- Email: [email protected]
The Impact of Time-Zero Biopsy on Early Graft Outcomes After Living Donor Kidney Transplantation
The Impact of Time-Zero Biopsy on Early Graft Outcomes After Living Donor Kidney Transplantation A.L. Lee, Y.S. Kim, B.J. Lim, H.J. Jeong, D.J. Joo, M.S. Kim, and K.H. Huh ABSTRACT Background. In contrast with deceased donor transplantation, the clinical significance of pathologic findings in time-zero biopsies after living donor kidney transplantation are rarely reported, due to the expectation that histologic findings and renal function are normal. The aim of this study was to identify subclinical pathologic findings in living donors and examine the effect on early graft renal function. Methods. Between December 2006 and July 2011, 146 living-donor kidney transplant recipients were enrolled in this study. We retrospectively analyzed donor and recipientrelated clinical parameters, and post-transplant 6 months and 1 year estimated glomerular filtration rate (eGFR) as early graft renal function. Time-zero biopsies were evaluated using the 2007 Banff criteria. Results. Most abnormal histologic findings were of mild degree as determined by Banff scores. Global glomerulosclerosis (GS, 35.6%), tubular atrophy (CT, 36.3%), interstitial fibrosis (CI, 20.5%), vascular fibrous intimal thickening (CV, 4.1%), arteriolar hyaline thickening (AH, 14.4%), interstitial inflammation (I, 3.4%) were pathologic findings in time-zero biopsies. The univariate analysis revealed that donor age and gender were significantly associated with eGFR at post-transplant 6 months and at 1 year (P < .05). Furthermore, GS and CT were significantly associated with early graft renal function (P < .05). However, multivariate linear regression analysis showed only donor age was significantly associated with early graft renal function (P ¼ .001). Conclusion. A mild degree of subclinical, pathologic findings on time-zero biopsy did not affect early graft renal function in living-donor kidney transplantation.
T
HE CLINICAL and histologic statuses of donors are known to influence graft outcome after kidney transplantation, especially after deceased donor kidney transplantation.1e4 Many authors have reported on the importance of time-zero biopsy. Time-zero biopsies could predict allograft renal function in deceased donor kidney transplantation.5 Sometimes, unsuspected renal pathology was reported in donor kidney, although all donors were fully studied and all of them accepted the guideline criterion as healthy kidney donors.6,7 The aim of this study was to identify subclinical, pathologic findings in living donors and examine the effect on early graft renal function. MATERIALS AND METHODS Patient Selection One hundred forty-six living-donor kidney transplant recipients were enrolled in this study between December 2006 and July 2011 at
Severance Hospital, Yonsei University Health System. The clinical characteristics and histologic findings of time-zero biopsies were analyzed. This study was approved by our institutional review board.
Clinical Data We used estimated glomerular filtration rate (eGFR) at posttransplant 6 months and 1 year as parameters of early graft outcomes. The values of eGFR were calculated using with the
From the Department of Surgery and The Research Institute for Transplantation, and Department of Pathology, Yonsei University College of Medicine, Seoul, Korea. Supported by the Research Institute for Transplantation, Yonsei University College of Medicine. Address reprint requests to Kyu Ha Huh, MD, PhD, Department of Surgery, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemoon-gu, Seoul 120-752, Korea. E-mail: [email protected]
ª 2013 by Elsevier Inc. All rights reserved. 360 Park Avenue South, New York, NY 10010-1710
0041-1345/13/$esee front matter http://dx.doi.org/10.1016/j.transproceed.2013.08.081
Transplantation Proceedings, 45, 2937e2940 (2013)
2937
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LEE, KIM, LIM ET AL
Table 1. Clinical Characteristics of Donors and Recipients Clinical Characteristics
Donors Age (y) Gender (male/female) Body mass index (kg/m2) Systolic blood pressure (mm Hg) Diastolic blood pressure (mm Hg) Serum creatinine (mg/dL) Creatinine clearance (mL/min/1.73 m2) Recipients Age (y) Gender (male/female) Body mass index (kg/m2) History of diabetes Human leucocyte antigen mismatch 0e1 2e4 5e6 Mian immunosuppressant Cyclosporine Tacrolimus
Mean SD or %
40.7 11.4 65/81 23.1 3.0 125.6 15.1 77.3 10.6 0.93 0.18 98.6 31.3 43.8 10.8 87/59 22.5 3.4 20 (13.7%) 33 (22.6%) 100 (68.5%) 13 (8.9%) 65 (44.5%) 81 (55.5%)
SD, standard deviation.
Modification of Diet in Renal Disease (MDRD) formula. Graft loss was defined as death or conversion to maintenance dialysis. Timezero biopsies were performed using an 18-G needle gun on the upper kidney pole before reperfusion. Paraffin-embedded permanent sections were stained with hematoxylin and eosin with Masson trichrome, and read by a pathologist specializing in transplantation. Histopathologic findings were rated using the 2007 Banff scoring system.8,9
independent t-test or analysis of variance and the chi-square-test or linear regression analysis. Multivariate linear regression analysis was performed with adjustment for recipient and donor clinical parameters. Kaplan-Meier survival curves were used for graft survival analysis. A two-sided P < .05 was considered to be significant.
RESULTS Patient Characteristics
Mean donor age was 40.7 11.4 years. Mean serum creatinine and creatinine clearance values were 0.93 0.18 mg/dL and 98.6 31.3 mL/min/1.73 m2. Recipients had a mean age of 43.8 10.8 years. Almost all recipients received calcineurin inhibitor based immunosuppressive therapy. Basiliximab was used as an induction therapy (Table 1). Hisotologic Findings in Time-Zero Biopsy
The mean number of glomeruli measured in time-zero biopsies was 14.0 6.8. Immunoglobulin (Ig) A nephritis was detected incidentally in 6 biopsies (5 cases in subclass I, 1 case in subclass II by the Haas classification).10 Abnormal histologic findings were obtained in 61.6% of the 146 biopsies. Glomerulosclerosis (GS), tubular atrophy (CT), interstitial fibrosis (CI), arteriolar hyaline thickening (AH), vascular fibrous intimal thickening (CV), and interstitial inflammation (I) were observed in 35.6%, 36.3%, 20.5%, 14.4%, 4.1%, and 3.4%, respectively, of 135 the donor kidneys. The majority of histologic findings were of mild degree according to the Banff criteria (grade I).8,9 Post-transplant Outcomes
Statistics All statistical analyses were performed using SPSS 18.0 for Windows (SPSS, Chicago, IL). Univariate analysis was performed using the
Mean eGFRs at post-transplant 6 months and 1 year were 60.2 17.6 and 62.3 18.7 mL/min/1.73 m2. Mean followup duration after transplantation was 33 18.8 months, and
Table 2. Univariate Analysis of the Association Between Histologic Parameters and Graft Outcome Banff Score (n ¼ 146)
Glomerulosclerosis 0% (n ¼ 94; 64.4%) <10% (n ¼ 25; 17.1%) 10% (n ¼ 27; 18.5%) Tubular atrophy 0 (n ¼ 93; 63.7%) 1 (n ¼ 53; 36.3%) Interstitial fibrosis 0 (n ¼ 116; 79.5%) 1 (n ¼ 30; 20.5%) Arteriolar hyaline thickening 0 (n ¼ 125; 85.6%) 1 (n ¼ 21; 14.1%) Vascular fibrous intimal thickening 0 (n ¼ 140; 95.9%) 1 (n ¼ 6; 4.1%) Interstitial inflammation 0 (n ¼ 141; 96.6%) 1 (n ¼ 5; 3.4%)
eGFR at 6 Months
P
eGFR at 1 year
.016 62.76 18.11 53.82 10.1 54.37 17.16
65.03 19.03 57.16 10.37 54.90 20.40 .044
62.39 19.03 56.26 14.04
.006 65.52 17.97 56.61 18.75
.995 60.19 18.42 60.17 14.33
.63 62.69 18.71 60.84 18.83
.676 60.44 18.06 58.70 14.95
.681 62.57 18.78 60.75 18.5
.295 60.51 17.75 52.79 12.81
.081 62.87 18.70 49.26 13.75
.799 60.13 17.67 62.41 17.18
eGFR, estimated glomerular filtration rate. Univariate analysis was conducted using the independent t-test and analysis of variance.
P
.018
.451 62.09 18.86 69.84 9.57
IMPACT OF TIME-ZERO BIOPSY
2939
Table 3. Multivariate Analysis of the Association between Clinicohistological Parameters and Graft Outcome eGFR at 6 Months Parameter
Donor clinical Age Gender Systolic blood pressure Diastolic blood pressure Histologic Glomerulosclerosis Tubular atrophy
B (SE)
0.55 4.96 0.05 0.04
(0.13) (2.96) (0.11) (0.15)
P
eGFR at 1 Year B (SE)
P
.001 0.538 (0.15) .001 .097 3.5 (3.29) .29 .64 0.04 (0.12) .722 .79 0.05 (0.16) .739
2.64 (1.73) .130 1.41 (3.0) .634
2.72 (1.92) .159 4.08 (3.27) .214
eGFR, estimated glomerular filtration rate; SE, standard error. Multivariate linear regression analysis was adjusted for recipients’ clinical parameters.
all patients were followed for at least 1 year. The graft survival of 146 recipients was 98.6% at 1 and 5 years; only two recipients experienced graft failure during the year following transplantation. Associations Between Clinical Parameters, Histologic Findings, and Early Graft Outcomes
The univariate analysis revealed that donor age and gender were significantly associated with eGFR at post-transplant 6 months and 1 year (P ¼ .001, .001 in eGFR at 6 months, P ¼ .001, .017 in eGFR at 1 year, respectively, Table 2). In addition, histologic findings were found to be associated with early graft outcomes. GS and CT were significantly associated with early graft outcome (P ¼ .016, .044 in eGFR at 6 months, P ¼ .018, .006 in eGFR in eGFR at 1 year, respectively; Table 2). A multivariate linear regression analysis showed only donor age affected early graft renal function (Table 3). DISCUSSION
Glomerulosclerosis, interstitial fibrosis, hypertensive vascular changes, and tubular atrophy have been suggested to predict poor graft survival, and donor age has been consistently reported to be associated with allograft outcome.11e18 Furthermore, age-related declines in renal function have been associated with the appearance of glomerular, tubulointerstitial, and vascular lesions in kidneys.17e20 However, the majority of these studies concerned deceased donors. In a study of time-zero biopsy in living donors, Mancilla et al7 reported that 54.4% had abnormal findings, namely, CI in 29%, CT in 13%, MI in 12%, AH in 10%, and GS in 10%. Likewise, we found abnormal findings were 61.6% of all donors and all abnormal findings were mild. Previous studies have showed that posttransplant renal function in the first year predicts long-term kidney transplant survival.1,21 We used eGFR at post-transplant 6 months and 1 year as measures of early graft renal function. As shown in results, GS and CT were associated with early graft renal function on univariate analysis. However,
donor age was only associated with early graft renal function on multivariate analysis. In the present study, the subclinical, pathologic findings of living donors were not found to be associated with early graft outcome by multivariate analysis, which could have been resulted from the mild degree of histological findings on donor kidneys. In conclusion, a mild degree of subclinical, pathologic findings on time-zero biopsy did not affect early graft renal function in living-donor kidney transplantation. Therefore, we intend to conduct a further evaluation to detect changes in graft outcome, and donor renal function, by long-term follow-up. REFERENCES 1. Anglicheau D, Loupy A, Lefaucheur C, et al. A simple clinicohistopathological composite scoring system is highly predictive of graft outcomes in marginal donors. Am J Transplant. 2008;8:2325. 2. Munivenkatappa RB, Schweitzer EJ, Papadimitriou JC, et al. The Maryland aggregate pathology index: a deceased donor kidney biopsy scoring system for predicting graft failure. Am J Transplant. 2008;8:2316. 3. Nyberg SL, Matas AJ, Rogers M, et al. Donor scoring system for cadaveric renal transplantation. Am J Transplant. 2001;1:162. 4. Pessione F, Cohen S, Durand D, et al. Multivariate analysis of donor risk factors for graft survival in kidney transplantation. Transplantation. 2003;75:361. 5. El-Husseini A, Sabry A, Zahran A, et al. Can donor implantation renal biopsy predict long-term renal allograft outcome? Am J Nephrol. 2007;27:144. 6. Rea DJ, Heimbach JK, Grande JP, et al. Glomerular volume and renal histology in obese and non-obese living kidney donors. Kidney Int. 2006;70:1636. 7. Mancilla E, Avila-Casado C, Uribe-Uribe N, et al. Time-zero renal biopsy in living kidney transplantation: a valuable opportunity to correlate predonation clinical data with histological abnormalities. Transplantation. 2008;86:1684. 8. Racusen LC, Solez K, Colvin RB, et al. The Banff 97 working classification of renal allograft pathology. Kidney Int. 1999;55:713. 9. Solez K, Colvin RB, Racusen LC, et al. Banff 07 classification of renal allograft pathology: updates and future directions. Am J Transplant. 2008;8:753. 10. Haas M. Histologic subclassification of IgA nephropathy: a clinicopathologic study of 244 cases. Am J Kidney Dis. 1997;29:829. 11. Gaber LW, Moore LW, Alloway RR, et al. Glomerulosclerosis as a determinant of posttransplant function of older donor renal allografts. Transplantation. 1995;60:334. 12. Karpinski J, Lajoie G, Cattran D, et al. Outcome of kidney transplantation from high-risk donors is determined by both structure and function. Transplantation. 1999;67:1162. 13. Pokorna E, Vitko S, Chadimova M, et al. Proportion of glomerulosclerosis in procurement wedge renal biopsy cannot alone discriminate for acceptance of marginal donors. Transplantation. 2000;69:36. 14. Randhawa P. Role of donor kidney biopsies in renal transplantation. Transplantation. 2001;71:1361. 15. Randhawa PS, Minervini MI, Lombardero M, et al. Biopsy of marginal donor kidneys: correlation of histologic findings with graft dysfunction. Transplantation. 2000;69:1352. 16. Escofet X, Osman H, Griffiths DF, et al. The presence of glomerular sclerosis at time zero has a significant impact on function after cadaveric renal transplantation. Transplantation. 2003;75:344. 17. Rao KV, Kasiske BL, Odlund MD, et al. Influence of cadaver donor age on posttransplant renal function and graft outcome. Transplantation. 1990;49:91.
2940 18. Terasaki PI, Gjertson DW, Cecka JM, et al. Significance of the donor age effect on kidney transplants. Clin Transplant. 1997;11:366. 19. Baylis C, Corman B. The aging kidney: insights from experimental studies. J Am Soc Nephrol. 1998;9:699.
LEE, KIM, LIM ET AL 20. Epstein M. Aging and the kidney. J Am Soc Nephrol. 1996;7:1106. 21. McLaren AJ, Jassem W, Gray DW, et al. Delayed graft function: risk factors and the relative effects of early function and acute rejection on long-term survival in cadaveric renal transplantation. Clin Transplant. 1999;13:266.
T
HE CLINICAL and histologic statuses of donors are known to influence graft outcome after kidney transplantation, especially after deceased donor kidney transplantation.1e4 Many authors have reported on the importance of time-zero biopsy. Time-zero biopsies could predict allograft renal function in deceased donor kidney transplantation.5 Sometimes, unsuspected renal pathology was reported in donor kidney, although all donors were fully studied and all of them accepted the guideline criterion as healthy kidney donors.6,7 The aim of this study was to identify subclinical, pathologic findings in living donors and examine the effect on early graft renal function. MATERIALS AND METHODS Patient Selection One hundred forty-six living-donor kidney transplant recipients were enrolled in this study between December 2006 and July 2011 at
Severance Hospital, Yonsei University Health System. The clinical characteristics and histologic findings of time-zero biopsies were analyzed. This study was approved by our institutional review board.
Clinical Data We used estimated glomerular filtration rate (eGFR) at posttransplant 6 months and 1 year as parameters of early graft outcomes. The values of eGFR were calculated using with the
From the Department of Surgery and The Research Institute for Transplantation, and Department of Pathology, Yonsei University College of Medicine, Seoul, Korea. Supported by the Research Institute for Transplantation, Yonsei University College of Medicine. Address reprint requests to Kyu Ha Huh, MD, PhD, Department of Surgery, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemoon-gu, Seoul 120-752, Korea. E-mail: [email protected]
ª 2013 by Elsevier Inc. All rights reserved. 360 Park Avenue South, New York, NY 10010-1710
0041-1345/13/$esee front matter http://dx.doi.org/10.1016/j.transproceed.2013.08.081
Transplantation Proceedings, 45, 2937e2940 (2013)
2937
2938
LEE, KIM, LIM ET AL
Table 1. Clinical Characteristics of Donors and Recipients Clinical Characteristics
Donors Age (y) Gender (male/female) Body mass index (kg/m2) Systolic blood pressure (mm Hg) Diastolic blood pressure (mm Hg) Serum creatinine (mg/dL) Creatinine clearance (mL/min/1.73 m2) Recipients Age (y) Gender (male/female) Body mass index (kg/m2) History of diabetes Human leucocyte antigen mismatch 0e1 2e4 5e6 Mian immunosuppressant Cyclosporine Tacrolimus
Mean SD or %
40.7 11.4 65/81 23.1 3.0 125.6 15.1 77.3 10.6 0.93 0.18 98.6 31.3 43.8 10.8 87/59 22.5 3.4 20 (13.7%) 33 (22.6%) 100 (68.5%) 13 (8.9%) 65 (44.5%) 81 (55.5%)
SD, standard deviation.
Modification of Diet in Renal Disease (MDRD) formula. Graft loss was defined as death or conversion to maintenance dialysis. Timezero biopsies were performed using an 18-G needle gun on the upper kidney pole before reperfusion. Paraffin-embedded permanent sections were stained with hematoxylin and eosin with Masson trichrome, and read by a pathologist specializing in transplantation. Histopathologic findings were rated using the 2007 Banff scoring system.8,9
independent t-test or analysis of variance and the chi-square-test or linear regression analysis. Multivariate linear regression analysis was performed with adjustment for recipient and donor clinical parameters. Kaplan-Meier survival curves were used for graft survival analysis. A two-sided P < .05 was considered to be significant.
RESULTS Patient Characteristics
Mean donor age was 40.7 11.4 years. Mean serum creatinine and creatinine clearance values were 0.93 0.18 mg/dL and 98.6 31.3 mL/min/1.73 m2. Recipients had a mean age of 43.8 10.8 years. Almost all recipients received calcineurin inhibitor based immunosuppressive therapy. Basiliximab was used as an induction therapy (Table 1). Hisotologic Findings in Time-Zero Biopsy
The mean number of glomeruli measured in time-zero biopsies was 14.0 6.8. Immunoglobulin (Ig) A nephritis was detected incidentally in 6 biopsies (5 cases in subclass I, 1 case in subclass II by the Haas classification).10 Abnormal histologic findings were obtained in 61.6% of the 146 biopsies. Glomerulosclerosis (GS), tubular atrophy (CT), interstitial fibrosis (CI), arteriolar hyaline thickening (AH), vascular fibrous intimal thickening (CV), and interstitial inflammation (I) were observed in 35.6%, 36.3%, 20.5%, 14.4%, 4.1%, and 3.4%, respectively, of 135 the donor kidneys. The majority of histologic findings were of mild degree according to the Banff criteria (grade I).8,9 Post-transplant Outcomes
Statistics All statistical analyses were performed using SPSS 18.0 for Windows (SPSS, Chicago, IL). Univariate analysis was performed using the
Mean eGFRs at post-transplant 6 months and 1 year were 60.2 17.6 and 62.3 18.7 mL/min/1.73 m2. Mean followup duration after transplantation was 33 18.8 months, and
Table 2. Univariate Analysis of the Association Between Histologic Parameters and Graft Outcome Banff Score (n ¼ 146)
Glomerulosclerosis 0% (n ¼ 94; 64.4%) <10% (n ¼ 25; 17.1%) 10% (n ¼ 27; 18.5%) Tubular atrophy 0 (n ¼ 93; 63.7%) 1 (n ¼ 53; 36.3%) Interstitial fibrosis 0 (n ¼ 116; 79.5%) 1 (n ¼ 30; 20.5%) Arteriolar hyaline thickening 0 (n ¼ 125; 85.6%) 1 (n ¼ 21; 14.1%) Vascular fibrous intimal thickening 0 (n ¼ 140; 95.9%) 1 (n ¼ 6; 4.1%) Interstitial inflammation 0 (n ¼ 141; 96.6%) 1 (n ¼ 5; 3.4%)
eGFR at 6 Months
P
eGFR at 1 year
.016 62.76 18.11 53.82 10.1 54.37 17.16
65.03 19.03 57.16 10.37 54.90 20.40 .044
62.39 19.03 56.26 14.04
.006 65.52 17.97 56.61 18.75
.995 60.19 18.42 60.17 14.33
.63 62.69 18.71 60.84 18.83
.676 60.44 18.06 58.70 14.95
.681 62.57 18.78 60.75 18.5
.295 60.51 17.75 52.79 12.81
.081 62.87 18.70 49.26 13.75
.799 60.13 17.67 62.41 17.18
eGFR, estimated glomerular filtration rate. Univariate analysis was conducted using the independent t-test and analysis of variance.
P
.018
.451 62.09 18.86 69.84 9.57
IMPACT OF TIME-ZERO BIOPSY
2939
Table 3. Multivariate Analysis of the Association between Clinicohistological Parameters and Graft Outcome eGFR at 6 Months Parameter
Donor clinical Age Gender Systolic blood pressure Diastolic blood pressure Histologic Glomerulosclerosis Tubular atrophy
B (SE)
0.55 4.96 0.05 0.04
(0.13) (2.96) (0.11) (0.15)
P
eGFR at 1 Year B (SE)
P
.001 0.538 (0.15) .001 .097 3.5 (3.29) .29 .64 0.04 (0.12) .722 .79 0.05 (0.16) .739
2.64 (1.73) .130 1.41 (3.0) .634
2.72 (1.92) .159 4.08 (3.27) .214
eGFR, estimated glomerular filtration rate; SE, standard error. Multivariate linear regression analysis was adjusted for recipients’ clinical parameters.
all patients were followed for at least 1 year. The graft survival of 146 recipients was 98.6% at 1 and 5 years; only two recipients experienced graft failure during the year following transplantation. Associations Between Clinical Parameters, Histologic Findings, and Early Graft Outcomes
The univariate analysis revealed that donor age and gender were significantly associated with eGFR at post-transplant 6 months and 1 year (P ¼ .001, .001 in eGFR at 6 months, P ¼ .001, .017 in eGFR at 1 year, respectively, Table 2). In addition, histologic findings were found to be associated with early graft outcomes. GS and CT were significantly associated with early graft outcome (P ¼ .016, .044 in eGFR at 6 months, P ¼ .018, .006 in eGFR in eGFR at 1 year, respectively; Table 2). A multivariate linear regression analysis showed only donor age affected early graft renal function (Table 3). DISCUSSION
Glomerulosclerosis, interstitial fibrosis, hypertensive vascular changes, and tubular atrophy have been suggested to predict poor graft survival, and donor age has been consistently reported to be associated with allograft outcome.11e18 Furthermore, age-related declines in renal function have been associated with the appearance of glomerular, tubulointerstitial, and vascular lesions in kidneys.17e20 However, the majority of these studies concerned deceased donors. In a study of time-zero biopsy in living donors, Mancilla et al7 reported that 54.4% had abnormal findings, namely, CI in 29%, CT in 13%, MI in 12%, AH in 10%, and GS in 10%. Likewise, we found abnormal findings were 61.6% of all donors and all abnormal findings were mild. Previous studies have showed that posttransplant renal function in the first year predicts long-term kidney transplant survival.1,21 We used eGFR at post-transplant 6 months and 1 year as measures of early graft renal function. As shown in results, GS and CT were associated with early graft renal function on univariate analysis. However,
donor age was only associated with early graft renal function on multivariate analysis. In the present study, the subclinical, pathologic findings of living donors were not found to be associated with early graft outcome by multivariate analysis, which could have been resulted from the mild degree of histological findings on donor kidneys. In conclusion, a mild degree of subclinical, pathologic findings on time-zero biopsy did not affect early graft renal function in living-donor kidney transplantation. Therefore, we intend to conduct a further evaluation to detect changes in graft outcome, and donor renal function, by long-term follow-up. REFERENCES 1. Anglicheau D, Loupy A, Lefaucheur C, et al. A simple clinicohistopathological composite scoring system is highly predictive of graft outcomes in marginal donors. Am J Transplant. 2008;8:2325. 2. Munivenkatappa RB, Schweitzer EJ, Papadimitriou JC, et al. The Maryland aggregate pathology index: a deceased donor kidney biopsy scoring system for predicting graft failure. Am J Transplant. 2008;8:2316. 3. Nyberg SL, Matas AJ, Rogers M, et al. Donor scoring system for cadaveric renal transplantation. Am J Transplant. 2001;1:162. 4. Pessione F, Cohen S, Durand D, et al. Multivariate analysis of donor risk factors for graft survival in kidney transplantation. Transplantation. 2003;75:361. 5. El-Husseini A, Sabry A, Zahran A, et al. Can donor implantation renal biopsy predict long-term renal allograft outcome? Am J Nephrol. 2007;27:144. 6. Rea DJ, Heimbach JK, Grande JP, et al. Glomerular volume and renal histology in obese and non-obese living kidney donors. Kidney Int. 2006;70:1636. 7. Mancilla E, Avila-Casado C, Uribe-Uribe N, et al. Time-zero renal biopsy in living kidney transplantation: a valuable opportunity to correlate predonation clinical data with histological abnormalities. Transplantation. 2008;86:1684. 8. Racusen LC, Solez K, Colvin RB, et al. The Banff 97 working classification of renal allograft pathology. Kidney Int. 1999;55:713. 9. Solez K, Colvin RB, Racusen LC, et al. Banff 07 classification of renal allograft pathology: updates and future directions. Am J Transplant. 2008;8:753. 10. Haas M. Histologic subclassification of IgA nephropathy: a clinicopathologic study of 244 cases. Am J Kidney Dis. 1997;29:829. 11. Gaber LW, Moore LW, Alloway RR, et al. Glomerulosclerosis as a determinant of posttransplant function of older donor renal allografts. Transplantation. 1995;60:334. 12. Karpinski J, Lajoie G, Cattran D, et al. Outcome of kidney transplantation from high-risk donors is determined by both structure and function. Transplantation. 1999;67:1162. 13. Pokorna E, Vitko S, Chadimova M, et al. Proportion of glomerulosclerosis in procurement wedge renal biopsy cannot alone discriminate for acceptance of marginal donors. Transplantation. 2000;69:36. 14. Randhawa P. Role of donor kidney biopsies in renal transplantation. Transplantation. 2001;71:1361. 15. Randhawa PS, Minervini MI, Lombardero M, et al. Biopsy of marginal donor kidneys: correlation of histologic findings with graft dysfunction. Transplantation. 2000;69:1352. 16. Escofet X, Osman H, Griffiths DF, et al. The presence of glomerular sclerosis at time zero has a significant impact on function after cadaveric renal transplantation. Transplantation. 2003;75:344. 17. Rao KV, Kasiske BL, Odlund MD, et al. Influence of cadaver donor age on posttransplant renal function and graft outcome. Transplantation. 1990;49:91.
2940 18. Terasaki PI, Gjertson DW, Cecka JM, et al. Significance of the donor age effect on kidney transplants. Clin Transplant. 1997;11:366. 19. Baylis C, Corman B. The aging kidney: insights from experimental studies. J Am Soc Nephrol. 1998;9:699.
LEE, KIM, LIM ET AL 20. Epstein M. Aging and the kidney. J Am Soc Nephrol. 1996;7:1106. 21. McLaren AJ, Jassem W, Gray DW, et al. Delayed graft function: risk factors and the relative effects of early function and acute rejection on long-term survival in cadaveric renal transplantation. Clin Transplant. 1999;13:266.