The outcomes and controversies of transplant tourism—Lessons of an 11-year retrospective cohort study from Taiwan
The outcomes and controversies of transplant tourismÐLessons of an 11-year retrospective cohort study from Taiwan
Daniel Fu-Chang Tsai 0 1
Shi-Wei Huang 1
Soren Holm 1
Yi-Ping Lin 1 5
Yu- Kang Chang 1 3 4
Chih-Cheng Hsu 1 2 4
0 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 , 2 Department of Urology, National Taiwan University Hospital Yunlin Branch , Yunlin, Taiwan , 3 School of Law, University of Manchester , Manchester , United Kingdom
1 Editor: Stanislaw Stepkowski, University of Toledo , UNITED STATES
2 Department of Health Services Administration, China Medical University , Taichung , Taiwan
3 Department of Medical Research, Tungs' Taichung Metro Harbor Hospital , Taichung , Taiwan
4 Institute of Population Health Sciences, National Health Research Institutes , Zhunan , Taiwan
5 Office of Health Care Policy Research, Koo Foundation Sun Yat-Sen Cancer Center , Taipei , Taiwan
Data Availability Statement: 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 ªPersonal Information
Protection Actº, 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/
Funding: This work was supported by the National
Health Research Institutes, Ministry of Science and
Methods and findings
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
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 fail
ure. 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
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.
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.
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 [
tourism was estimated to account for 10% of organ transplants performed around the world in
]. Such practice, though saving lives, has been discouraged by many international
organizations because it involves the exploitation of vulnerable groups and the poor [
Taiwan's hepatitis B carrier rate and the country's prevalence and incidence of renal dialysis
are among the world's highest [
]. 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 [
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 [
]. 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 [
], 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 [
in 2008, the Declaration of Istanbul prohibited transplant tourism [
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 ªHow are patients who
engaged in transplant tourism different from other patients?º and ªAre there differences in the
outcomes for overseas and domestic transplants?º 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 [
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
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Subjects and methods
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.
Those who received KT or LT were divided into two groups: ªdomestic recipientsº (Taiwanese
receiving a transplant in Taiwan) and ªoverseas recipientsº (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
NHIbased registry of catastrophic illness to exempt co-payment, and transplantation, cancer and
dialysis were all included in the designated categories of catastrophic illness. The
transplantrelated 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
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 [
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,
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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 [
]. 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).
Fig 1. Number of domestic vs overseas transplants, 1998±2014. (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.
[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).
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
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).
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.
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Note: Results are n (%) or means (SD).
CCI = Charlson comorbidity index.
* The chance to reject null hypotheses, assuming no difference in demographic characteristics between patients receiving a kidney transplant in Taiwan
and patients receiving a kidney transplant overseas, by using chi-square tests (for categorical data), Student's t-tests (for continuous data), and log-rank
tests (for patient and graft survival rate).
² The diagnoses recorded in the National Health Insurance dataset within 1 year (excluding the index hospitalization for the kidney transplant) before
receiving a kidney transplant was used to calculate CCI score. Because patients undertaking dialysis de®ned our study cohort, we excluded the diagnosis of
renal failure (de®ned as at least three outpatient service claims or one single hospitalization) from index calculations.
# the patient resumed dialysis but was still alive.
$ January 1, 1998 to June 30, 2009, excluding domestic graft failure and those who died within one month.
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*TThe chance to reject null hypotheses, assuming no difference in demographic characteristics between patients receiving a kidney transplant in Taiwan
and patients receiving a kidney transplant overseas, by using chi-square tests (for categorical data), Student's t-tests (for continuous data), and log-rank
tests (for patient and graft survival rate).
² The diagnoses recorded in the National Health Insurance dataset within 1 year (excluding the index hospitalization for the liver transplant) before receiving
a liver transplant was used to calculate CCI score and indication of liver transplant. When calculating CCI score, we excluded diagnoses of mild hepatitis,
moderate hepatitis, and hepatocellular carcinoma from index calculations. The diagnosis was de®ned as at least three outpatient service claims or one
$ Excluding domestic patients who died within one month.
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,
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Fig 2. Kaplan±Meier estimates of survival for overseas vs domestic transplant recipients. (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.
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*Hazard ratio (HR) was used to estimate excess risks of mortality and graft failure for those receiving transplants overseas vs domestically, by using a
multivariable Cox proportional hazards regression model adjusted for age, sex, hemodialysis duration prior to transplantation, CCI score, and location of
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
Patient and graft survivals. Two previous studies show that the clinical outcomes of
overseas KTs were comparable to those of domestic KTs after 2000 [
]; 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 ªqualityº 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.[
] 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
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* Hazard ratio (HR) was used to estimate excess risks of mortality for those receiving transplants overseas vs domestically, by using a multivariable Cox
proportional hazards regression model adjusted for age, sex, CCI score.
$ 0±45 as reference because sparse data in <18 y/o strata.
(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
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 [
] and cadaver LT according to Milan criteria [
]. 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 [
]. 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
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The causes of mortality were primarily de®ned as the principal diagnosis when patient expired unless some vague diagnoses for nosology such as
cardiovascular symptoms (ICD9 = 785) or other disease of lung (ICD9 = 518). In these cases, we chose the second diagnoses to de®ne the causes of
The mortality rate was estimated by cases per 1000 person-years, which were calculated as the time elapsed from the transplantation to the death date, or
the end of follow-up, whichever came ®rst. The calculation of a 95% CI for the mortality rate was based on the Poisson distribution.
*Causes of death in kidney transplantation: Liver disease-included liver cirrhosis, acute hepatitis, hepatic failure; chronic kidney failure include
-complication after kidney transplantation, chronic kidney failure and kidney transplantation. Others-include cardiovascular and cerebrovascular accident,
GI disease (intestinal perforation, pancreatitis, peritonitis) and others.
& Malignancy in overseas vs. domestic: genitourinary malignancy: 39 vs 12, hepatocellular carcinoma: 29 vs 6, others: 37 vs 15.
²Cause of death in liver transplantation: liver disease include hepatic failure, and side effect of hepatic failure. Others include tumor except hepatocellular
carcinoma, cardiovascular, cerebrovascular accident and GI disease.
#IRR (incident rate ratio) was used to assess association between cause of death and the transplant operation sites (overseas vs. domestic) by using
Poisson regression model adjusted for age, sex, and CCI score.
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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 [
]. The WMA Statement on Organ and Tissue Donation (2012)
indicates that ªin 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 casesº . In relation to the commercial aspects
of transplant tourism, the Declaration of Istanbul contains prohibitions against a range of
practices, including ªa 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.º And the recently adopted ªConvention against Trafficking in Human
Organsº (2014) by the Council of Europe obligates ratifying states to criminalize ªtrafficking in
human organsº [
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 [
]Ða 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 ªpatientsº 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 [
]. 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 ªmandatory choiceº and ªrequired requestº in deceased organ procurement
policy, promoting ªdonation after circulatory death,º and allowing ªpaired exchangeº were all
included in the amended law . Although it will take time to observe the amendments'
actual effects on transplant tourism, the overall trend has shown a reduction in numbers.
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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
]. In 2007, the Philippines prohibited foreigners from travelling to that
country for transplantation, which quickly led to a remarkable decrease in such cases [
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 [
]. 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)Ðrequiring
relevant transplantation information to be open, accessible, and monitoredÐcould serve as a
reference, with enacting principles 10 and 11 (ªtraceabilityº and ªtransparency,º respectively)
serving as the first step .
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:
1. Set up compulsory registration policies for overseas transplantation for monitoring this
2. Sanction and punish all parties involved in organ trade and brokering.
3. Develop international and national legislation to criminalize and prevent all activities
involving organ trafficking.
4. Develop an effective national organ procurement and donation policy so as to reduce the
organ shortage and achieve national self-sufficiency in transplant organs.
5. 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
intrahospital 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.
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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.
S1 Table. Numbers of domestic kidney and liver transplants, stratified by living and
deceased status, April 2005±2015.
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
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.
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Visualization: DFCT SWH CCH.
Writing ± original draft: DFCT SWH.
Writing ± review & editing: CCH SH.
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