| Abstract|| |
Patients with established renal failure, living in developing countries, face many obstacles including lack of access to transplantation centers, quality and safety issues, and exploittation associated with transplant tourism. This review aims to determine the state and outcome of renal transplantation performed in developing countries and to recommend some solutions. The lack of suitable legislation and infrastructure has prevented growth of deceased donor programs; so, living donors have continued to be the major source of transplantable kidneys. Transplant tourism and commercial kidney transplants are associated with a high incidence of surgical complications, acute rejection and invasive infection, which cause major morbidity and mortality. Developing transplant services worldwide has many benefits - improving the results of transplantation as they would be performed legally, increasing the donor pool, making transplant tourism unnecessary and granting various governments the moral courage to fight unacceptable practices. A private-public partnership underpinned by transparency, public audit and accountability is a prerequisite for effective transplant services in the developing world. Finally, lack of dialysis facilities coupled with better outcomes in patients spending <6 months on dialysis prior to transplantation favor pre-emptive transplantation in developing countries.
|How to cite this article:|
Akoh JA. Renal transplantation in developing countries. Saudi J Kidney Dis Transpl 2011;22:637-50
| Introduction|| |
Improving results have made transplantation the favored option for treating patients in established renal failure (ERF). ,, Successful renal transplantation is cost-effective and offers survival and quality of life advantages over dialysis. ,, Establishing a properly functioning renal transplant service is both labor intensive and costly. Concordance between nephrologists, urologists, laboratory scientists, pathologists, immunologists, and transplant surgeons plays a very important role in ensuring a successful renal transplant service. Data on transplantation activity and outcome in many developing countries are not comprehensive, and are, to some extent, tainted by the specter of commercial transplantation. Patients with ERF, living in developing countries, face many obstacles: lack of access to transplantation centers due to limited or no facilities, quality and safety issues, restricted choice of organs from living donors, and exploitation associated with transplant tourism. Economic deprivation in developing countries and the relatively modest expenditure on health care by government contributes to poor transplantation activity, with a rate of 0-10 per million population (pmp) in contrast to the rate in the developed world at around 30-50 pmp. In addition, lack of public awareness, education and motivation for organ donation as well as lack of manpower contribute to an insufficient transplant program. ,,
The aim of this review is to determine the state and outcome of renal transplantation performed in developing countries, the effect of transplant tourism on outcome, key challenges with transplantation in such economies, and to recommend a way forward.
| Need for Renal Transplantation|| |
Etiology of ERF
Conditions including chronic glomerulonephritis, hypertension and diabetes mellitus that are associated with progression to ERF are prevalent in developing countries. ,, Hypertension, a strong independent risk factor for ERF,  affects 20% of the adult population in Africa.  The population-attributable risk for kidney failure is 42% for diabetes mellitus, which has a major effect on the incidence of ERF in young and middle-aged adults and may be responsible for a larger proportion of endstage renal disease than is suggested by the use of clinical diagnoses of underlying renal disease by the nephrologists.  It is estimated that about 30% of the 170 million people with diabetes mellitus worldwide have or will develop diabetic nephropathy. 
Human immunodeficiency virus (HIV)-associated nephropathy has become the third leading cause of ERF in African Americans (AA).  Prior to the introduction of highly effective antiretroviral therapy in the mid-1990s, transplantation centers were reluctant to transplant patients with HIV infection. As treated patients can now expect to live substantially longer than before  and have excellent outcomes following renal transplantation,  the demand for transplantation is likely to rise in countries where HIV is endemic.
High incidence of chronic kidney disease (CKD)
Data on chronic kidney disease (CKD) for many developing countries are either not available or inaccurate, but considering the prevalence of poor socioeconomic factors, the incidence of ERF is likely to be similar to or higher than that in high-income countries.  It is thought that CKD is more prevalent and virulent in Africa than that found in the Western countries.  CKD, which affects the young and productive members of the population, is a major cause of morbidity and mortality in Nigeria,  where the prevalence of ERF is estimated to be 300-400 pmp. 
Unavailability of services
The availability of dialysis and transplantation is variable in Africa, with treatment rates in North Africa between 30 and 186.5 pmp. Services are predominantly urban and therefore generally inaccessible to poorer and less educated rural patients.  In poorer nations, for example in sub-Saharan Africa, economic and manpower factors influence a conservative approach to therapy. The majority of those with ERF die because of lack of funds as few can afford regular maintenance dialysis or renal transplantation (often not available). ,,
Developing national transplant services is the most effective way of curtailing organ trafficking and transplant tourism. A socioeconomic and health survey of 239 kidney vendors from Punjab in eastern Pakistan showed that while 93% vended kidneys for debt repayment, 88% had no economic improvement in their lives after the event and 98% reported deterioration in general health status. 
Arguments against transplantation services
Transplantation is one of the most challenging and complex areas of modern medicine. Issues such as rejection, bioethical issues, and organ procurement lead some to argue that renal transplantation is not the greatest need for the generality of the population in developing countries who are battling communicable diseases, particularly malaria and HIV-AIDS. Another argument proffered is that the infrastructure in many developing economies is not sufficiently developed to support such high technology service.
There are major challenges to transplantation programs in developing economies because dialysis facilities, a useful adjunct to transplantation, are scarce. Sixty percent of an estimated one million population on hemodialysis resides in five countries (US, Japan, Germany, Brazil and Italy), whereas 20% is treated in 100 developing countries that comprise 50% of the world population.  Other obstacles to transplantation include lack of vascular access service, lack of access for patients living in remote areas to the centers for dialysis and transplantation and lack of manpower. Even where technical expertise exists such as in South Asia, economic, cultural and societal indifference to organ donation has hampered renal transplantation. 
| Access to Transplantation|| |
ERF is more prevalent in racial and ethnic minorities in the United States, and although organ donation rates are lower in these groups, AA wait twice longer for transplantation than Caucasian Americans. Furthermore, ethnic minorities in the US are more likely not to be offered transplantation as a treatment choice or to die waiting for a transplant than their counterparts.  The reasons for this disparity in the rate of transplantation include: lack of awareness of the need for organ donation, religious myths and misconceptions, mistrust of medical system, concerns about allocation issues, money and insurance barriers, and attitudes of medical practitioners.  Inequity of access is a major issue in developed countries, and ability to pay may be the most significant factor in developing countries.
Improved understanding of the immune system and the availability of effective immunosuppressive drugs have made the rejection problem less imposing than earlier.  As a result, there have been significant developments in transplant services in countries like India, Pakistan, South Africa, and Sudan. However, there is a wide difference among countries with respect to organ donation practices. ,
| Transplant Tourism and Organ Trafficking|| |
The lack of legislation and infrastructure has prevented growth of deceased donor programs in most developing countries; so, living donors have continued to be the major source of transplantable kidneys.  Individuals in developing countries are aware of the technological developments and treatment modalities elsewhere, and given the financial means would seek such treatment. Patients seeking renal transplantation in a different country would usually have to travel with an identified donor. Some patients from developed countries with established transplant programs, whose immediate prospects of being transplanted are low, travel to other countries where they can acquire kidneys either from executed prisoners or live unrelated donors (LURD).  LURD transplantation is amenable to donor recruitment by undesirable or illegal practices. The possibility of coercion is one of the major concerns of LURD.  Commercial LURD transplantation is made possible because a high proportion of the population in developing countries lives below the poverty line and some believe that selling an organ can positively change their circumstances. Chugh and Jha  believe that commercial transaction is involved in most LURD renal transplants in developing countries.
Transplant tourism is dictated by market laws and is profit driven. It is thought that the lack of provision of transplant services in developping countries has made transplant tourism inevitable.  Though commercial transplantation is prohibited in most countries, , the practice of organ sales is common in some parts of the world and drives transplant tourism.  The countries where such practices are pervasive score poorly on the corruption perception index compiled by Transparency International.  The declaration of Instanbul  on organ trafficking and transplant tourism provides clear strategies for stopping these practices, but no sanctions for those states failing to comply. It is suspected that in some countries such as India, where there is a strong government initiative against organ trafficking, sale of organs might still be going on due to bribery and corruption.  The lack of awareness of organ donation or the social and cultural barriers to it also fuel commercial kidney transplantation in developing countries. 
Though controversial and condemned by many international organizations, transplant tourism is perceived in certain cultures and developing economies as a human right that meets the demands of all stakeholders and should therefore be organized rather than declined in the interest of Western countries.  Clemmons  advocates a legalized organ market as a way of curtailing the black market in organ procurement, but this risks donors being treated as commodities.
Reported outcomes of commercial kidney transplants may not be reliable for the following reasons: commercial transplantation is illegal, recipients of such transplants return to their native countries soon after the operation and may not return for follow up, and it may not be in the interest of practitioners to publish poor results.  Transplants performed in less than ideal circumstances are characterized by inadequate pre-transplant evaluation, general lack of information about preoperative issues, immunosuppression, and long term outcome. They are also associated with a high incidence of surgical complications, acute rejection, and invasive infection, which cause major morbidity and mortality. ,,,,,,,,,,, A comprehensive review of commercial kidney transplantation performed in several developing countries showed patient and graft survival were generally inferior to those obtained in the US and a higher incidence of unconventional and life threatening infections such as malaria, invasive fungal infection, pneumonia, HIV and hepatitis.  This is supported by results of Living donor kidney transplantation (LDKT) from the UK  [Table 1].
|Table 1: Outcome of living donor renal transplantation in different economies.|
Click here to view
| Organ Donation|| |
General comments and global trends
LDKT has several advantages over deceased donor transplantation, including a shorter waiting time with the possibility of transplantation before dialysis (very useful in developing economies where dialysis facilities are scare), a lower rate of delayed graft function, and improved long-term graft survival.  In a comprehensive global assessment of LDKT involving 94 countries, Horvat et al  showed that Saudi Arabia had the highest reported living kidney donor transplant rate at 32 pmp, followed by Jordan (29 pmp), Iceland (26 pmp), Iran (23 pmp), and the US (21 pmp). Rates of LDKT have steadily risen in most regions of the world. 
LURD, which became popular following the successful experience of spousal and other unrelated LDKT by Pirsch et al  and Wyner and co-workers,  is an important factor in the increase in living donor transplants seen in many countries.  Despite this increase, about 30% of potential kidney donor/recipient pairs are biologically incompatible and do not proceed to living donor transplantation.  New strategies to expand the living donor pool include paired kidney exchange, altruistic donation, desensitization and transplantation across ABO blood group barrier ,,, -measures that may not be practicable in developing countries at present.
Assessment of potential living donors
The Amsterdam Forum has established guidelines for ensuring safe selection of donors.  All donors should have certain standard tests performed [Table 2],  and where indicated, tests for trypanosomiasis, schistosomiasis, Brucellosis More Details, and typhoid should be included.  The purpose of assessment of living kidney donation is to discover medical conditions that could increase donor risk of complications and to determine whether the donor can provide a suitable graft for the recipient. Living kidney donation is justified only if it results in minimal or no harm to the donor (including being left with the better kidney) and a significant benefit to the recipient.
Due to the relatively low yield and significant workload involved, staged assessment with the possibility of exclusion of donors at an early stage is particularly appropriate.  Exclusions during the first stage assessment, when non-invasive, less expensive tests are performed, avoid unnecessary investigations in the second stage. As CT angiography (defines the vascular anatomy, thereby contributing to the decision on which kidney to remove) exposes potential donors to irradiation and is the most expensive of the tests, it should be conducted last.  Donor related morbidity constitutes the reason for exclusion on medical grounds in approximately 2-23% of potential donors; ,,, this may be possibly higher in developing countries due to hidden morbidity in residents.
Living donor nephrectomy (LDN) may be performed by the following methods: open (posterior, posterolateral, anterolateral); totally laparoscopic; ,, and hand-assisted laparoscopic (HALDN) methods.  The technique of LDN has evolved from open lumbotomy, through mini-incision muscle-splitting open donor nephrectomy, to minimally invasive laparoscopic approaches.  Minimally invasive techniques also include hand-assisted retroperitoneoscopic, pure retroperitoneoscopic, and robotic assisted live donor nephrectomy. In a comprehensive review of the literature, Dols et al  showed that despite longer operation and warm ischemia times, laparoscopic LDN results in shorter hospital stay, faster recovery, less pain, less blood loss, earlier return to work, and better quality of life compared to conventional open LDN, but no statistically significant differences when compared to minimally invasive open approach. A meta-analysis of LDN (3,751 laparoscopic versus 2,843 open) showed that complications were higher in the open group (P <0.007), but length of stay (P <0.001) and return to work (P <0.001) were more favorable in the laparoscopic group.  Compared to the pure laparoscopic techniques, the HALDN technique is associated with shorter operative time, less warm ischemia and a lower risk of adverse outcomes. Improvements in surgical outcomes following donor nephrectomy may enhance living donor programs. 
Risks of living kidney donation
Living kidney donors are at risk of developing surgical complications, death, and deterioration of kidney function that may result in need for dialysis and renal transplantation. Major complications (Clavien grade ≥3) of LDN (higher in laparoscopic than in open) are reported in about 2.6-4.2%, ,, but overall complication rate ranges from 8 to 47%, , with the annual center volume ≤50 being significantly associated with a risk of major complications.  Postoperative mortality following LDN is calculated to be 1:3000 (0.03%).  More recent series have reported a lower mortality rate of 0.02%, , whereas others reported no deaths. ,, Complications peculiar to laparoscopic LDN include bowel injury during trochar placement and revascularization of the ureter with a conversion to open rate of 5.7-8.3%. 
The risk of developing progressive renal impairment, hypertension, or significant proteinuria after kidney donation appears to be low. ,,,, However, Mjoen et al  showed a significant rise in blood pressure five years after donation. A recent long-term follow-up study of 3,698 donors in the US showed 11 incidents of ERF at a mean of 22.5 years after donation (180 pmp per year), which is lower than the general US population (268 pmp per year).  With over 20 years follow- up of 400 LKD, a 29% survival advantage over a comparative population cohort was found.  This is possibly because of the stringent selection criteria for kidney donors and the regular follow-up. 
Due to lack of an enabling law and an unclear definition of brain death, initial efforts at deceased donor transplantation were from cardiac death donors. The donation procedure was often performed at the bedside with crude facilities,  the sort of facilities present at many specialist hospitals in developing countries today. At the time (1960s), there was less effective method of kidney preservation and use of immunosuppressive drugs. As a result, outcomes of such transplantation were poor, and it was not surprising that with the establishment of brain stem legislation, donation after cardiac death (DCD) programs were abandoned. The situation has improved since those early days, and due to a continuing lack of organs, many transplant centers in the developed world have returned to DCD. , Where dedicated, sufficiently motivated, and trained teams are available, it is possible to introduce DCD programs (using Maastricht category III donors  ) to supplement living donor programs in developing economies.
Kidney preservation and cold ischemia times
Better outcomes of living donor compared to well-matched deceased donor renal transplants , demonstrate the impact of brain death (pre-mortem shock and cytokine release), organ preservation, and ischemia-reperfusion injury. The procedure of flushing and keeping the kidney cool during retrieval and storage either on ice or in a pulsatile perfusion machine, while awaiting implantation, reduces cellular metabolism to the barest minimum and stabilizes cell membrane to keep the internal milieu in the absence of the Na + /K + pump. Machine perfusion has been shown to be beneficial for extended criteria donor kidneys,  but the results from a UK based trial comparing machine perfusion with cold storage were equivocal.  In a report of kidney preservation involving 91,674 transplants in 195 centers spread over three continents, Opelz and Dohler  showed that graft survival in deceased donor transplants remained stable for up to 18 hours of cold ischemia and worsened further with time, particularly after 36 hours.  Other studies have shown the detrimental effects of short increments of cold ischemia time. ,
| Immunosuppression|| |
Majority of the transplant recipients are maintained on a triple regimen of steroids, calcineurin inhibitor (tacrolimus or cyclosporine) and either azathioprine or mycophenolate mofetil (MMF). The use of MMF instead of azathioprine improved survival (patient and death-censored graft loss) in AA renal transplant recipients, but disparities between them and Caucasians persisted.  Tacrolimus is superior to cyclosporine in improving graft survival and preventing acute rejection after kidney transplantation, but increases post-transplant diabetes mellitus. , AA require a 37% mean higher dose of tacrolimus than Whites to achieve compatible blood concentrations.  The excess risk of acute rejection in Blacks may reflect differences in immune responsiveness  and/or pharmacokinetics of immunosuppressive agents.  The profound deleterious effect of acute rejection appears to be largely responsible for the accelerated rate of late graft loss in AA. 
Though cheap, steroids are associated with severe complications prompting several authors to advocate steroid-free maintenance immunosuppression. , Late steroid withdrawal is associated with an increase in acute rejection  or long-term deterioration of renal function, even in the absence of overt acute rejection.  However, rapid withdrawal (≤7 days post-transplantation) is not complicated by increased acute rejection rate. Steroid withdrawal protocols require the use of new and more expensive agents and protocol biopsies.  These are difficult objectives to meet in developing countries.
Due to a narrow therapeutic index for most immunosuppressive drugs, there is a fine balance between underdosing (associated with acute rejection) and overdosing (associated with infections and malignancy and organ-specific toxicities). A significant complication of immunesuppression is the development of de novo cancer after solid organ transplantation.  There is a 2-3 times increase in cancer incidence and the risk is related to the type, degree, and duration of immunosuppression, and viral co-factors and recipient age. A major obstacle to effective immunosuppression in developing countries remains the cost of these drugs.
| Outcome of Renal Transplantation|| |
The risk and type of infection varies with time after transplantation.  Bacterial infections are common during the first month. Thereafter, viral, particularly cytomegalovirus (CMV), fungal, and opportunistic infections take over. Mycobacterium tuberculosis is an important consideration in patients in developing countries,  with 15% developing the infection in Pakistan.  This has implications for immunosuppression monitoring due to drug interactions requiring cyclosporine dose adjustments and tuberculosis prophylaxis with isoniazid in transplant recipients in countries with prevalence of tuberculosis. 
CMV infection (viral replication regardless of symptoms) and CMV disease (symptoms/ invasion) , are the most common infectious complications affecting solid organ transplant recipients. It is necessary to perform serological tests pre-transplant to define the status of both the donor and recipient. The highest category of risk is when a positive donor kidney is implanted into a negative recipient. The lack of adequate laboratory facilities and the prevalence of malaria may account for the low incidence of CMV infection reported in some developing countries. , The options are to either adopt universal prophylaxis for the highest risk group or monitor viral replication and apply pre-emptive therapy. The cost of effective prophylaxis may be prohibitive, but the logistic demands of monitoring viral replication may make the alternative option equally difficult.
Medium to long-term outcome
Patient and graft survival are best with LRD transplantation, followed by LURD, donation after brain death (DBD) and then DCD transplants. Despite histo-incompatibility, the survival rates of LURD transplantation were reportedly higher than those of DBD kidneys.  Though early results of LRD and LURD kidney transplantation are comparable,  the degree of mismatch exerts a significant influence on long-term graft survival as demonstrated by 10-year graft survival of 73% for HLA identical grafts and 55% for other allografts.  Blacks are reported to have a worse outcome following transplantation than non-Blacks. Whether the transplant experience of Black people living in developed countries can be extrapolated to those living in developing countries is not known. A single UK center reported that all transplant outcomes were significantly worse for Black than non-Black patients, for example, death-censored graft survival (5-year 66% versus 87%) and first-year graft loss (12% versus 3.8%). 
Whether the poor outcomes of commercial transplantation [Table 2] reflect poor preparation of recipients prior to transplantation is not entirely clear. Prolonged waiting for renal transplantation is associated with increased morbidity and mortality.  In developing countries where dialysis facilities are scarce, many patients do not start dialysis on time or do not dialyze properly, rendering it difficult to know the influence of the duration before transplant on function. Meier-Krische and co-workers  analyzed the outcome of paired donor kidneys using the United States Renal Data System data (USRDS) and showed a 10-year overall adjusted graft survival of 69% for pre-emptive transplants versus 39% for transplants after 24 months on dialysis for cadaveric transplants. For living donor transplants, the figures were 75% and 49%, respectively.
| Current Developments and Way Forward|| |
Several cross-sectional surveys in developing countries suggest that only about 60% (majority of whom were educated and of a high socioeconomic status) had some level of knowledge about organ donation ,, and approximately 30% were willing to consider organ donation.  The main pillars of the Sindh Institute of Urology and Transplantation (SIUT), Pakistan program, are: alleviation of poverty; educating the general population; and expanding transplant programs in public sector hospitals where commerce is less likely to play a major role. The SIUT model of funding in a community-government partnership has increased transplant activity and improved patient and graft survival substantially by ensuring free immunosuppressive drugs. 
In 2002, The Transplantation Society created the Global Alliance for Transplantation, with the purpose of reducing the existing disparity regarding transplantation activities across the globe. Following consultations with international scientific societies, international governmental organizations and pharmaceutical companies, three strategic programs have been initiated: collection of information on transplantation; expansion of education in transplantation; and development of professional guidelines for organ donation and transplantation.  This should provide real support to governments and organizations wishing to establish transplant services.
Providing renal care to all developing nations can be achieved through a concerted effort between nephrologists, governments, patients, charitable organizations, and industry.  Kidney transplantation, supported by use of the more affordable generic immunosuppressive drugs, should be promoted as the treatment of choice for ERF patients.
There is need for international cooperation aimed at supporting the development of organ donation and transplantation programs, within an effective ethical and regulatory framework, while taking into account the public health context of each country. The French programs for Morocco, Tunisia, Romania, Bulgaria, Mexico, and Vietnam on how to develop health policies regarding ERF and transplantation in a context of scarce resources provide a good model. They focus on the main public health issues relating to transplantation, particularly in terms of epidemiology, health economics, access to care, and access to immunosuppressive treatment. A program of skills transfer and mentoring of transplant units in these countries has yielded dividends in the shape of more capable and established local teams. 
A twin-pronged attack in the form of development of services and regulation is required to combat organ trafficking and transplant tourism.  At a World Health Organization Regional Consultation held in Kuwait City in 2007, transplant professionals from North Africa and the Middle East supported the development of deceased donation, opposed commercialism and transplant tourism and produced The Kuwait Statement with the following goals:
- development of a legal framework and national self-sufficiency in organ donation and transplantation in each country;
- transparency of transplantation practice; and
- preventing citizens from traveling to destination countries for commercial transplantation. 
| Conclusions|| |
ERF does not respect economic boundaries and is associated with a worse outcome in countries of low socioeconomic status. Although it makes economic sense to transplant people rather than keeping them on dialysis, dialysis services need to be improved. This would improve the health status of people awaiting transplantation and provide much needed care for those who would not succeed in getting transplanted. A private-public partnership that ensures complete transparency, public audit and accountability as exemplified by SIUT is required to properly develop transplant services. There is a plethora of efforts in many developing countries characterized by poor funding, poor organization, inadequate manpower, lack of technology, lack of ancilliary services and poor/inadequate results. A staged process of developing renal transplantation in developing countries could include the following:
The main driver for medical tourism in developing countries is the lack of adequate facilities and reliable manpower in patients' home countries. Where facilities and manpower are available, the issue is financial and/or geographic access to treatment. Most people in the medical profession and governments accept that trade in human organs for transplantation is illegal and should be stopped. However, legislation does not address the root cause. Developing transplant services all over the world has many benefits - improving results of transplantation as they would be performed legally, increasing the donor pool, making transplant tourism unnecessary and granting various governments the moral courage to fight unacceptable practices.
- Legislation on development of transplantation.
- Starting with LDKT, related donation initially and then unrelated, progressing to more complex forms.
- Developing DCD in tertiary or teaching hospitals where facilities exist or can be easily improved.
- Health and public education initiatives as a way of setting the scene for brain stem death legislation and DBD transplantation.
- Enabling targeted medical missions, skills and knowledge transfer aimed at helping local staff develop transplantation.
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Jacob A Akoh
Consultant General & Transplant Surgeon, Level 04, Derriford Hospital Plymouth PL6 8DH
[Table 1], [Table 2]