Challenges for Renal Retransplant: An Overview

Transcription

1 Challenges for Renal Retransplant: An Overview Mohamed Adel Bakr, Ahmed Abdelfattah Denewar, Mohamed Hamed Abbas Abstract Despite many achievements in renal transplant in the past few years regarding immunosuppression and tissue matching, the rates of early and late graft loss and return to dialysis are still high. Many of those with primary graft failure will be listed for a kidney retransplant, as this allows for better quality of life than dialysis. Many challenges face those requiring renal retransplant, including first graft nephrectomy and whether site of retransplant should be ipsilateral or contralateral, whether to conduct preemptive retransplant or wait while on dialysis, additional immunologic factors, immunosuppression after retransplant, cancer risk, BK virus infection, and retransplant in pediatrics. Despite the increased relative risks associated with retransplant, patients receive a significant survival benefit, better quality of life, and low health care costs versus remaining on dialysis after a failed transplant. Key words: Kidney retransplant, Donor Introduction A significant percentage of patients with failed renal grafts are candidates for retransplant. The outcomes of retransplant are worse than those of primary transplant, and sensitization is documented to be a major reason. The management of a failed allograft that is not immediately symptomatic is still very controversial. The aim of this study was to determine the effects of failed allograft nephrectomy on subsequent transplants and the importance in From the Department of Dialysis and Transplantation, Urology and Nephrology Center, Mansoura University, Mansoura, Egypt Acknowledgements: The authors declare that they have no sources of funding for this study, and they have no conflicts of interest to declare. Corresponding author: Mohamed Adel Bakr, Urology & Nephrology Center, Mansoura University, El-Gomhoria Street, PO Box: Mansoura, Egypt Phone: mabakr9092@yahoo.com Experimental and Clinical Transplantation (2016) Suppl 3: sensitization. 1 The rate of renal retransplant has increased from 7.1% for living donors and from 9.7% in deceased donors in to 11.8% in 2011, 3 to 14.5% in 2014, 4 and to 15% in 2015, 5 with immunologic risk much greater among retransplanted patients than first-time kidney recipients. It is likely that retrans plant will become even more prevalent in the future. 6 As shown in the literature, there are many challenges and controversies facing retransplant recipients. Here, we will highlight these challenges in some detail. Outcomes Outcomes of retransplant are highly dependent on many factors, including source of donor (living vs deceased donor), functional duration of first graft, and elapsed time between first and second graft. Survival rates (patient and graft) are better in patients receiving 2 related grafts and worse in patients receiving 2 sequential deceased donations, with intermediate rates of success with deceased donor retransplant after rejection of a related graft. The highest failure rate is shown in those patients who sustained an early loss of the first deceased donation and received a subsequent deceased donation graft within a few months. 7 Comparable retransplanted graft outcomes have been documented by many authors. In 2009, Barocci and associates reported on 100 patients who received retransplants between 1983 and At 1, 5, and 10 years after kidney transplant, patient survival rates were 100%, 96%, and 92%, whereas graft survival rates were 85%, 72%, and 53%. Good outcomes were shown for kidney retransplants, with allocation based on anti-hla antibody identification together with induction immunosuppression. 8 In a retrospective study conducted by Barba Abad and associates, when comparing 370 first transplant Copyright Başkent University 2016 Printed in Turkey. All Rights Reserved. DOI: /ect.tondtdtd2016.L26

2 22 Mohamed Adel Bakr et al/experimental and Clinical Transplantation (2016) Suppl 3: Exp Clin Transplant recipients and 45 second transplant recipients, graft survival rates were not different between groups (3- and 5-year survival rates of 89% and 84% vs 88% and 85%). In addition, recipient survival rates were also not different between groups (3- and 5-year survival of 98% and 96% vs 97%). 9 Another study confirmed comparable outcome results. In this study, which compared 116 retrans - plants versus 3337 first transplants, retransplant recipients were older (mean age of 46.2 ± 12.8 y) than first transplant recipients (mean age of 42.2 ± 12.8 y). The proportion of living-related kidney transplants and male sex were similar between first and retransplant recipients. Fourteen percent of retrans - plant recipients showed high immunologic risk, defined as current panel reactive antibodies 30%, compared with 3% of those in the first transplant group (P <.001). Induction therapy with anti - thymocyte globulin and anti-interleukin 2 antibody was higher in the retransplant versus first transplant group: 18.3% versus 4.3% and 60.0% versus 32.6%. Graft survival rates at 1, 5, and 10 years were 88.6%, 87.3%, and 74.4% among retransplant recipients versus 95.0%, 87.0%, and 70.7% among first trans - plant recipients (P =.63). 10 In a retrospective 10-year study between 2000 and 2009 of 62 retransplant patients, 38 patients received kidneys from deceased donors and 24 patients received kidneys from living donors. The 1-year, 5-year, and 10-year patient survival rates were 85.33%, 66.7%, and 66.7%, and the graft survival rates were 96.7%, 79.7%, and 79.7%. The acute rejection rate was 17.6%, with a mean serum creatinine concentration of 1.92 ± 0.5 mg/dl. The conclusion was that retransplant results in acceptable graft and patient survival over a 10-year follow-up and should be encouraged for better quality of life compared with dialysis. 11 Between March 1976 and January 2002, 1406 kidneys were transplanted at Mansoura Urology and Nephrology Center. Among these, 54 patients received a second graft (39 men, mean age [standard deviation] of 32.1 [8.60] y). The mean duration of the first graft was 49.1 months, and the main cause of graft failure was immunologic. The mean duration of graft failure was 17.3 months. There were 33 episodes of acute rejection in 23 patients. Most complications were hypertension (70%), infection (30%), and hepatitis (11%). The overall graft and patient survival was good; 15 grafts (27%) were lost during follow-up of 1 to 17 years. Ten patients died, 5 with a functioning graft. Multivariate analysis showed that donor relation, primary immuno - suppression, duration of first graft, and serum creatinine level at 1 year were predictors of graft survival. The conclusion was that renal retransplant is the treatment of choice in patients who have lost their graft. The use of related living donors and potent immunosuppression could help to improve outcomes. 12 In a more recent report from 2013 on 1891 first graft patients versus 73 second graft patients, 5-year and 10-year graft survival rates were reported as 86% versus 90% and 65.1% versus 77.8%. 13 On the other hand, many trials have documented inferior graft outcomes with retransplant versus first transplant. Among 61 retransplanted patients between 1990 and 2010, inferior outcomes were as expected among elderly patients, hyperimmunized recipients, and recipients with multiple surgical procedures at the site of last renal transplant. 14 Among 108 retransplanted patients (78 men and 30 women), 1-, 2-, 3-, and 5-year graft survival rates were 81.4%, 78.9%, 78.9%, and 73.7% among retransplants versus 92.9%, 91.5%, 89.8%, and 85.3% with first transplant (P =.0037). Patient survival was 96%, 94.6%, 92.4%, and 87.8% in the retransplant group versus 93.1%, 92.4%, 90.9%, and 87.4% in the first transplant group (P =.63). 15 Incorporating prior transplant outcome data to retransplant outcomes is a critical issue to be highlighted. In a study published in 2014, 16 retrans - plant recipients were more likely to be treated for acute rejection (P =.005) or were hospitalized (P =.001) within 1 year of retransplant if these outcomes were experienced within 1 year of primary transplant. Delayed graft function after primary transplants was associated with 35% increased likelihood of recurrence (P <.001). An increase in 1-year glomerular filtration rate after primary transplant was associated with increased glomerular filtration rate 1 year after retransplant (P <.001), and retransplant graft failure was inversely associated with 1-year primary transplant glomerular filtration rate. Long-term graft survival decreases with sub - sequent retransplants, which can be affected by the status of failed graft, prevention of recurrence, cause of prior graft failure, correction of technical impediments, and reduced potential for recidivism

3 Mohamed Adel Bakr et al/experimental and Clinical Transplantation (2016) Suppl 3: of nonadherence. 5 In addition, factors that sig - nificantly affected patient survival included age at time of previous transplant and factors that significantly affected graft survival included need for repeated surgery, acute rejection episodes, primary graft nonfunction, type of immunosuppression, number of HLA mismatches, and number of surgical complications. 14 Graft Nephrectomy Graft nephrectomy may be indicated before renal retransplant if refractory hypertension, persistent urinary tract infections, urinary tuberculosis, acquired renal cystic disease, or nephrotic-range proteinuria occur. It may also be indicated if graft tenderness and hematuria occur during gradual immuno suppression withdrawal. The effect of an in situ failed graft on the development of panel reactive antibodies (PRA) remains to be determined. Does the retained graft absorb or stimulate antibody production? Limited data are available. 5 Therefore, the management of an asymptomatic failed renal graft remains contro - versial. In a retrospective study that compared patients undergoing kidney retransplant with (group A) and without (group B) preliminary nephrectomy, nephrectomy led to increased PRA levels before retransplant and was associated with significantly increased rates of primary nonfunction (P =.05) and acute rejection (P =.04). Overall graft survival after retransplant was significantly worse in group A than in group B (P =.03). 17 Another retrospective study compared the number of acute graft rejections and graft survival between patients undergoing a second transplant. In 91 patients who received a second renal graft, 43 underwent graft nephrectomy (group I) and 48 kept their nonfunctional renal graft (group II). Group I had 5 episodes of acute graft rejection, whereas group II had 12 (P =.3). Six grafts (13.9 %) failed in group I and 8 (16.6 %) in group II. Five- and 10-year graft survival rates were 91% and 85% in group I and 82.7% and 69% in group II (P =.2). Panel reactive antibody level and number of acute rejection episodes did significantly influence graft survival, regardless of whether the patient had a nephrectomy (P =.2). 18 Therefore, nephrectomy does not seem to significantly influence the survival of the second graft, and nephrectomy decisions should be based on clinical indications. 19 Ipsilateral Retransplant In a retrospective study that compared 99 patients with ipsilateral versus 270 patients with contralateral retransplant, kidney retransplant in ipsilateral iliac fossa was surgically challenging, with more blood loss, significantly longer operative time, and more vascular complications and graft loss within the first year after transplant. The recommendation was to proceed with contralateral retransplant whenever feasible. 20 Donor Selection In a United Network for Organ Sharing study that analyzed outcomes, benefits, and risks of retrans - plant with expanded criteria donations (ECD), patients with ECD for first transplant were compared with 1658 patients with ECD for retransplant and patients with standard criteria donations for retransplant. The results showed that retransplant with ECD had greater risk of graft failure than the other 2 groups (hazard ratios of 1.19, 1.76), higher mortality than the other 2 groups (hazard ratios of 1.45, 1.79), worse patient survival than the standard criteria donation group (hazard ratio of 1.82), but better patient survival than first transplant with ECD group (hazard ratio of 0.89). In conclusion, there is a benefit to accepting ECD kidneys for select patients requiring retrans plant. Retransplant with ECD kidneys should be undertaken with trepidation, and appropriate informed consent should be obtained. 21 Preemptive Retransplant To determine the relation between wait time for a second transplant and outcomes after that second transplant, a study that analyzed 911 recipients from the Australia and New Zealand Dialysis and Transplant registry stated that increasing wait time, independent of donor, recipient, and immunologic factors, is associated with increased all-cause mortality (P =.001), overall graft failure (P =.001), increased risk of early acute rejection (P =.001), increased death with functioning graft (P =.001), and severe vascular/humoral rejection (P =.011). In conclusion, a prolonged wait time for a second graft is associated with inferior patient and graft outcomes. 22 In a single-center retrospective cohort that included all kidney retransplants (second trans - plants) between 2000 and 2012, 18 patients who had preemptive retransplant were compared with 83

4 24 Mohamed Adel Bakr et al/experimental and Clinical Transplantation (2016) Suppl 3: Exp Clin Transplant patients who had retransplant after starting dialysis. In the preemptive group, no patient had PRA levels > 10% at any time. In the retransplant after dialysis group, 26.5% had PRA > 10% at time of transplant (P =.014) and 54.2% had a historical highest PRA > 10% (P <.001). The rejection rate was 11.1% in the preemptive group and 27.7% in the retransplant after dialysis group during the first year after retransplant (P =.227). Patient survival rate was 100% in the preemptive group at 5-year follow-up, whereas, in the retransplant after dialysis group, it was 95.2% at 1 year and 85.9% at 5 years after retransplant. Allograft survival at 1 and 5 years was 88% and 89% in the preemptive group. However, in the retransplant after dialysis group, it was 89% after the first year and 65% at 5 years after retransplant. In conclusion, preemptive renal retransplant is a feasible option that should be assessed in patients with kidney graft failure and may help to minimize the morbidity associated with reinitiation of dialysis. 23 Immunologic Factors Recipient evaluation for antibodies with sensitive assays is mandatory before retransplant. Highly sensitized patients to HLA of potential living donations had low possibility to find a proper deceased donor. 24 HLA-DR matching of initial transplant in pediatric patients affects retransplant outcomes. Two HLA-DR mismatches with the initial graft had an adverse effect on the timing and outcome of retransplant. 5 Patients who undergo repeat kidney transplants are considered at high risk for experiencing immunologic and nonimmunologic complications. Eleven patients who underwent a third kidney transplant were investigated regarding allograft outcomes and complication rates. After transplant, 3 patients (27.2%) showed delayed graft function. Acute rejection developed in 4 patients (36.4%), and surgical complications that required surgical correction occurred in 3 patients. Allograft failure developed due to acute rejection (n = 3) or chronic rejection (n = 1) in 4 patients. Allograft survival rates at 1, 5, and 10 years were 81.8%, 42.9%, and 42.9%; however, the allograft survival rate at 5 years was > 80% in patients who underwent kidney transplant only after results of the PRA test became available. In conclusion, a third kidney transplant procedure may be acceptable, although aggressive pretransplant immunomonitoring and patient selection may be required to reduce the risks of acute rejection and surgical complications. 25 Immunosuppression A 12-month single-arm pilot trial was carried out to evaluate efficacy and safety of sirolimus-tacrolimus in high-risk patients, including 28 patients who un - derwent retransplant versus a retrospective control group administered tacrolimus-mycophenolate mofetil (69 recipients). All patients were given basiliximab induction therapy. The sirolimus group showed a higher, but not statistically significant, incidence of biopsy-proven acute rejection and a lower glomerular filtration rate than the control group. Furthermore, the sirolimus group was associated with significant increases in BK virus infection (P =.031), dyslipidemia (P =.004), and lymphocytes (P =.020). The study was terminated prematurely due to a high incidence of adverse events. 26 BK Virus BK virus has emerged as a major complication of kidney transplant. The Organ Procurement and Transplantation Network in the United States has stated BK virus as a primary or secondary cause of graft. Among 126 retransplant patients in a United Network for Organ Sharing study, first graft was lost either to transplant BK virus or BK virus attributed, with treatment for BK virus reported in 17.5% of retransplant patients. One-year acute rejection was 7%, graft survival rates at 1 and 3 years were 98.5% and 93.6%, and median glomerular filtration rate was 68.4 ml/min, with the conclusion that retransplant after BK virus infection appears to be associated with good results. 27 Whether allograft nephrectomy and viral clearance are required before retransplant is con - troversial. Some recent studies have suggested that retransplant can be successfully achieved without allograft nephrectomy if viremia is cleared before retransplant, with the only published experience of successful retransplant in the presence of active viremia occurring in the presence of concomitant allograft nephrectomy of the failing kidney. In this report, a successful repeat kidney transplant was conducted in a patient with high-grade BK viremia and fulminant hepatic failure without concomitant allograft nephrectomy, performed in the setting of a simultaneous liver-kidney transplant. 28

5 Mohamed Adel Bakr et al/experimental and Clinical Transplantation (2016) Suppl 3: Cancer Risk Recipients of kidney transplant have an elevated risk of developing cancer. There are limited data on cancer risk in recipients of kidney retransplant. In a study that included data from the Transplant Cancer Match Study, primary recipients were compared to 6621 retransplant patients. A total of 5757 cancers were observed in primary recipients and 245 in retransplants. Overall cancer risk was similar in retransplants compared with primary recipients. However, renal cell carcinoma occurred in excess among retransplants (0.6% vs 0.47%; relative risk, 2.03; 95% confidence interval, ). Overall cancer risk did not differ in retransplant patients compared with primary recipients. Increased risk of renal cell carcinoma may be explained by the presence of acquired cystic kidney disease, which is more likely to develop with additional time with kidney disease and time spent on dialysis waiting for retransplant. 29 Posttransplant lymphoproliferative disease (PTLD) is an uncommon but serious complication of solid-organ transplant. Reduction in immunosuppression is the mainstay of PTLD treatment, but it may precipitate graft loss. Retransplant remains controversial, as immuno - suppression resumption may trigger PTLD relapse. In 8 patients retransplanted after successful treatment of PTLD and median follow-up of 62.5 months (range, mo), allograft survival was 87.5% (with 7 functioning grafts and 1 failed graft from chronic rejection), with no recurrence of PTLD. In all, 5 patients had remained alive, with the other 3 dying from causes other than PTLD. In conclusion, kidney retransplant appears to be safe in patients with prior PTLD and without major risk of hematologic recurrence, provided that PTLD was in remission. 30 Retransplant in Pediatrics In an analysis of first and second graft survival among pediatric recipients (< 18 y old) who underwent kidney transplant between 1987 and 2010, patients with living-donor grafts had longer survival rates than those with deceased-donor grafts. Rates were similar among both first transplant (adjusted hazard ratio of 0.78; 95% confidence interval, ; P <.001) and second transplant (adjusted hazard ratio, 0.74; 95% confidence interval, ; P <.001). Living-donor second grafts had longer survival than deceased-donor second grafts, similarly to living-donor (adjusted hazard ratio of 0.68; 95% confidence interval, ; P <.001) and deceaseddonor (adjusted hazard ratio of 0.77; 95% confidence interval, ; P =.02) first transplants. Cumulative graft life of 2 transplants was similar regardless of the order of deceased-donor and living-donor transplant. In conclusion, deceased-donor kidney transplant in pediatric recipients followed by living-donor retransplant does not negatively affect the livingdonor graft survival advantage and provides similar cumulative graft life compared with living-donor kidney transplant followed by deceased-donor retransplant. Clinical decision-making for pediatric patients with healthy, willing living donors should consider these findings in addition to the risk of sensitization, age of the living donor, and deceaseddonor wait times. 31 Other Challenges Regarding retransplant in children, in a report of 9209 patients that included retransplant recipients, advances in clinical management and newer immunosuppressive agents have had a significant effect on improving short-term allograft function; however, it is apparent that long-term allograft function remains suboptimal. Therefore, it is likely that most pediatric renal allograft recipients will require 1 or more retransplants during their lifetime. Unfortunately, a second or subsequent graft in pediatric recipients has inferior long-term graft survival rates versus initial grafts, with decreasing rates with each subsequent graft. Multiple issues influence the outcome of retransplant, with the most significant being the cause of the prior transplant failure. Nonadherence-associated graft loss poses unresolved ethical issues that may affect access to retransplant. Graft nephrectomy before retransplant may benefit selected patients, but the effect of an in situ failed graft on the development of PRA remains to be definitively determined. It is important that these and other factors discussed in this review be taken into consideration during the counseling of families on the optimal approach for their child who requires a retransplant. 5 Conclusions Despite the increased relative risks associated with retransplant, patients receive a significant survival benefit, better quality of life, and lower health care costs versus remaining on dialysis after a failed

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