Objectives: Renal allograft function and graft survival depends on many factors, including the source of the graft, immunologic matching between donor and recipient, incidence of acute rejection, and recurrence of the original kidney disease. This work aimed to evaluate the effects of the original kidney disease on patient and graft survival.

Materials and Methods: This was a retrospective, single-center study that included 2189 kidney transplant recipients who were transplanted at The Urology and Nephrology Centre, Mansoura University, between 1976 and 2010. Of 2189 recipients, 1350 patients with unknown original kidney disease were excluded, with the remaining 839 patients divided into 4 groups according to their original kidney disease.

Results: We found pretransplant dialysis and blood transfusion to be statistically significant among the 4 groups. Regarding induction immunosuppressive therapy, a statistical significance was found between the 4 groups regarding the presence and type of induction therapy, with no statistical significance regarding the type of maintenance immunosuppression. There was no statistical significance between the 4 groups regarding the incidence of acute and chronic rejection. We also found recurrence of original kidney disease to be statistically significant in the 4 groups, particularly in the group that included patients with glomerular disease, where the highest rate of recurrence was reported in patients with focal segmental glomerulosclerosis and membranop­roliferative glomerulonephritis, and patient and graft survival was also statistically significant.

Conclusions: The original kidney disease has an effect on renal allograft function and graft and patient survival.

Key words : Graft outcome, Living donor, Recurrence

Introduction

Despite significant improvements in 1-year kidney allograft survival, the rate of chronic graft loss after the first year remains substantial, with perhaps no improvement over the past decade.¹ In addition, despite a reduction in acute rejection rates, there have been no improvements over the past 10 years in long-term allograft survival.² The rate of decline in kidney allograft function appears to have slowed, suggesting that improved results related to long-term allograft survival are possible.³ Several factors have been shown to influence graft survival, including delayed graft function,⁴ presence of HLA antigen antibodies,⁵ type of kidney (whether from living or deceased donor),⁶ pretransplant dialysis and dialysis duration versus preemptive transplant,⁷ episodes of acute rejection,⁸ and sensitization by pregnancy, blood transfusion, or prior HLA mismatched allograft.⁹ Inadequate renal mass may be associated with a higher risk of renal graft failure; this is based on the observation of lesser graft survival rates with older and very young donor kidneys.¹⁰ Tissue injury that may be induced by different events, including brain death, cold ischemia time, ischemia and/or reperfusion, and infection, is thought to be a critical risk factor for both early delayed graft function and late allograft dysfunction.4 Also, drug noncompliance is one of the most important risk factors for renal graft loss over the long term.¹¹ Other nonimmunologic factors include posttransplant hypertension, hyper­lipidemia, a more marginal kidney, calcineurin inhibitor nephrotoxicity, and recurrent or de novo glomerular disease.¹²

Recurrence of original kidney disease results in significantly lower short- and long-term allograft survival and is considered the third most common cause of graft loss after death with functioning graft and chronic allograft nephropathy.¹²

Materials and Methods

This work was carried on all patients with end-stage renal disease who received a transplant at Mansoura Urology and Nephrology Center starting from March 1976 to the end of December 2010. The study was approved by the Ethical Review Committee of our hospital. Patient data were retrospectively reviewed, and patients with unknown original kidney disease were excluded. Patients with known original kidney disease (839 patients) were then classified according to their original kidney disease into 4 groups.

Group 1 comprised 320 patients with known pretransplant glomerular diseases, including focal segmental glomerulosclerosis, membranous nephro­pathy, mesangial-proliferative glomerulonephritis, membranoproliferative glomerulonephritis, crescentic glomerulonephritis, diabetic nephropathy, hereditary nephritis, and amyloidosis. Group 2 comprised 57 patients with hypertensive nephrosclerosis. Group 3 included 55 patients with polycystic kidney disease. Group 4 comprised 407 patients with urologic causes of renal failure.

Pretransplant evaluation
All patients were evaluated before kidney transplant, with thorough history including emphasis on original kidney disease, previous blood transfusion, pre­transplant hemodialysis and its duration, presence of type 2 diabetes mellitus and hypertension, and clinical and laboratory investigations including immunologic work-up. All patients received grafts from living-related donors, except in some situations in which unrelated donors were accepted, including for presence of hereditary kidney disease, second transplant, and absence of medically suitable related donor.

Posttransplant evaluation
After kidney transplant, our recipients were primarily immunosuppressed according to the standard protocols. These included different immuno­suppressive drugs such as steroids, tacrolimus, cyclosporine, mycophenolate mofetil, sirolimus, and azathioprine. Serum creatinine levels, creatinine clearance, urine dipstick, and 24-hour proteinuria were used to evaluate graft function, prevalence of acute and chronic rejection episodes, and recurrence of original kidney disease, with graft biopsy carried out in cases of graft impairment or presence of proteinuria. Patient survival and graft survival also were assessed.

Additional data collected
Additional data collected included recipient age and sex, donor age and sex, donor and recipient relationship, same or different compatible blood group (HLA-A, HLA-B, and HLA-DR, with number of matches and mismatches), and viral profile (hepatitis B surface antigen and antibody, hepatitis C virus antibody, Cytomegalovirus IgM, human immunodeficiency virus 1 and 2 antibodies).

Statistical analyses
Qualitative data were displayed as cross tabulations, and quantitative data were described in terms of means ± standard deviation. Bivariate techniques were used for initial evaluation of contrasts. Thus, the chi-square and Fisher exact tests were used for comparisons of frequencies of qualitative variables; the Mann-Whitney test and the unpaired t test were used for comparisons of means of two quantitative variables. P values < .05 were considered statistically significant. Graft and patient survival rates were assessed using the Kaplan-Meier method. All statistical analyses were performed with SPSS software for Windows (SPSS: An IBM Company, version 16.0, IBM Corporation, Armonk, NY, USA).

Results

Demographic data of the donors and recipients The mean age of recipients was lower in the glomerular and urologic groups (26.6 vs 28.6 y), with statistical significance shown in relation to mean age for the hypertension and polycystic kidney disease groups (34.8 and 37.4 y; P < .001); however, no statistically significant difference between the 4 groups was shown regarding mean age of donors. There was a statistically significant difference regarding the recipient gender, with male predominance in the urologic, hypertension, and polycystic kidney disease groups versus the glomerular disease group (P < .001). In addition, male predominance was noticed among donors in both the glomerular disease and polycystic kidney disease groups versus the hypertension and urologic groups, with high statistical significance (P < .001). Consanguinity also showed statistical significance between the 4 groups (P < .001) (Table 1).

Pretransplant hypertension, dialysis, and hepatitis C infection detected by hepatitis C virus antibody Pretransplant hypertension had a high statistical significance (P = .003), with of course highest percentage in the hypertension group (100%) followed by the glomerular group (60.3%). In addition, pretransplant dialysis showed statistical significance, with great number of preemptive transplants in the polycystic kidney disease and urologic disease groups (P = .01). However, pretransplant hepatitis C virus infection had no significance despite being prevalent in all 4 groups (P = .244)  (Table 2).

Immunologic work-up
Pretransplant testing for HLA class I and HLA-DR was carried out and showed that HLA class I mismatch showed statistical significance difference among the 4 groups (P = .003), with no significance regarding HLA-DR mismatch (Table 3).

Induction and maintenance immunosuppression
A statistical significance was found among the 4 groups regarding presence and type of adjuvant therapy (P < .001), with basiliximab induction having the highest percentage. There was a statistical significance regarding total dose of steroid in the first 3 months among the different groups (P = .001) (Table 4). Regarding maintenance primary immuno­suppressive protocol, no statistical significance was found among the 4 groups (Table 5).

Posttransplant medical complications
A statistical significance was found between the 4 groups regarding the development of posttransplant type 2 diabetes mellitus, with the highest prevalence among polycystic kidney disease patients (P < .001). In addition, posttransplant hypertension showed statistical significance (P = .01) with more prevalence among the hypertension group followed by the glomerular disease group. Regarding posttransplant bacterial infection, viral infection, and malignancy, no statistical significance was found (Table 6). No statistical significance was found regarding acute tubular necrosis (ATN), calcineurin inhibitor nephrotoxicity, type of acute rejection, and chronic rejection among the 4 groups (Table 7).

Recurrence of original kidney disease
A statistical significance was found between the 4 groups regarding recurrence of original kidney disease (Table 8), which was more evident in the group with glomerular diseases and with the highest rate of recurrence found for patients with focal segmental glomerulosclerosis and membrano­proliferative glomerulonephritis (Table 9).

Multivariate analyses
All factors that had a significant value in the univariate analysis among the 4 groups underwent multivariate analyses. We found that only donor age, donor sex, HLA antigen mismatching, type of induction therapy, total dose of steroid in the first 3 months after transplant, and hypertension before and after transplant sustained their significance on multivariate analysis (Table 10).

Graft and patient survival
A statistical significance was shown in the 4 groups regarding 10-year graft and patient survival (Figures 1 and 2).

Discussion

Kidney transplant is the treatment of choice for selected patients with end-stage renal disease. A successful kidney transplant improves the quality of life and reduces mortality risk for most patients, when compared with maintenance dialysis.¹³

Transplant is a treatment and not a cure. Although it may restore kidney function to the recipient, it does not necessarily remove the cause of the recipient’s original kidney disease. Therefore, we should be aware that many diseases can recur in the allograft and, in some cases, can lead to graft failure.¹⁴ However, the type of original kidney disease is not a contraindication to transplant.¹⁵

In our study, we found a statistical significance in the 4 groups regarding patient and graft survival, with the best patient survival shown in the group with polycystic kidney disease, followed by glomerular diseases and urologic diseases, and worst patient survival shown in patients with hypertensive nephrosclerosis (P = .005). The deleterious effect of hypertension on graft and patient survival has been demonstrated by many studies; one of these was carried out by Opelz and Döhler¹⁶ who found that consistent control of systolic blood pressure to ≤ 140 mm Hg during the first 5 years after transplant was associated with the best graft and patient outcomes. In addition, hypertension is a strong risk factor for the development of cardiovascular diseases, which is considered to be the most common cause of death in patients with functioning grafts.¹⁶

Regarding graft survival, we found that the best graft survival was found in the polycystic kidney disease group followed by the urologic disorder group and then the glomerular disease group, with worst graft survival for the hypertensive nephrosclerosis group (P = .026). This significant inferiority of graft outcome in the glomerular disease group may be attributed to the recurrent glo­merulopathy that occurs only in such patients. It is also well known that recurrence has a significant adverse effect on short- and long-term graft function and is considered the third most common cause of graft loss after death with functioning graft and chronic allograft nephropathy. This finding is supported by the study done by Fairhead and Knoll who stated that recurrence of glomerular disease is a strong determinant of long-term outcome after kidney transplant.¹⁷ Jeon and associates also found that graft survival is affected mainly by recurrent glomerulonephritis.¹⁸ In contrast, Toledo and associates found no differences in graft survival between long-term recurrence of glomerulonephritis and other causes of chronic graft dysfunction. The recurrence of primary disease did not worsen the renal graft prognosis versus other causes of chronic graft dysfunction. This difference was because of racial differences, small number of patient studied in this study, and differences in immunosuppressive protocols.¹⁹

In our study, the rate of acute rejection episodes showed no statistical significance in the 4 groups (P = .12), reflecting that original kidney disease had no effect on incidence of acute and chronic rejection. This finding was in concordance with those reported by Yazici and associates who compared incidence of rejection among recipients with reflux nephropathy as a cause of end-stage renal disease in relation to the general population and found no significant dif­ference.²⁰ Similarly, Moroni and associates showed that the incidence of acute and chronic rejection was not higher in patients with focal segmental glomerulo­sclerosis or idiopathic membranous nephropathy than in those with other causes of end-stage renal disease.²¹ The same results were obtained by Vega and associates who found no differences in rate of acute rejection episodes between kidney transplant recipients who had polycystic kidney disease and the control group,²² with this finding also supported by Kute and associates.²³

Regarding recurrence of original kidney disease, our study showed a statistically significant difference in the 4 groups regarding the incidence of recurrence, most commonly occurring with glomerular disorders. However, recurrence did not exist in the polycystic kidney disease group, a finding consistent with that published by Bretagnol and associates.²⁴ Therefore, recurrence affects outcome of kidney transplant and graft survival. Such a finding is consistent with those published by Morozumi and associates and Moroni and associates, who found that recurrence of native kidney disease after kidney transplant affects between 10% and 20% of patients and accounts for up to 8% of graft failures.^25,26

Regarding the frequency of recurrent glomerular disease in kidney allograft, we found that focal segmental glomerulosclerosis and membrano­proliferative glomerulonephritis are the most common recurrent diseases in the renal allograft with frequency of 10.5%. For focal segmental glomer­ulosclerosis, this rate is considered lower than recurrence rates reported by other studies, including Shimizu and associates²⁷ who reported recurrent focal segmental glomerulosclerosis in about 30% of studied recipients. This finding is also supported by Choi and associates²⁸ who stated that recurrence of primary focal segmental glomerulosclerosis was 48% in Korean renal allograft recipients. The difference of these rates may be attributed to demographic variation, difference in types of induction and maintenance immunosuppressive protocols, age of presentation of glomerulonephritis, and duration of active disease before dialysis.

Regarding membranoproliferative glomerulo­nephritis as original kidney disease, our study found a recurrence rate of 10.5%; this percentage is much less than that reported by Ponticelli and associates who found a recurrence rate ranging from 27% to 65%.²⁹ Similar findings were found in other studies, such as that by Lorenz and associates who reported nearly similar results to the latter.³⁰ The major difference between our study and others may be due to presence of larger number of patients (1321 patients) and also to difference in study methodology, as Lorenz and colleagues used a protocol biopsy in detection of recurrence, whereas in our study only event biopsy was carried out. Therefore, a more accurate detection of subclinical cases was not traced.

Although it is well known from the literature that membranous nephropathy carries a high risk of recurrence in the renal allograft, our recurrence rate was 0%. This finding differs from other studies that showed recurrence rates of 10% to 45%.³¹ Other studies by Debiec and associates and Kennedy and associates demonstrated recurrence rates of 30% to 45%.^32,33 The difference between these results could be attributed to racial differences and the use of kidney grafts from deceased donors. Another study by Dabade and associates showed the same result.³⁴ However, in that study, all patients had surveillance allograft biopsies done at the time of kidney implant (time 0) and at 4, 12, 24, and 60 months after transplant. These biopsies were not motivated by clinical events; rather, they were done at fixed time points after transplant.

Regarding crescentic glomerulonephritis, we found no recurrence in the included renal allograft recipients who had crescentic glomerulonephritis in the native kidney biopsy. Although there are limited data about crescentic glomerulonephritis recurrence, Nachman and associates published that crescentic glomerulonephritis secondary to small vessel vasculitis recurred in 17% of cases. However, regarding antiglomerular basement membrane antibody disease, published data have shown variable recurrence, with rates ranging from 0% to 50% and incidence markedly decreased if transplant was carried out after having negative antiglomerular basement membrane antibody for 6 to 12 months before transplant. However, we found no recurrent antiglomerular basement disease among our studied groups. This might be explained by the long duration of patients that had antiglomerular basement disease as original kidney disease from transplant until circulating antiglomerular basement disease levels declined to very low or even undetected levels.³⁵

Regarding mesangioproliferative glomerulo­nephritis and IgA nephropathy, a recurrence rate of 9.7% was observed in this study versus a much higher incidence described by Floege, with histologic recurrence rate reaching 60%, of which 13% of patients showed some recurrence-related renal graft dysfunction and approximately 5% lost their graft as a result of recurrent IgA nephropathy.³⁶

Regarding the recurrence of hemolytic uremic syndrome and thrombotic thrombocytopenic purpura, this study showed no recurrence. The published data showed recurrence rates of 25% to 50%; however, this may be an overestimation because both acute vascular rejection and calcineurin inhibitor therapy can lead to vascular injury and a thrombotic microangiopathy indistinguishable from the primary disease.³⁷

Lupus nephritis is well known to recur in the renal allograft, and the rate of recurrence is variable. In 2010, Contreras and associates reported that recurrent lupus nephritis occurred in 2.44% of their studied cases.³⁸ In our patient groups, we had a recurrence rate of 6.25%. This difference is attributable to the well-known racial differences for lupus nephritis and its female-to-male predominance, as 41.6% of studied patients were female in our study but 81.8% in the previously mentioned study.

Amyloidosis is one of the secondary disorders affecting native kidneys and may lead to end-stage renal disease. Previous studies have shown that amyloid light-chain amyloidosis and hereditary amyloidosis regularly recur after kidney transplant; however, few examples have been reported in the literature.39 In one example, successful renal transplant without recurrence of amyloidosis after 9 years was described in a patient with familial Apo lipoprotein II amyloidosis.⁴⁰ The recurrence in the renal allograft is mainly dependent on the cause of amyloidosis. Up to 26% of patients with reactionary amyloidosis secondary to chronic inflammatory disorders such as rheumatoid arthritis and familial Mediterranean fever may develop a renal recurrence.41 In our study, we found a biopsy-proven recurrence rate of 8.3% of all diagnosed cases of renal amyloidosis pretransplant.

Conclusions

The recurrence of original kidney disease is a possible and variable complication after renal transplant. Through this extended work, we reported a significant difference between the 4 groups included, particularly in the glomerular disease group, where the highest rate of recurrence was reported in patients with focal segmental glo­merulosclerosis and membranoproliferative glo­merulonephritis. We also documented a statistical significance regarding both patient and graft survival, reflecting the importance of original kidney disease as a determinant of both patient and graft survival.

References:

1. Hariharan S, Johnson CP, Bresnahan BA, Taranto SE, McIntosh MJ, Stablein D. Improved graft survival after renal transplantation in the United States, 1988 to 1996. N Engl J Med. 2000;342(9):605-612.
   CrossRef - PubMed
2. Meier-Kriesche HU, Schold JD, Srinivas TR, Kaplan B. Lack of improvement in renal allograft survival despite a marked decrease in acute rejection rates over the most recent era. Am J Transplant. 2004;4(3):378-383.
   CrossRef - PubMed
3. Kasiske BL, Gaston RS, Gourishankar S, et al. Long-term deterioration of kidney allograft function. Am J Transplant. 2005;5(6):1405-1414.
   CrossRef - PubMed
4. Quiroga I, McShane P, Koo DD, et al. Major effects of delayed graft function and cold ischaemia time on renal allograft survival. Nephrol Dial Transplant. 2006;21(6):1689-1696.
   CrossRef - PubMed
5. Terasaki PI, Ozawa M. Predictive value of HLA antibodies and serum creatinine in chronic rejection: results of a 2-year prospective trial. Transplantation. 2005;80(9):1194-1197.
   CrossRef - PubMed
6. Port FK, Merion RM, Goodrich NP, Wolfe RA. Recent trends and results for organ donation and transplantation in the United States, 2005. Am J Transplant. 2006;6(5 Pt 2):1095-1100.
   CrossRef - PubMed
7. Gill JS, Tonelli M, Mix CH, Johnson N, Pereira BJ. The effect of maintenance immunosuppression medication on the change in kidney allograft function. Kidney Int. 2004;65(2):692-699.
   CrossRef - PubMed
8. Cole EH, Johnston O, Rose CL, Gill JS. Impact of acute rejection and new-onset diabetes on long-term transplant graft and patient survival. Clin J Am Soc Nephrol. 2008;3(3):814-821.
   CrossRef - PubMed
9. Cecka JM, Cicciarelli J, Mickey MR, Terasaki PI. Blood transfusions and HLA matching--an either/or situation in cadaveric renal transplantation. Transplantation. 1988;45(1):81-86.
   CrossRef - PubMed
10. de Fijter JW. The impact of age on rejection in kidney transplantation. Drugs Aging. 2005;22(5):433-449.
    CrossRef - PubMed
11. Butler JA, Peveler RC, Roderick P, Smith PW, Horne R, Mason JC. Modifiable risk factors for non-adherence to immunosuppressants in renal transplant recipients: a cross-sectional study. Nephrol Dial Transplant. 2004;19(12):3144-3149.
    CrossRef - PubMed
12. Briganti EM, Russ GR, McNeil JJ, Atkins RC, Chadban SJ. Risk of renal allograft loss from recurrent glomerulonephritis. N Engl J Med. 2002;347(2):103-109.
    CrossRef - PubMed
13. Schnuelle P, Lorenz D, Trede M, Van Der Woude FJ. Impact of renal cadaveric transplantation on survival in end-stage renal failure: evidence for reduced mortality risk compared with hemodialysis during long-term follow-up. J Am Soc Nephrol. 1998;9(11):2135-2141.
    PubMed
14. Chadban S. Glomerulonephritis recurrence in the renal graft. J Am Soc Nephrol. 2001;12(2):394-402.
    PubMed
15. Briggs JD, Jones E. Recurrence of glomerulonephritis following renal transplantation. Scientific Advisory Board of the ERA-EDTA Registry. European Renal Association-European Dialysis and Transplant Association. Nephrol Dial Transplant. 1999;14(3):564-565.
    PubMed
16. Opelz G, Dohler B, Collaborative Transplant S. Improved long-term outcomes after renal transplantation associated with blood pressure control. Am J Transplant. 2005;5(11):2725-2731.
    CrossRef - PubMed
17. Fairhead T, Knoll G. Recurrent glomerular disease after kidney transplantation. Curr Opin Nephrol Hypertens. 2010;19(6):578-585.
    CrossRef - PubMed
18. Jeon HJ, Kim YS, Lee SM, et al. The effect of recurrent glomerulonephritis and acute rejection episodes in zero human leukocyte antigen-mismatched kidney transplantation. Transplant Proc. 2012;44(3):600-606.
    CrossRef - PubMed
19. Toledo K, Perez-Saez MJ, Navarro MD, et al. Impact of recurrent glomerulonephritis on renal graft survival. Transplant Proc. 2011;43(6):2182-2186.
    CrossRef - PubMed
20. Yazici H, Caliskan Y, Ozturk S, Ozkan O, Turkmen A, Sever MS. Outcome of kidney transplantation following end-stage renal disease due to reflux nephropathy. Transplant Proc. 2011;43(5):1566-1569.
    CrossRef - PubMed
21. Moroni G, Gallelli B, Quaglini S, Banfi G, Montagnino G, Messa P. Long-term outcome of renal transplantation in adults with focal segmental glomerulosclerosis. Transpl Int. 2010;23(2):208-216.
    CrossRef - PubMed
22. Vega J, Lira D, Medel S, Betancour P, Goecke H, Carrasco A. [Outcome of renal transplantation in patients with autosomal dominant polycystic kidney disease]. Rev Med Chil. 2012;140(8):990-998.
    CrossRef - PubMed
23. Kute VB, Shah PR, Goplani KR, et al. Deceased donor kidney transplantation in autosomal dominant polycystic kidney disease: a single-center experience. Saudi J Kidney Dis Transpl. 2011;22(5):911-916.
    PubMed
24. Bretagnol A, Buchler M, Boutin JM, Nivet H, Lebranchu Y, Chauveau D. [Renal transplantation in patients with autosomal dominant polycystic kidney disease: pre-transplantation evaluation and follow-up]. Nephrol Ther. 2007;3(7):449-455.
    CrossRef - PubMed
25. Morozumi K, Takeda A, Otsuka Y, Horike K, Gotoh N, Watarai Y. Recurrent glomerular disease after kidney transplantation: an update of selected areas and the impact of protocol biopsy. Nephrology (Carlton). 2014;19 Suppl 3:6-10.
    CrossRef - PubMed
26. Moroni G, Longhi S, Quaglini S, et al. The impact of recurrence of primary glomerulonephritis on renal allograft outcome. Clin Transplant. 2014;28(3):368-376.
    CrossRef - PubMed
27. Shimizu A, Higo S, Fujita E, Mii A, Kaneko T. Focal segmental glomerulosclerosis after renal transplantation. Clin Transplant. 2011;25 Suppl 23:6-14.
    CrossRef - PubMed
28. Choi KH, Kim SI, Yoon SY, et al. Long-term outcome of kidney transplantation in adult recipients with focal segmental glomerulosclerosis. Yonsei Med J. 2001;42(2):209-214.
    CrossRef - PubMed
29. Ponticelli C, Glassock RJ. Posttransplant recurrence of primary glomerulonephritis. Clin J Am Soc Nephrol. 2010;5(12):2363-2372.
    CrossRef - PubMed
30. Lorenz EC, Sethi S, Leung N, Dispenzieri A, Fervenza FC, Cosio FG. Recurrent membranoproliferative glomerulonephritis after kidney transplantation. Kidney Int. 2010;77(8):721-728.
    CrossRef - PubMed
31. Sprangers B, Lefkowitz GI, Cohen SD, et al. Beneficial effect of rituximab in the treatment of recurrent idiopathic membranous nephropathy after kidney transplantation. Clin J Am Soc Nephrol. 2010;5(5):790-797.
    CrossRef - PubMed
32. Debiec H, Hanoy M, Francois A, et al. Recurrent membranous nephropathy in an allograft caused by IgG3kappa targeting the PLA2 receptor. J Am Soc Nephrol. 2012;23(12):1949-1954.
    CrossRef - PubMed
33. Kennedy C, Traynor C, O'Kelly P, Dorman A, Conlon PJ. Transplant outcomes in patients with idiopathic membranous nephropathy. Int J Nephrol. 2013;2013:818537.
    CrossRef - PubMed
34. Dabade TS, Grande JP, Norby SM, Fervenza FC, Cosio FG. Recurrent idiopathic membranous nephropathy after kidney transplantation: a surveillance biopsy study. Am J Transplant. 2008;8(6):1318-1322.
    CrossRef - PubMed
35. Nachman PH, Segelmark M, Westman K, et al. Recurrent ANCA-associated small vessel vasculitis after transplantation: A pooled analysis. Kidney Int. 1999;56(4):1544-1550.
    CrossRef - PubMed
36. Floege J. Recurrent IgA nephropathy after renal transplantation. Semin Nephrol. 2004;24(3):287-291.
    CrossRef - PubMed
37. Oyen O, Strom EH, Midtvedt K, et al. Calcineurin inhibitor-free immunosuppression in renal allograft recipients with thrombotic microangiopathy/hemolytic uremic syndrome. Am J Transplant. 2006;6(2):412-418.
    CrossRef - PubMed
38. Contreras G, Mattiazzi A, Guerra G, et al. Recurrence of lupus nephritis after kidney transplantation. J Am Soc Nephrol. 2010;21(7):1200-1207.
    CrossRef - PubMed
39. Chen DJ, Jiang H, Yang H, He Q, Wang HP, Chen JH. Unusual cause of proteinuria and re-renal failure after kidney transplantation: de novo localized AL amyloidosis in renal allograft. Int Urol Nephrol. 2010;42(2):507-511.
    CrossRef - PubMed
40. Magy N, Liepnieks JJ, Yazaki M, Kluve-Beckerman B, Benson MD. Renal transplantation for apolipoprotein AII amyloidosis. Amyloid. 2003;10(4):224-228.
    CrossRef - PubMed
41. Ponticelli C, Moroni G, Glassock RJ. Recurrence of secondary glomerular disease after renal transplantation. Clin J Am Soc Nephrol. 2011;6(5):1214-1221.
    CrossRef - PubMed