do They Go?

Compared with patients who underwent transplantation at UCLA, tourists included a larger proportion of Asian-American patients, and most patients traveled to the region of their ethnicity to obtain transplantation. Although this may be a reflection of the large Asian population that resides in Southern California, it is in keeping with other reports on commercial transplantation in North America. In a Canadian series, patients who were born outside Canada (mostly South Asian and East Asian) were more likely to obtain a kidney transplant abroad ( 7 ). Similarly, the recent analysis of the United Network for Organ Sharing data found that patients of Asian ethnicity were the largest ethnic group to obtain transplants abroad ( 8 ). That most patients traveled to regions of their ethnicity may suggest a greater degree of comfort in traveling to a familiar region to obtain medical care. The cultural issues that may relate to why patients of certain ethnic groups are more or less willing to travel abroad for transplantation is not well understood and warrants further examination.

In our analysis, tourists also had a substantially lower mean dialysis time before transplantation compared with patients who underwent transplantation at UCLA, suggesting that many patients may have considered the option of transplantation before initiation of dialysis. This may also reflect a lack of potential living donors or a reluctance to consider family members as living donors, although we have no specific data to address this issue.

Most patients traveled to Asia or the Middle East to obtain transplantation, with most traveling to China. Indeed, in the aforementioned report by Merion et al. ( 8 ), Asia and the Middle East were the transplanting regions in >60% of identified tourism cases.

Living-donor transplants were most common. The lack of documentation from transplanting centers made it difficult to determine accurately how many of the reportedly living-unrelated transplants were performed using organs from vendors; however, the reported prevalence of vendor-driven transplantation in the Middle East and Asia ( 10 , 11 ) may lead us to believe that most of these have been using organs from vendors. In addition, nine deceased-donor transplants were performed in China, with no further information provided regarding the donor, leaving us to presume that executed prisoners were the source of these organs ( 12 , 13 ).

Of note, four US residents traveled abroad to receive living-related transplants, including two from siblings. This begs the question, why was it easier for these patients to travel abroad rather than coordinate a transplant in the United States from their related donors? Addressing these limitations may help to facilitate local transplantation for patients with related donors abroad.

Documentation and Communication with Transplanting Center

In our experience, a major source of frustration was the lack of complete documentation from the transplanting center, echoing the sentiments reported in previous such analyses ( 6 , 7 ). Most centers provided information on the date of transplantation, discharge immunosuppression, and the serum creatinine level upon discharge from the hospital. Beyond the provision of a generic donor category, no information was provided regarding the general health, age, or viral status of the donor. Furthermore, few details regarding transplantation, including cold-ischemic time, warm-ischemic time, and HLA matching status, were provided.

Reasonable Outcomes after Transplantation but not without Risk

One-year graft and patient survivals were not statistically different between tourists and all patients who underwent transplantation at UCLA. Given that tourists had the lower risk characteristics of shorter dialysis times and more living-donor transplants, it is difficult to draw firm conclusions from this unadjusted comparison. To compare better the posttransplantation outcomes between tourists and patients who underwent transplantation locally and had similar characteristics, we performed a matched analysis comparing tourists with a cohort of patients who underwent transplantation at UCLA matched for age, race, gender, donor source, and transplant year. Although low event rates limited the statistical power of the matched analysis, there seemed to be a trend toward worse outcomes among tourists. Compared with a single graft loss in the matched cohort, there were four cases of graft loss, including one patient death in the tourist group, suggesting that graft and patient survivals may be inferior among tourists. It is important to recall that we had data only on tourists who ultimately returned for follow-up, potentially excluding patients who died early after transplantation.

Variable results regarding graft and patient outcomes have been reported in the past ( 5 , 9 , 14 , 15 ). Prasad et al. ( 7 ) reported inferior graft and patient survival among recipients of commercial living-donor transplants compared with living-unrelated donor transplants performed in Toronto. Meanwhile, Canales et al. ( 6 ) reported a single graft loss and patient death in their series of 10 patients who returned to the United States after undergoing transplantation abroad.

In addition, we found that the rate of acute rejection in the first year after transplantation was higher among tourists compared with the matched cohort. This may reflect underimmunosuppression or inconsistent monitoring of immunosuppressive drug levels early after transplantation. There was no documentation relating to immunosuppressive monitoring in our series.

We found an increased incidence of severe infectious complications that required hospitalization and ICU management among tourists compared with the matched cohort of patients who underwent transplantation at UCLA. The higher incidence of infectious complications is consistent with previous reports ( 4 , 6 , 7 , 15 , 16 ) and may reflect a series of issues relating to tourism, including the increased complexity of immunosuppressive management during the transition of care from the transplanting center to our center as a result of the lack of communication and information, the lack of infectious prophylaxis administered early after transplantation, the varying infectious disease profiles of different countries, and the unclear mechanism of donor evaluation.

CMV infection was much more common among tourists and contributed to significant morbidity in three cases and graft loss in one case. This may not be surprising, because the majority of patients did not receive CMV prophylaxis until they returned to our center. Perhaps routine improved donor screening and routine infectious prophylaxis may have resulted in improved outcomes in these cases. Conversely, routine bacterial infections seemed to be less frequent in the tourism group but were likely underreported in tourists because we first saw tourists an average of 35 d after transplantation.

The lone death in our series was attributed to complications from donor-contracted hepatitis B and raises serious concerns regarding the donor selection process. In an examination of characteristics and outcomes among organ vendors in Pakistan, Naqvi et al. ( 17 ) reported that 25% of organ vendors identified were positive for hepatitis B or C on follow-up, with nearly 8% reporting a history of jaundice and nearly 30% of infected vendors requiring active treatment. It is unclear what proportion of these vendors were infected before donation, but reports of hepatitis among tourists in previous studies ( 5 , 15 ) and ours suggest that this is a significant issue.

Is Transplant Tourism a Public Health Issue?

The potential for acquiring infectious diseases that are endemic to different regions of the world through transplant tourism is an important consideration from both a clinical and a public health perspective. The unclear circumstances under which donors are selected and the increase in organ vending practices in certain regions of the world contribute further to this concern. Reports from Turkey and the United Arab Emirates described among tourists infectious complications that were unusual for their respective regions, including tuberculosis, malaria, and aspergillosis ( 9 , 15 ). This highlights the potential impact of transplant tourism on the infectious disease profiles of the countries to which tourists return and clearly indicates a need to examine the impact of transplant tourism from a public health perspective.

Trust and the Doctor–Patient Relationship

The safe and ethical practice of transplantation, particularly from living donors, is contingent on a trustworthy doctor–patient relationship ( 18 ). The “patient” in this case refers to both the recipient and the living donor. Of the 29 tourists who had been evaluated for transplantation in our center, very few had expressed their plans to travel abroad for transplantation. Furthermore, the details and circumstances surrounding donor selection and transplantation were largely unclear. Detailed discussion regarding the ethical implications of transplant tourism and the concern for the health of donors are beyond the scope of this article and have been the source of discussion in many recent reports and editorials ( 19 – 24 ); however, that this practice undermines trust in the doctor–patient relationship has significant implications for the treatment of returning patients and the maintenance and evolution of the doctor–patient relationship in transplantation.

Limitations

In interpreting these results, readers must consider the limitations that are inherent to retrospective observational studies. We cannot account for a possible selection bias in the analysis of retrospective data, because we have information only on patients who underwent transplantation and ultimately returned to our center. Furthermore, data and outcomes in the first month after transplantation were largely obtained from patient accounts and information provided from the transplanting center, which were often incomplete and may be subject to recall bias. The matched analysis was limited by the relatively small number of tourists, low event rates, and a lack of donor factors provided by the transplanting center. Last, the findings of our experience may be reflective only of our experience and may not be generalizable to other centers or regions in the United States.

Conclusions

Transplant tourism seems to be increasing over time, with most patients traveling to regions of their ethnicity. Graft and patient survival do not seem to be significantly worse among tourists who return, but transplantation abroad is associated with a more complex posttransplantation course with a higher rate of acute rejection and increased severity of infectious complications after transplantation. Transplant tourism is a risky option for patients who are awaiting kidney transplantation, and its implications on public health warrant further evaluation.

Disclosures

Published online ahead of print. Publication date available at www.cjasn.org .

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Transplant Tourism - Patients Travel Around the U.S. for their Best Transplant Options

Transplant tourism: a growing phenomenon

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Transplant Tourism: The Shadow World of Medicine

The Burden of International Organ Trade

Forms of International Organ Trade

Risks of Transplant Tourism

The Way Out

Bottom Line

Exploring the Surge of Cosmetic Tourism: Trends and Considerations in Aesthetic Procedures Abroad

Transplant tourism

Publication types

The outcomes and controversies of transplant tourism—Lessons of an 11-year retrospective cohort study from Taiwan

Methods and findings

Introduction

Subjects and methods

Study subjects

Statistical analysis

Numbers of transplants and trends

Demographic comparison

Clinical outcome

Features of transplant tourism from Taiwan to China

Patient and graft survivals.

Malignancy.

Transplant tourism in Asia and organs from executed prisoners

Taiwan and transplant tourism trends.

Policy suggestion for regulating transplant tourism in Asia

Strengths and limitations of this research

Supporting information

Acknowledgments

Author Contributions

Transplant Tourism in the United States: A Single-Center Experience

Bhaskara R. Madhira

Materials and Methods

Definitions

Study Design

Statistical Analysis

Demographic Data

Country of Transplantation

Donor Information

Transplant Characteristics and Discharge Medications ( Table 3 )

Posttransplantation Outcomes

Condition on Arrival to UCLA

Graft and Patient Survival among Tourists

Rejection, Primary Nonfunction, and Delayed Graft Function

Infectious Complications

Viral Infections

Bacterial Infections

Surgical Complications

Who Are Tourists, and Where Do They Go?

Documentation and Communication with Transplanting Center

Reasonable Outcomes after Transplantation but not without Risk

Is Transplant Tourism a Public Health Issue?

Trust and the Doctor–Patient Relationship

Limitations

Conclusions

Disclosures

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