Review

Transplant tourism: a literature review on development, ethical and law issues

Le Chi Conga,, Linh Tranb,c,https://orcid.org/0000-0001-8667-082X, Le Thi Phong Land,, Giang Jan Nguyenehttps://orcid.org/0000-0002-0527-7055, Mohamed Essam Elrggalfhttps://orcid.org/0000-0002-7049-4777, Nguyen Hai Namghttps://orcid.org/0000-0001-5184-6936, Nguyen Tien Huyh,*https://orcid.org/0000-0002-9543-9440, Nguyen Duc Truongi,*https://orcid.org/0000-0002-9315-1611
Author Information & Copyright
aNephrology-Hemodialysis Department, Universisty Medical Center, Ho Chi Minh City, Vietnam
bInstitute of Fundamental and Applied Sciences, Duy Tan University, Ho Chi Minh City, Vietnam
cFaculty of Natural Sciences, Duy Tan University, Da Nang City, Vietnam
dDepartment of Radiology, Phuong Chau International Hospital, Can Tho, Vietnam
eAmerican University of Antigua College of Medicine, St. John’s, Antigua and Barbuda, US
fNephrology Department, Kidney and Urology Center, Alexandria, Egypt
gDivision of Hepato-Biliary-Pancreatic Surgery and Transplantation, Department of Surgery, Graduate School of Medicine, Kyoto University, Kyoto, Japan
hDepartment of Clinical Product Development, Institute of Tropical Medicine (NEKKEN), School of Tropical Medicine and Global Health, Nagasaki University, Nagasaki, Japan
iDepartment of Obstetrics and Gynecology, FV Hospital, Ho Chi Minh City, Vietnam
*Address correspondence to Nguyen Duc Truong at the Department of Obstetrics and Gynecology, FV Hospital, Ho Chi Minh City, Vietnam; E-mail: nguyenductruongdr@gmail.com

⊕ Authors equally contributed to the work

© Copyright 2023 MedPharmRes. This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Received: Feb 08, 2022; Revised: May 04, 2022; Accepted: May 30, 2022

Published Online: Mar 31, 2023

Abstract:

Objectives:

This study aims to narratively review the progression of ethical and legal issues related to transplant tourism.

Methods:

PubMed search and Google search with keywords were used in March 2022 to identify relevant studies and law documentation.

Results:

The progression of transplant tourism was classified into three main periods. Before 2000, the most popular destination country was India (1,308 cases), this period was characterized by the absence of laws and regulations worldwide. The period from 2000 to 2010 was the peak explosion of transplant tourism, China became the most popular destination of tourists (7,591 cases). This triggered alarms by World Health Organization (WHO) resolution in 2004 and Istanbul declaration in 2008 calling for regulations to prohibit transplant tourism. From 2010 till today, additional scientific publications reported several complications in overseas transplanted patients. Laws and regulations restricting transplant tourism were promulgated by many countries such as Israel, Taiwan, Spain and others.

Conclusions:

Transplant tourism is considered as illegal worldwide. WHO and many developed countries announced laws and measures to prevent this activity. The incidence of transplant tourism is currently decreasing, continued efforts should persist to end this criminal act.

Keywords: ethics; legislation; organ harvesting; transplant tourism; progression

1. INTRODUCTION

Organ transplantation is an option in the treatment for organ failure. It has saved the lives of millions of patients with end-stage organ failure. However, donated organs are not sufficient to cope with the rising number of demanding patients. The data from the Global Observatory on Donation and Transplantation (GDOT) program demonstrated a substantial increase in the total number of transplanted cases over the years in 111 involved countries; however, donated organs only met 10% of the organ transplant demand [1]. This disparity between organ demand and organ supply has led to the emergence of organ trading and transplant tourism (TT), which accounted for 5-10% of total transplanted cases at that time, according to World Health Organization (WHO) [2]. This term, TT, emerged to describe the surge of wealthy foreigners arriving in India and other countries in search of organs for a price in the late 1980s. India was the most popular destination for commercial transplants at that time [3].

TT was first globally described in the WHA57.18 resolution of WHO in 2004, which called for measures to protect poor people who are the most vulnerable group from this activity. The resolution included drawing attention to the wider problem of international trafficking of human tissues and organs [4].

In 2008, TT and other related terms were defined in the Istanbul declaration [5], then it was revised in 2018 as follows: travel for transplantation is the movement of persons across jurisdictional borders for transplantation purposes. Travel for transplantation becomes TT, and thus unethical, if it involves trafficking in persons for the purpose of organ removal or trafficking in human organs, or if the resources (organs, professionals and transplant centers) devoted to providing transplants to non-resident patients undermine the country’s ability to provide transplant services for its own population [6].

To better classify TT, Yosuke Shimazono has described four different modes of TT and explained the various activities of recipients, commercial living donors, and involved transplant centers at Second Global Consultation on Human Transplantation, WHO headquarters meeting in Geneva in 2007 [7]. Among those modes, mode 1 describes a recipient traveling from country B to country A where both the donor and transplant center were located. Mode 2 describes a donor from country A traveling to country B where the recipient and transplant center were both located. Mode 3 demonstrates both a donor and recipient from country A traveling to country B where the transplant center was located, and mode 4 represents a donor from country A and a recipient from country B both traveling to another country where the transplant center was located [5] (Figure 1).

mpr-7-1-27-g1
Figure 1. Four different modes of international organ trade and organ trafficking. Adapted from (Shimazono March 28-30, 2007)
Download Original Figure

Two full reports about TT were published by researchers of European Union [8] and Council of Europe [9]. These reports described in detail the illegality of TT and declared it condemned by the Council of Europe, WHO, World Medical Association (WMA) and the Transplantation Society. The practice is unethical because of two points: harms on donors and the unethical practice or organ harvesting. In this review, we aim to characterize the progression of TT, describe the ethical issues and legislative implementation.

2. MATERIALS AND METHOD

This review was conducted by searching on PubMed database using the term “transplant tourism” for original research or reviews. Ancestry searches were also conducted by reviewing the references section of all worthwhile articles to identify additional studies on the topic until March 2022. Related legislation and policies were searched by using Google search with keywords including “legislation,” “law,” “organ trafficking,” “organ harvesting,” and “organ abuse” in March 2022.

3. RESULTS AND DISCUSSION

A total of 103 original studies (Table 1) and three websites related laws and policies [10-12] were identified. Among these publications, 16 studies were excluded for under-reporting of the number of transplanted patients and the year of transplantation; while 87 studies were included (Figure 2).

Table 1. Destination of transplant tourist
Destination of transplant tourist before 2000.
Author Year of publication Year of transplantation Number of Patients Resident Country of transplant
Akpolat and Ozturk [13] 1998 1991–1994 12 Turkey India (12)
Al Asfari [13] 1995 1988–1993 38 Syria India (38)
Al-Wakeel [13] 2000 1990-1996 57 Saudi Arabia India (37), Egypt (14), USA (5), Pakistan (1)
Al-Wakeel [13] 2000 1998–2001 51 Saudi Arabia India (51)
Ben Hamida [13] 2001 1995–1999 20 Tunisia Iraq (14), Egypt (3), Pakistan (3)
Chien [14] 2000 1991–1998 100 Taiwan China (100)
Colakoglu [13] 1998 1991–1995 127 Turkey India (127)
Friedlaender [13] 1993 1988–1992 36 Israel India (36)
Fukushima [14] 2013 1992 1 Japan USA
Hussein [13] 1996 1984–1994 56 Saudi Arabia India (56)
Johny [13] 1990 1985–NW 53 Kuwait India (49), Egypt (2), Philippines (1), Iraq (1)
Kennedy [13] 2010 1990–2004 13 Australia India (3), China (6), Iraq (1), Philippines (1), Lebanon (1), Eastern Europe (1)
Lei [13] 1992 1986–1991 101 Malaysia India (101)
Morad [13] 2000 1990–1996 515 Malaysia India and China
Prabhakar [13] 2000 1986–1991 115 Singapore India (115)
Salahudeen [13] 1990 1984–1988 130 United Arab Emirates, Oman India (130)
Sanal [35] 2004 1995, 1992 2 Turkey Russia, India
Sever [13] 1994 1992–1993 34 Turkey India (34)
Sever [13] 2001 1992–1999 115 Turkey India (106), Iraq (7), Iran (2)
Destination of transplant tourist 2000-2010
Author Year of publication Year of transplantation Number of Patients Resident Country of transplant
Adamu [14] 2012 2006–2009 45 NW Pakistan (28), Egypt (10), Philippines (6), China (1
Ahn [36] 2018 2000-2010 1576 Korea China (1528)
Alghamdi [13] 2010 2003–2008 93 Saudi Arabia Pakistan (46), Philippines (26 Egypt (11), USA (3), China (2), Iran (2), Syria (1), Lebanon (1), Jordan (1) USA (10), UK (6)
Allam N [14] 2010 2001-2007 74 Saudi and Egyptian China (74)
Berglund [14] 2012 2005-2006 3 Sweden Pakistan (2), Iran (1)
Canales [13] 2006 2002-2006 39 USA Pakistan (8), China (1), Iran (1)
Canales [13] 2006 2002–2006 10 United States Pakistan (8), China (1), Iran (1)
Cha [14] 2011 200-2009 87 South Korea China
Chung [14] 2010 2002-2008 69 South Korea Philippines (3), China (66)
Chung MC [14] 2014 1999-2009 2309 Taiwan China (2309)
Cronin [14] 2011 2000-2009 245 UK Pakistan (121), India (48), China (12), Philippines (8), Iran (8), Egypt (7), USA (4), NW (37)
Dulal [14] 2008 2003-2008 452 Nepal India (449), Germany (2), USA (1)
Geddes [14] 2008 2000–2007 18 Scotland Pakistan (18)
Gill [14] 2011 2000-2007 93 Canada China (39), India (14), Iran (5), Philippines (16), Pakistan (11)
Gill J [14] 2008 1995-2007 33 Canada China (14), Philippines (4), India (3), Pakistan (1), Iran (6), Peru (1), Egypt (1), Turkey (1), Mexico (1), Thailan (1)
Goh BI [37] 2012 2000-2012 1117 Malaysia China (1005), India (67), Other (45)
Hsu CC [14] 2011 2001-2003 398 Taiwan China (398)
Ivanovski N [14] 2011 2006-2007 36 Bailkan Pakistan (36)
Kapoor [14] 2011 2001–2007 10 Canada China (4), Pakistan (3), India (1), Philippines (1), Mexico (1)
Kwon CH [14] 2011 2000-2005 966 Korea China (966)
Leung [14] 2007 2001-2007 12 Hong Kong China (12)
Malakoutian [14] 2007 2005–2006 NW Iran Iran
Merion RM [14] 2008 2001-2006 373 USA China (26) Philippines (12), India (10), Pakistan (4)
Polcari [14] 2011 2001-2007 9 USA China (3), Pakistan (3), Philippines (1), India (2)
Quach K [38] 2016 2000-2011 45 Canada China (36)
Scheper-Hughes [14] 2006 2003 1 USA South Africa
Shimizu [14] 2007 2006 1 Japan NW
Shoham [14] 2010 2006 19 USA Asia or Middle East (11), India (3), Pakistan (2), Philippines (1), Lebanon (1), Iran (1)
Solak [39] 2012 2003–2010 14 Turkey Egypt (5), Iraq (4), Pakistan (2), Russia (2), India (1)
Tsai [14] 2014 2003-2009 307 Taiwan China (307)
van Balen [14] 2016 2000-2009 22 Kosovo, the Netherlands, and Sweden Pakistan (14) India (4) China (1) Russia (1) Columbia (1) Iran (1)
Vathsala [14] 2009 2001–2006 209 Singapore NW
Zargooshi [14] 2008 2006–2007 100 Iran Iran
Destination of transplant tourist 2010 to date
Author Year of publication Year of transplantation Number of Patients Resident Country of transplant
Ahn HJ [36] 2018 2011-2016 151 Korea China (146)
Al Salmi I [40] 2018 2013-2015 158 Qatar Pakistan (142), China (12), Egypt (2), Iraq (2)
AlBugami MM [41] 2017 2013-2016 86 Audi Arabi Egypt (46), Iran (16), China (13)
Okafor [42] 2017 2008-2015 126 Nigeria India (113), UK (4); Pakistan (2), USA (1)
Wong HS [43] 2017 2013-2015 61 Malaysia China (39), India (3), Other (19)
Destination of transplant tourist in mixed period
Author Year of publication Year of transplantation Number of Patients Resident Country of transplant
Ackoundou-N’Guessan [14] 2010 1995–2009 16 Ivory Coast India (5), Tunisia (5), NW (6)
Alkhunaizi [14] 2005 1998-2003 80 Saudi Arabia Pakistan (1), Iran (1), Philippines (1), NW (77)
Ambagtsheer [14] 2013 1994–2005 45 The Netherlands Indian, China, India, Iran, Iraq, Pakistan, USA, Colombia
Sugo [14] 2002 1985–2001 14 Japan NW
Jung [14] 2015 2009–2013 33 Mongolia South Korea
Khalaf [14] 2004 1993–2004 67 Egypt Europe (49), USA (12), Japan (6)
Krishnan [14] 2010 1996–2006 40 UK Pakistan
Kucuk [14] 2005 1978–2001 220 Turkey India, Iraq, Iran
Majid [14] 2010 1993–2009 45 Dubai Philippines (15), Pakistan (7), India (7), Iran (2), Syria (1), Jordan (1), Egypt (1), Germany (2), UK (2), France (1), Singapore (1), USA (1), Israel (1), NW (4)
Ng [14] 2009 1989–2007 4 Singapore China
Rizvi [14] 2009 1993–2007 126 Pakistan Pakistan
Tsai [14] 2011 1987–2006 215 Taiwan China
Wahab [14] 2014 2004–2012 12 Egypt China
Go [14] 2004 1993-2003 53 Malaysia NW
Studies report number of patients without reporting year of transplantation
Author Year of publication Year of transplantation Number of Patients Resident Country of transplant
Abdeldayem [14] 2008 NW 15 Egypt China (15)
Cader [44] 2013 NW 39 Malaysia China
Chen [14] 2010 NW 19 Taiwan China
Coker [13] 1994 NW 21 Turkey India (11), Russia (3), Germany (2) United States (2), England (1), Belgium (1), Greece (1)
Dodo[14] 2000 NW 8 Japan USA (7), Germany (1)
Erikoglu [14] 2004 NW 6 Turkey Iraq (5) and India (1)
Greenberg [14] 2013 NW 10 Israel Egypt
Guy [14] 2013 NW 1 USA Guyana
Huang [14] 2011 NW 15 Taiwan China
Inston [14] 2005 NW 6 UK India
Ivanovski [14] 2005 NW 16 Macedonia (81.3%), Kosovo (18.8%) India (16)
Lu [14] 2014 NW 19 Taiwan NW
Muraleedharan [14] 2006 NW 20 India India
Scheper-Hughes [14] 2011 NW 1 Israel South Africa
Solak [14] 2010 NW 1 Turkey Egypt
Spasovski [14] 2008 NW 1 Macedonia Pakistan
Sugiyama [14] 2009 NW 1 Japan NW
Tsai [14] 2014 NW 185 Taiwan China
Wright [14] 2013 NW 3 Canada Asia
Yakupoglu [14] 2010 NW 5 Turkey Egypt

NW: Not Written

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mpr-7-1-27-g2
Figure 2. Diagram of the study and law database search
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Most of the included studies were also included in another two systematic reviews [13, 14]. The number of patients engaged in TT and their destination was reported in Table 2. In terms of the country of origin and number of recipients, the highest was Taiwan with 3,567 cases, followed by Korea and Malaysia with 2,849 and 1,886 cases, respectively. It must be noted that TT occurred mainly in the black market; therefore, the definitive number remains unknown. Therefore, we identified three major periods of the progression of TT with the corresponding laws or policies of international organizations and nations during three intervals of time: before 2000, from 2000 to 2010, and from 2010 until now.

Table 2. Country of origin and number of recipients
Country of origin Number of recipients
Taiwan 3,567
Korea 2,849
Malaysia 1,886
Turkey 557
Nepal 452
United States 452
Saudi Arabia 337
Singapore 328
UK 291
Canada 244
Qatar 158
United Arab Emirates, Oman 130
Nigeria 126
Egypt 94
Audi Arabi 86
Saudi and Egyptian 74
Kuwait 53
Israel 47
Dubai 45
The Netherlands 45
Syria 38
Bailkan 36
Mongolia 33
Japan 25
Kosovo, the Netherlands, and Sweden 22
Tunisia 20
Scotland 18
Macedonia 17
Ivory Coast 16
Australia 13
Hongkong 12
Sweden 3
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3.1. Progress of TT and related legislation/policies

The progress of TT is virtually parallel to the progress of organ transplantation. With the advancement in transplant techniques and the development of new effective anti-rejection medications approved by Food and Drug Administration (FDA) in 1983, the number of organ transplants has dramatically increased [15]. However, due to the economic, moral, and religious issues, the need for better immunological matching, the lack of organ donors, and other legal restrictions, organ transplantation has been restricted. These factors triggered commercial transplantation and organ trafficking in unregulated countries.

Before 2000, there were a total of 1,977 overseas transplant cases reported (Figure 3A). India was the most popular destination of TT with 1,308 cases, followed by China with 528 cases, Egypt with 14 cases, Pakistan with 5 cases, and others. The only legal document against TT at that time was the resolution of WHA44.25, which was proposed by the WHO in 1991 to call for protection of the minors and other vulnerable persons from the coercion and improper exploitation to donate organs.

mpr-7-1-27-g3
Figure 3. Destination of TT before 2000 (A), during 2000-2010 (B), and after 2010 (C)
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From the year 2000 to 2010, the total number of transplant tourists was nearly five times higher than the previous period with 9,795 cases worldwide. The numbers of transplant tourists visiting China was 7,591 cases; it increased exponentially at 14 times higher in comparison to the previous period (Figure 3B). China became the most popular destination country for TT during this timeframe; India, Pakistan, and Egypt were still among the top popular sites with 667,327 and 123 cases, respectively. Philippines joined with 133 cases reported. In this decade, more legislation was announced and resolutions established by WHO, Council of European, WMA, in addition to the Istanbul declaration against TT.

From the year 2010 to 2016, the number of published papers about TT complications decreased significantly, which may denote the success in the international fight against TT. The total number of reported TT cases was 592 with China still being the most popular destination (Figure 3C). During this interval, a surge of legislation against TT, especially organ harvesting leading to death in China, emerged from the United States, the Council of Europe, and Medical Association.

Subsequently, many countries implemented laws or health policies against TT from 2006 thereafter. People participating in TT were fined or even imprisoned. Enforced consequences demonstrated more awareness in the prevention of the activity globally.

3.2. Exploitation of susceptible populations

Since its establishment, a first scientific report about the harmful consequences of TT for both donors and organ recipients was published in 1990 [16]. The recipients received organ transplants through organ-brokers, and then consequently suffered from severe postoperative complications, including serious infections, leading to a high rate of mortality (18.5% at one year) [16].

Despite the expensive prices for the organs offered for sale on the internet, as described by Shimazono in 2007 such as: 75,000 USD for a kidney; 120,000 USD for a liver; 110,000 USD for a pancreas; and 150,000 USD for a lung transplant [2], the studies in India and Pakistan showed that the vendors were merely only paid a small portion. In fact, the vendors were are defined as commercial living donors whose motivation is monetary gain the destitute with a high rate of illiteracy [17]. They sold their organs to pay off debts and for other essential needs of life such as food and clothing [18]. However, there was no improvement in their economic status; their average income even declined a third after selling their organs. Moreover, their health deteriorated for the remainder of their lives [18, 19]. The similar condition has been reported in Iran, Egypt, and the Philippines. Furthermore, accompanied by physical and economical downgrade, the vendors or commercial living donors also suffered from psychological burden such as being ashamed and isolated from the society [20]. The four trafficking networks in India, South Africa, Kosovo, and the USA were discovered by authorities proved that what we know about the TT based on scientific data may be just a tip of the iceberg [8].

3.3. The story of organs source in China

As China is one of the main countries practicing OT/TT since the year 2000, we are discussing separately the story of organ source in China. According to data from the Ministry of Health of China, before 2000, the annual number of kidney transplants were only about 4,000 in total, and limited report about liver transplant cases was found [21]. However, during the period from 2000 to 2007, the figure for kidney transplants exceeded 6,000 cases per year, and it even peaked to 12,000 cases annually in 2005. Concurrently, there was an exponential growth in the number of liver transplants, which increased from under 100 cases in 2000, to 2,300 cases in 2004, and finally reached its peak at 3,500 cases per year in 2005 [22]. Jiefu Huang, the former Vice Minister of Health of the People’s Republic of China stated that about 90% of organ sources were from deceased donors and most of them came from executed prisoners, and another small portion came from traffic accident victims [23]. However, there has been no transparent data of executed prisoners published by the Chinese government. According to tabulations constructed by Amnesty International report from the publicly-available data, the number of annual executed prisoners were considerably less than the number of annual organ transplant in China, specifically the estimated sentenced death in 2005 was only about 3900 people while the total number of kidney transplant reached to 12,000 cases as described above [24]. A report revealed that the Chinese government performed forced removal of organs leading to death not only from executed prisoners but also from prisoner of conscience who were mainly Falun Gong (a Chinese spiritual practice) practitioners [25-27]. The actual number of cases is difficult to get due to lack of accessible data and could be greatly underestimated. It is difficult to know the actual fact due to lacking of transparent data from China and the action of prohibiting independent investigator of Chinese government.

This unethical practice was stated by Council of Europe [9]. Concerns about ethical standards implemented in research publications using materials from executed prisoners, a recent review investigating on Chinese organ transplantation concluded that around 92.5% (412/445 included studies) failed to clarify whether or not, the organs were sourced from executed prisoners and 99% (439/445 included studies) failed to report that organ sources gave consent for transplantation [28]. Scholars in genocide study presented that forced organ harvesting from Falun Gong practitioner in China is one part of Chinese Government’s effort to eradicate of this group [29].

3.4. Legislation effectiveness against TT act

International efforts to fight against TT has been continuously evolving. The effectiveness of legislation imposed by some countries of origin including Europe, Malaysia, Israel, Turkey, United States, Australia, Spain, Taiwan was reported in details in Table 3. Before 2000, there were extremely limited organizations or nations that paid attention to TT; Turkey played a pioneer in ordering legislation with the law on organ transplantation in 1979 [30]. This law was used as a model by many other countries in the following time. In 1991, WHO proposed resolution calling for protecting the vulnerable from TT. After the 2000, TT expanded very rapidly resulting in some severe unethical issues; criminal organ trafficking network and forced organ-harvesting leading to death in China. Many international organizations and nations have raised their voices against TT. The most significant evolution in the fight against TT was the declaration of Istanbul in 2008, which officially condemned organ commercialism and TT. Moving forward, with the efforts of human rights activists and medical specialist association, law against TT has been implemented in numerous countries of origin (Table 3), and law regulating organ transplantation has also been implemented in countries of destination.

Table 3. Development Progression of legislation/policies against TT before 2000, during 2000-2010, and after 2010
Year Organization/Nation Document Impact on OT/TT
Legislation against TT before 2000
1979 Turkey Law no 2238 on the Harvesting, Storage, Grafting, and Transplantation of Organs and Tissues [28] Forbidding buying and selling and all advertisement in connection with the harvesting and donation of organs and tissues and require penalty.
1991 WHO WHA44.25 Resolution [45] Protection to minors and other vulnerable persons from coercion and improper exploitation to donate organs
Legislation against TT during 2000-2010
2004 WHO WHA57.18 Resolution [46] Measures to protect the poorest and most vulnerable groups from “TT”
2005 Council of Europe CETS No. 197 [47] Action against trafficking of human organs
2006 World Medical Association Resolution [48] Demand China to stop using prisoners as organ donors
2008
2018
Transplantation Society and the International Society of Nephrology Istanbul declaration [49] Define TT
Call to bring TT to an end
Legislation of leading nations/organizations against TT and organ harvesting in China during 2010 - 2016
February 2014 United States Resolution HR0730 of the State of Illinois [50] Condemning Forced Organ Harvesting, urge the government to bring an end to the revolting practice of harvesting organs from living Falun Gong practitioners for transplants
October 2014 Resolution No.1052 of Pennsylvania State [51] Calling upon the People’s Republic of China to immediately end the practice of forced organ harvesting
2015 Council of Europe Treaty series – No.216 [49] Action against trafficking of human organs
2016 European Parliament Rule 136 of Parliament’s Rules of Procedure [49] End organ harvesting from prisoners of conscience in China
2016 World Medical Association Repeated Resolution [48] Demand China to stop using prisoners as organ donors
2016 United States Resolution 343 of US House of Representatives[52] Expressing concern regarding organ harvesting in the People’s Republic of China
Legislation/policies against TT/organ harvesting in China by other nations from 2006 - now
2006 Australia Australian Health Ministry [53] Abolition of training programs for Chinese doctors in organ transplant technique Banning joint research programs with China on organ transplant.
2008 Israel Israel Organ Transplant Act [11] Prohibit reimbursement. Three years’ imprisonment and a large fine for the purchase, sale, or brokerage of an organ
2009 Spain The New Criminal Code [11] Consider the illegal trafficking of human organs as a felony
2010 The New Criminal Code, Article 156 bis [11] Impose penalties for participants of organ trafficking with imprisonment from six to twelve years
2012 Malaysia Ministry of Health [31] Prohibit reimbursement to TT patients
2015 Taiwan The Human Organ Transplantation Act [11] Fine and imprisonment of 1 to 5 years for involvement in brokering organs or organ tourism Doctors who engage in organ brokerage will have their licenses revoked
2015 Italy Senate Bill [11] 3 to 12 years’ imprisonment and a fine between 50,000 and 300,000 euros Doctors who promote or facilitate illegal organ tourism would face lifetime disqualification
2016 Law No. 2937 [11] Ban organ trafficking in November 2016
2017 Norway The Norwegian law of June 16th 2017 nr. 54[10] Prevent and combat trade with human organs Increased penalties for breach of the provisions in legislation
2019 Belgium Amendment to the Belgian Penal Code [46] Imprison up to 10 years and a fine of up to 75,000 EUR for anyone who forcedly takes an organ from a person

WHO = World Health Organization, TT = transplant tourism, OT = Oversea Transplantation, WMA: World Medical Association

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Law implementation and related policies against TT has been effective in many countries of origin to reduce the number of transplant tourists travelling abroad to countries where laws prohibiting organ sales are poorly enforced or overrode by loopholes. Council of Europe was the leading league of countries that actively fought against TT. From the Convention on Human Rights and Biomedicine in 1997, an additional protocol concerning Transplantation of Organ and Tissues of Human Origin, to the passing law prohibited organ trafficking in 2016 and 2017. The number of patients going abroad for transplant within this region has dropped down significantly [9]. The same trend occurred in Israel and Malaysia. After implementing law in 2008, the number of patients going abroad for kidney transplant decreased from 155 in 2006 to 35 in 2011 [31]. Amongst the top three countries of tourist’s origin, Taiwan implemented a law against TT in 2015, yet there is no report on its effectiveness till now [32]. Malaysia implemented a policy that refuses to dispense immunosuppressive therapy for free to TT patient without the approval of the Ministry of Health from January 2012, resulting in at least one third reduction of the number of patients engaging in TT annually [33].

On the other hand, some top countries of destination where transplantation takes place, according to a subsequent report from the Council of Europe, transplant legislation was adopted. In October 2014, Hangzhou Resolution was promulgated which terminate the usage of organ from executed prisoners [34]. However, recent reports have provided that thousands of patients from South Korea, Gulf Region and Western Chinese community still going to China for organ transplant [35]. Regular visit transplant center of members of the Declaration of Istanbul Custodian travel to China suspected that TT is still active and on-going [9]. The same story has been reported in India, although this country building law in 2008, but TT is still ongoing with poor regulation [9]. After implementing the laws, Philippines had a success in controlling the foreigner transplant tourist but was unable to deal with local one [36]. There was no report on other countries of destination in medical literature.

There are several limitations in our narrative review. Since there was no universal obligation to report cases of TT, the reported numbers might underestimate the magnitude of the problem. Moreover, even after China announced that starting 2015, hospital-based donors would be the sole source of organs in response to international criticism, the reported numbers following this announcement appeared to be falsified according to a recent study [37]. In addition, being a narrative review with unstructured search terms, some studies might have been missed from our search.

CONCLUSIONS

Our review has characterized an overview on the progression of TT under the effectiveness of related policies and legal issues as well as clearly describe the unethical consequences that violate the ethical principles of medicine: “first do no harm”. It is clear that TT leading two unethical consequences: taking advantage from the destitute causing them to become physically, and mentally deficit and socioeconomic downgrade in some developing countries and forced organ removing leading to death in China.

During the early progression of TT, India was the most popular destination for commercial transplants before 2000, meanwhile China was the most popular destination country, followed by Pakistan and India, after 2000 until now. Legislative ethics on TT has been recently garnered more attention and has recently taken into considerations. It is proved that law implementation in countries of origin have positive effects on reducing TT; however, in countries of destination, law has played a limited role on abroad TT. Organ donation is an altruistic value; however, organ shortages led to TT, which has culminated in organ trading, organ harvesting, and taking advantage of the defenseless. We suggest an international cooperation in bringing TT to a termination.

LIST OF ABBREVIATIONS

TT:

Transplant tourism;

FDA:

Food and Drug Administration;

GDOT:

Global Observatory on Donation and Transplantation;

WMA:

World Medical Association;

OT:

Oversea Transplantation.

FUNDING

The authors received no financial support for the research, authorship, and/or publication of this article.

CONFLICT OF INTEREST

The authors declare that there is no conflict of interest.

AUTHORS’ CONTRIBUTION

LCC, NDT: concept/design, data analysis/interpretation. LT: drafting article, critical revision of article. LTPL: approval of article. GJM, MEE, NHN: data collection. NTH: approval of article, funding. All authors read and approved the final manuscript.

REFERENCES

1.

Organ Donation and Transplantation Activities. 2015 report [Internet]. 2017.

2.

Shimazono Y. The state of the international organ trade: a provisional picture based on integration of available information. Bulletin of the World Health Organization. 2007; 85((12)):955-62

3.

Jha V. Towards achieving national self-sufficiency in organ donation in India – A call to action. Indian Journal of Nephrology. 2014; 24((5)):271-5

4.

World Health Organization. Human organ and tissue transplantation. 2003.

5.

Budiani-Saberi DA, Delmonico FL. Organ trafficking and transplant tourism: a commentary on the global realities. 2008 (1600-6143 (Electronic))

7.

Shimazono Y. Mapping “Transplant Tourism.”. Presentation at the World Health Organization’s Second Global Consultation on Human Transplantation. Geneva. March; p. 28-30 2007.

8.

Study Trafficking in Human Organs [Internet]. 2015.

9.

Parliamentary Assembly CoE. Organ Transplant Tourism. 2018.

10.

Stop Organ Harvesting in China [Internet]. .

11.

China Organ Harvest Research Center [Internet]. 2018.

12.

International Coaliation to End Transplant Abuse in China [Internet]. .

13.

Anker AE, Feeley TH. Estimating the risks of acquiring a kidney abroad: a meta-analysis of complications following participation in transplant tourism. Clinical Transplantation. 2012; 26((3)):E232-E41

14.

Ambagtsheer F, de Jong J, Bramer WM, Weimar W. On Patients Who Purchase Organ Transplants Abroad. American Journal of Transplantation. 2016; 16((10)):2800-15 https://doi.org/

15.

Linden PK. History of solid organ transplantation and organ donation. 2009 (1557-8232 (Electronic)).

16.

Salahudeen AK, Woods HF, Pingle A, Nur-El-Huda Suleyman M, Shakuntala K, Nandakumar M, et al. High mortality among recipients of bought living-unrelated donor kidneys. The Lancet. 1990; 336((8717)):725-8

17.

Budiani-Saberi DA, Delmonico FL. Organ trafficking and transplant tourism: a commentary on the global realities. Am J Transplant. 2008; 8((5)):925-9

18.

Goyal M, Mehta RL, Schneiderman LJ, Sehgal AR. Economic and health consequences of selling a kidney in india. JAMA. 2002; 288((13)):1589-93

19.

Naqvi Syed Ali A, Ali B, Mazhar F, Zafar Mirza N, Rizvi Syed Adibul H. A socioeconomic survey of kidney vendors in Pakistan. Transplant International. 2007; 20((11)):934-9

20.

Budiani-Saberi D, Mostafa A. Care for commercial living donors: the experience of an NGO’s outreach in Egypt. Transplant international : official journal of the European Society for Organ Transplantation. 2011; 24((4)):317-23

21.

Hindi Z, Congly S, Tang E, Skaro A, Brahmania M. Liver Transplant Tourism. Liver transplantation : official publication of the American Association for the Study of Liver Diseases and the International Liver Transplantation Society. 2020; 26((2)):276-82

22.

Jiefu Huang YM, J Michael Millis. Government policy and organ transplantation in China. 2008

23.

Huang J. Ethical and legislative perspectives on liver transplantation in the People’s Republic of China. Liver Transplantation. 2007; 13((2)):193-6

24.

Amnesty International Report 2006 - China [Internet]. 2006.

25.

David Matas DK. Bloody Harvest: Revised Report into Allegations of Organ Harvesting of Falun Gong Practitioners in China. 2007.

26.

Trey T, Caplan AL, Lavee J. Transplant ethics under scrutiny - responsibilities of all medical professionals. Croatian medical journal. 2013; 54((1)):71-4

27.

Tibell A. The Transplantation Society’s policy on interactions with China. Transplantation. 2007; 84((3)):292-4

28.

Rogers W, Robertson MP, Ballantyne A, Blakely B, Catsanos R, Clay-Williams R, et al. Compliance with ethical standards in the reporting of donor sources and ethics review in peer-reviewed publications involving organ transplantation in China: a scoping review. BMJ Open. 2019; 9((2))e024473

29.

Cheung MT. Torsten; Matas, David; and An, Richard Cold Genocide: Falun Gong in China. Genocide Studies and Prevention: An International Journal. 2018; 12((1)):38

30.

Turkish Laws no 2238 on the Harvesting, Storage, Grafting, and Transplantation of Organs and Tissues [Internet]. 1979.

31.

Padilla B, Danovitch Gm Fau - Lavee J, Lavee J. Impact of legal measures prevent transplant tourism: the interrelated experience of The Philippines and Israel. 2013 (1572-8633)

32.

Tsai DF-C, Huang S-W, Holm S, Lin Y-P, Chang Y-K, Hsu C-C. The outcomes and controversies of transplant tourism—Lessons of an 11-year retrospective cohort study from Taiwan. Plos One. 2017; 12((6))e0178569

33.

Malaysia committed to eradicate human organ trafficking [Internet]. 2011.

34.

Huang J-F, Zheng S-S, Liu Y-F, Wang H-B, Chapman J, O’Connell P, et al. China organ donation and transplantation update: the Hangzhou Resolution. Hepatobiliary & Pancreatic Diseases International. 2014; 13((2)):122-4 https://doi.org/

35.

The dark side of transplant tourism in China: killing to live” — Documentary on China’s transplant tourism [Internet]. 2017.

36.

de Castro LD. The declaration of Istanbul in the Philippines: success with foreigners but a continuing challenge for local transplant tourism. Springer Netherland. 2013; 16:1572-8633 https://doi.org/

37.

Wise J. China’s organ donation figures appear to be falsified, study claims. BMJ. 2019; 367:l6550