Outcome of overseas commercial kidney transplantation: an Australian perspective

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This article discusses the outcome of overseas commercial kidney transplantation from an Australian perspective. It highlights the risks associated with commercial transplantation and the importance of increasing the availability of donor kidneys. Patients who received commercial transplants were more likely to develop infections such as HIV, hepatitis B virus, cytomegalovirus and fungal infections. Patient and graft survival were worse than transplantation within Australia. Patients considering the option of overseas commercial donation should be advised that heightened risks to life and graft survival exist.

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224 MJA Volume 182 Number 5 7 March 2005
H E A LT H C A R E
The Medical Journal of Australia ISSN: 0025-
729X 7 March 2005 182 5 224-227
©The Medical Journal of Australia 2005
www.mja.com.au
Healthcare
idney transplantation is accepted as a better treatment for
patients with endstage kidney disease (ESKD) than long-
term dialysis. Mortality, morbidity and cost comparisons
are significantly better than dialysis regimens.1-3 The major factor
limiting transplantation rates is availability of donor kidneys.
About 520 kidney transplantsare performedeach year in
Australia,4 and this number has remained relatively stable over
recent years, despite a steady increase in the number of patients
receiving dialysis treatment. There are about 2000 Australians
awaiting kidney transplantation.
The deceased donor (DD) rate has diminished over the past 10
years, but there has been a corresponding increase in living
donor (LD) transplants. In Australia, these now contribute 35%–
40% of kidney transplants. LD kidneys have traditionally been
from related donors (usually parents or siblings), but there has
been a recent rise in the number of living unrelated donors
(LURD).4 LURD kidneys are from spouses (69%), with other
emotionally related” donors making up most of the remainder. A
small number of kidneys are transplanted from donors who have
no direct genetic or emotional relationship with the recipient,
and increasing the frequency of this type of donation is seen as a
potential way of reducing the waiting list for transplantation.
Most Australian states have enacted laws that forbid payment for
organs and tissues for transplantation. Protocols enabling altruis-
tic donor procedures are currently under consideration by health
authorities.
The lack of transplantable organs is a universal problem in
developed countries, and has led to the growth of commercial
programs or renal transplantation in which donors are financially
compensated. The main centres for these practices were initially
in India; although the practices are now illegal in India, an
estimated 60% of kidney donations are still paid donations.5
More recently, programs have developed in Iraq, Iran, Eastern
Europe, South America, South Africa and the Philippines.6 Large
commercial transplantation programs have also been established
in China, attracting recipients from around the world. The source
of these commercially acquired kidneys is not always apparent;
some reports claim that up to 90% of transplanted kidne
China are retrieved from executed prisoners.7 South Korea is
notable for having developed an organ donation registry sup
ing both altruistic LURD and “paired-exchange” donation8 A
paired exchange occurs when two patients have incomp
potential donors and kidneys are exchanged. Paired excha
are presently illegal in Australia.
A small percentage of Australian patients with ESKD h
availed themselves of overseas commercial kidney transp
tion. We reviewed the literature about outcome of overs
commercial kidney transplantation and report the experience
four Australian centres.
Literature review
We reviewed the literature using the MEDLINE database 1966
June 2003. Primary search terms were “kidney transplantatio
and “commerce”, followed by a second search using “ki
transplantation” and “living donors” and “unrelated”. The ph
commercial transplantation” was used as a separate ke
The abstracts of retrieved articles were reviewed, and those
focused on outcome of commercialtransplantationwere
obtained in full, and their reference lists were searched
further articles. Four articles, each reviewing the outcom
more than 100 cases of commercial transplantation (1301 ca
in total), were published between 1990 and 2001 (Box 1). Th
are discussed below.
Outcome of overseas commercial kidney transplantation:
an Australian perspective
Sean E Kennedy, Yvonne Shen, John A Charlesworth, James D Mackie, John D Mahony, John J P Kelly and Bruce A Pussell
ABSTRACT
Lack of donors has led to a worldwide increase in commercial
kidney transplantation programs where recipients acquire
kidneys either from executed prisoners or live non-related
donors.
Commercial transplantation is prohibited by legislation in
Australia.
Our centres have had 16 patients who have travelled overseas
to receive a commercial kidney transplant; five have
subsequently died.
As has been found previously, patients who received
commercial transplants were more likely to develop infections
such as HIV, hepatitis B virus, cytomegalovirus and fungal
infections.
Previous reports have found that patient and graft survival
were comparable to local results, whereas we found that
patient and graft survival were worse than transplantation
within Australia.
Patients considering the option of overseas commercial
donation should be advised that heightened risks to life and
MJA 2005; 182: 224–227
graft survival exist.
FOR EDITORIAL COMMENT, SEE PAGE 204
East Coast Renal Services, Prince of Wales Hospital, Royal North
Shore Hospital, St George Hospital, Sydney, NSW, and Illawarra
Regional Hospital, Wollongong, NSW.
Sean E Kennedy, FRACP, Renal Registrar, Prince of Wales Hospital;
Yvonne Shen, FRACP, Renal Registrar, Prince of Wales Hospital;
John A Charlesworth, MD, FRACP, Professor of Renal Medicine,
Prince of Wales Hospital; James D Mackie, FRACP, Renal Physician,
Prince of Wales Hospital and Illawarra Regional Hospital;
John D Mahony, FRACP, Renal Physician, Royal North Shore Hospital;
John J P Kelly, MD, FRACP, Renal Physician, St George Hospital;
Bruce A Pussell, PhD, FRACP, Professor of Medicine,
Prince of Wales Hospital.
Reprints will not be available from the authors.
Correspondence: Professor Bruce A Pussell, Department of Nephrology,
Prince of Wales Hospital, Sydney NSW 2031. b.pussell@unsw.edu.au
K

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MJA Volume 182 Number 5 7 March 2005 225
H E A LT H C A R E
Renal outcomes
Salahudeen et al reported the outcome of 131 transplants in
patients from the United Arab Emirates and Oman who received
commercial transplants in India.9 All patients had arranged their
own transplants in Bombay through brokers and without reference
to their treating nephrologists. Eight patients died during the
perioperative period, a further eight within the first 3 months and
another eight before 12 months (patient survival rate, 81.5% at 1
year). Infections were the major cause of death (56%). One patient
developed AIDS and died within 3 months of transplantation; HIV
infection in the recipient had been suspected pre-transplantation.
A further four patients became HIV-positive. Other fatal infec
included pneumonia, septicaemia, tuberculosis, viral hepatiti
fungaemia. Most patients returned from India without ad
documentation (50 had no record or knowledge of their antir
tion regimen) and many were sick or undergoing rejecti
arrival home.
The pooled experience of several Saudi Arabian centre
reported in 1997.10 The outcomes of 540 patients who had
received commercial transplants in India between 1978 and
were compared with patients transplanted at their own
with LD kidneys. After adjusting for several variables, the 1-y
2 Pretransplant and transplant details and outcomes for the 16 patients seen in our Australian centres
Patient
No. Age Sex Primary disease
Time on
dialysis
Previous
transplant
Year and country
of transplant
Rejection
episodes Graft survival Outcome
1 53 M Glomerulonephritis 2 years No 1990, India 0 13 years Well with good function
2 75 M Interstitial nephritis 5 months No 1993, China 1 12 months
(death with
functioning
graft)
CMV disease at 3 months;
HBV hepatitis at 9 months;
death at 12 months with
fulminant hepatitis
3 43 M Diabetic nephropathy12 months No 1994, India 1 12 months
(renal infarction)
Death after 13 months;
ischaemic infarct
4 54 M Hypertension 12 months No 1994, India 1 1 month
(acute rejection)
Death after 4.5 years;
sepsis
5 56 M Glomerulonephritis 4 years No 1998, Iraq 0 4 years Well with good function
6 31 M Glomerulonephritis 2 years No 1999, China 0 5 years Well with good function
7 65 M Diabetic nephropathy 2 years No 1999, Philippines 0 5 years Well with good function
8 66 F Glomerulonephritis 2 years Yes 2000, ? Eastern
Europe
0 3 years Systemic CMV infection
on return
9 52 M Glomerulonephritis 12 months No 2000, China 1 3 years Well with good function
10 55 F Glomerulonephritis 10 months No 2002, China 0 2 years Well with good function
11 43 M Glomerulonephritis 12 months No 2002, China 0 2 years Disseminated herpes zoster
12 49 F Reflux nephropathy 0 No 2002, Lebanon Multiple 1 month
(aspergillosis)
Aspergillosis; septicaemia;
dialysis required
13 41 M Glomerulonephritis 10 months No 2004, China 0 4 months CMV pneumonitis
14 54 M Glomerulonephritis 6 weeks No Nil,* Lebanon na na Dialysis
15 70 M Diabetic nephropathy 5 years No Nil,* China na na Death
16 52 M Glomerulonephritis 3 years No Nil,* India na na HBV; death
HBV = hepatitis B virus; CMV = cytomegalovirus; na = not applicable.
* Travelled overseas for transplant but not transplanted. † Ongoing graft function. ‡ Acquired hepatitis (positive for HBV e antigen) while on dialysis awaiting tra
1 Summary of commercial transplantation case reports
First author
Country of origin
of patients
Country of
transplant Years No.
Patient survival
at 1 year
New
HIV infection
New
HBV infection
Salahudeen9 UAE and Oman India 1984–1988 131 81.5% 3.8% 2.3%
Living Non-
Related Renal
Transplant Study
Group10
Saudi Arabia India 1978–1993 540 96% 4.6% 8.1%
Sever11 Turkey India, Iraq, Iran 1992–1999 115 90% (2 years) nr 6%
Morad12 Malaysia nr 1990–1996 515 92% nr 12%
Onwubalili13 Saudi Arabia India 1985–1991 16 nr 6.25% 6.25%
Ivanovski14 Macedonia India 1993–1997 14 78% nr nr
UAE = United Arab Emirates; HIV = human immunodeficiency virus; HBV = hepatitis B virus;nr= not reported
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226 MJA Volume 182 Number 5 7 March 2005
H E A LT H C A R E
3-year, and 5-year patient survival rates in the Indian group were
similar to those of the locally transplanted group (95%, 91%, 91%
and 97%, 94%, 92%, respectively; P = 0.4921), as were the graft
survival rates. There was a higher incidence of HIV infection (4.6%
v 0), and hepatitis B virus infection (8.1% v 1.4%) in the cohort
transplanted in India.
Sever et al reported the experience of 115 Turkish patients who
were transplanted in India (106 patients), Iraq (7) and Iran (2)
between 1992 and 1999.11 There was a high incidence of early
surgical complications, as well as three cases of primary non-
functioninggrafts.The non-surgicalinfectiouscomplications
included 10 patients who developed malaria, 8 who developed
serious fungal infection (5 fatal) and six cases of atypical pneumo-
nia. Six patients became positive for hepatitis B. The patient
survival rates at 2 years (90%), 5 years (80%) and 7 years (74%)
were not significantly different from LD transplants performed in
Istanbul (90%, 85% and 80%, repectively; P = 0.53). Graft survival
rates for commercial transplants were 84%, 66% and 53% v 86%,
78% and 73% for Turkish LD transplants (P = 0.036) at these
endpoints.
A comparison of 515 Malaysian patients who had received
overseas commercial kidneys with 258 patients who had received
LD kidneys in Malaysia showed that patient and graft survival, as
well as infectious complications, were comparable between all
groups.12 The analysis did not include all patients who went
overseas for commercial transplants — only those who returned.
Other, smaller reviews have also been published, with similar
high rates of infectious complications(see Box 1).13,14
Local experience
We surveyed four renal units in the East Coast Renal Services of
New South Wales and identified 16 patients who had travelled
overseas for commercial kidney transplantation. Patient details and
outcomes are shown in Box 2. Three patients who travelled
overseas did not receive a kidney graft, but received haemodialysis
therapy while abroad. Two have subsequently died. Patient 15
travelled to China twice for transplantation. During his first visit
urological surgery was performed in preparation for transplanta-
tion, but on his return visit he was considered too unwell for
further surgery and has subsequently died. Patient 16 contracted
hepatitis B virus while undergoing dialysis in India and died of
liver failure.
Patient survival
Overall 1-year patient survival in this small series was 85%, with
long-term outcomes possibly worse. Seven of the patients were
transplanted more than 5 years ago. Three of these have since died,
all within 5 years. Two deaths followed graft failure and one was
the result of HBV infection. All eight patients transplanted in the
past 5 years have survived, but with an increased incidence of
infectious complications.
Graft survival
Four grafts failed within 12 months, giving a 1-year graft survival
rate of 66% compared with the Australian survival rate of 90% at
one year. Kidneys that survived beyond 12 months generally
continued to function well.
Acute rejection
Early acute rejection or delayed graft function was document
four cases. In one instance this was the result of the patient b
given an inadequate supply of medications before returning h
Infectious complications
Patients 2 and 16 contracted HBV in China and India, which le
death. Three patients were admitted to hospital soon af
return to Sydney with serious cytomegalovirus infections. Pa
12 returned from Lebanon with aspergillus infection of the kid
graft and required nephrectomy. Her surgical wounds we
infected by multiresistant Pseudomonas aeruginosa. Ther
been no instances of HIV seroconversion in this group of pati
Documentation and correspondence
Documentation of transplantation procedure, patient progres
medication doses was variable. In at least three instanc
documentation was available. All correspondence from China
in Chinese. Donor details were generally not available, althou
was known that at least two kidneys were from executed Chi
prisoners.
Discussion
Kidney transplantation has significant survival advantages
dialysis therapy,1 and the quality of life of kidney transplan
recipientsis significantlybetterthan that of similarpatients
maintained on dialysis.15 It is therefore not surprising that some
dialysis patients are prepared to seek alternatives to the unc
waiting period associated with a DD transplant. Similarly, pat
who, for reasons of comorbid disease or advanced age,
offered the option of DD transplantation may seek trans
donors from other sources.
Our case series highlights some areas of concern about ove
commercial kidney transplantation. As illustrated in previ
published series, the early postoperative mortality rate was h
The 1-year patient survival rate of overseas commercial tran
may be between 80% and 96%, compared with greater than
for Australian LD transplants.4 Although the early survival rate was
good in our relatively small series, two patients died 1 year a
transplant and the 5-year patient survival rate was 60%. This
marked survival disadvantage compared with the Australian
kidney transplantrecipients’5-yearsurvivalrate of 82% or
greater.4 Survival rates for Australian dialysis patients place
the transplant waiting list in Australia at 1 year (from t
joining the list) are also above 95%.1 The 3-year survival rate for all
dialysis patients in Australia is greater than 60%.
Our series covers a period of 14 years. The three patients w
died were transplanted in the early 1990s. More recent overs
transplants appear to have better outcomes, but even in this
group there has been a high incidence of serious infection. It
important to note that we (as in previously published se
reported only the outcomes of patients who have returned fr
overseas, which means early mortality and complications ma
under-reported.
Infectious complications were notable. Cytomegalovirus inf
tion is a common occurrence in the first 6 months after trans
and, to reduce the risk of CMV disease, most Australian centr
have instituted routine use of prophylactic therapy. Details o
screening of overseas donors were scarce. HIV and viral hepa
Document Page
MJA Volume 182 Number 5 7 March 2005 227
H E A LT H C A R E
could both be contracted during the transplant period, either from
an infected donor organ or blood products. Prospective Australian
organ donors and blood donors are screened for CMV, HIV, HBV
and hepatitis C virus. The screening procedures of commercial
transplant programs are not evident, despite a generally high
incidence of these infections in the populations of the countries
performing commercial transplantation.
An area of concern identified in our patients is the lack of
communication between the transplantation team and the unit
caring for the patient in Australia. Our experience is similar to that
reported by others. An obstacle in at least one instance was
reluctance on behalf of the patient to disclose information.
Conclusions
As physicians caring for patients with ESKD, we should be able to
offer informed advice about commercial transplantation. Ethical
reasons, in particular concerning the rights and well-being of donors,
are enough to prevent us from recommending overseas commercial
transplantation (in its current form) as a treatment for ESKD.16
We suggest that patients considering commercial organ donation
should be advised that heightened risks to life and graft survival exist.
If they decide to proceed with commercial transplantation, they
should specifically seek assurances about screening for HIV and viral
hepatitis before departure. They should also be aware that a donor
kidney may not be available and that haemodialysis overseas may
further expose them to blood-borne viruses. All attempts should be
made to ensure adequate documentation and communication.
Competing interests
None identified.
References
1 McDonald SP, Russ GR. Survival of recipients of cadaveric kidney trans-
plants compared with those receiving dialysis treatment in Australia and
New Zealand 1991–2001. Nephrol Dial Transplant 2002; 17: 2212-2219.
2 Winkelmayer WC, Weinstein MC, Mittleman MA, et al. Health economic
evaluations: the special case of end-stage renal disease treatment. Med
Decis Making 2002; 22: 417-430.
3 Wolfe RA, Ashby VB, Milford EL, et al Comparison of mortality in a
patients on dialysis, patients on dialysis awaiting transplantation, an
recipients of a first cadaveric transplant. N Engl J Med 1999; 341: 1725-
1730.
4 Australia and New Zealand Dialysis and Transplant Registry. Available at:
www.anzdata.org.au (accessed April 2004).
5 Phadke KD, Anandh U. Ethics of paid organ donation. Pediatr Nephrol
2002; 17: 309-311.
6 Scheper-Hughes N. Keeping an eye on the global traffic in human
organs. Lancet 2003; 361: 1645-1648.
7 Briggs JD. The use of organs from executed prisoners in China. Nephrol
Dial Transplant 1996; 11: 238-240.
8 Kim ST, Kim JH. Organ donation — third party donation: expanding the
living-donor pool. Transplant Proc 2000; 32: 1489-1491.
9 Salahudeen AK, Woods HF, Pingle A, Nur-El-Huda, et al. High mortality
among recipients of bought living-unrelated donor kidneys. Lancet 1990;
336: 725-728.
10 The Living Non-Related Renal Transplant Study Group. Commercially
motivated renal transplantation: results in 540 patients transplanted in
India. Clin Transplant 1997; 11: 536-544.
11 Sever MS, Kazancioglu R, Yildiz A, et al. Outcome of living unrelate
(commercial) renal transplantation. Kidney Int 2001; 60: 1477-1483.
12 Morad Z, Lim TO. Outcome of overseaskidney transplantationin
Malaysia. Transplant Proc 2000; 32: 1485-1486.
13 Onwubalili JK, Obineche EN, Assuhaimi S, Bassiouni M. Outcome of
bought living non-related donor kidneys followed up at a single centre.
Transplant Int 1994; 7: 27-32.
14 Ivanovski N, Stojkovski L, Cakalaroski K, et al. Renal transplantation from
paid, unrelated donors in India it is not only unethical, it is also
medically unsafe. Nephrol Dial Transplant 1997; 12: 2028-2029.
15 Valderrabano F, Jofre R, Lopez-Gomez JM. Quality of life in end-stage
renal disease patients. Am J Kidney Dis 2001; 38: 443-464.
16 Zargooshi J. Quality of life of Iranian kidney “donors”. J Urol 2001; 166:
1790-1799.
(Received 15 Jan 2004, accepted 30 Sep 2004)
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