Are there differences in overall and graft survival in diabetic patients undergoing kidney

transplantation?

Paola García-Padilla, MD1,2, Valentina Dávila-Rúales, MD1, Diana. C Hurtado, MD1,2, Diana C. Vargas,

MD1,2, Oscar M. Muñoz, MD, MSc, PhD1, Mayra A. Jurado, MD1

1
Department of Internal Medicine, Pontificia Universidad Javeriana, Hospital Universitario San Ignacio,

Bogotá, Colombia
2
Unit of Nephrology, Pontificia Universidad Javeriana, Hospital Universitario San Ignacio, Bogotá,

Colombia

Corresponding author(s):

Valentina Dávila-Rúales, Department of internal medicine, Pontificia Universidad Javeriana, Hospital

Universitario San Ignacio, Kra 7 No. 40-62, 110231 Bogotá, Colombia. Email: v.davila@javeriana.edu.co

1
Abstract

Purpose:

Patients with diabetes mellitus (DM) have worse graft and overall survival, however recent evidence suggest

that the difference is now not significant. We compared the outcomes between patients with and without DM

who underwent kidney transplantation up to 10 years of follow-up.

Methods:

Survival analysis on a prospective cohort that included all patients undergoing kidney transplantation at the

Hospital Universitario San Ignacio, Colombia between 2004-2022. The log-rank test and Cox proportional

hazards model were used to compare overall and graft survival among patients with diabetes and other

etiologies of kidney failure.

Results:

385 patients were included. 60 (16%) with DM. Median follow-up was 83.3 months. Overall survival in

patients with DM was lower at 5 (75.0 vs 90.8%, p <0.001) and at 10 years (55.0% vs 86.7%, p<0.001). A

higher proportion of cardiovascular death was observed in DM (27.3 vs 8.2%,p=0.021). Death-censored graft

survival was similar in both groups (96.7% vs 93.3% at 5 years, p=0.324), and (91.7% vs 88.0% at 10 years, p

=0.783). In multivariate analysis the factors associated with global survival were, DM (HR=2.11,CI95%

1,23-3,60,p=0.006), recipient age (HR=1.05; 1,02-1,08, p<0.001), delayed graft function (HR=2.07; CI95%

1,24-3,46:p=0.005) and donor age (HR=1.03; CI95% 1,01-1,05 p= 0.002).

Conclusion:

Overall survival in diabetics is lower, possibly attributed to the older age and greater comorbidities of this

population. Therefore, diabetic patients should have a closer follow-up to control cardiovascular

comorbidities. However, there is no difference in graft survival; this should not be a justification for not

offering kidney transplantation to diabetics.

Keywords: Kidney Transplantation, Graft Survival, Diabetes Mellitus, Type 1, Diabetes Mellitus Type 2.

2
Introduction:

Diabetes mellitus (DM) and arterial hypertension are the main causes of advanced chronic kidney disease,

accounting for approximately 80% of cases [1,2]. Elderly patients with diabetes admitted to dialysis have an

increased mortality risk of up to 3.9 times compared to the general population [3].

Kidney transplantation is the best kidney replacement therapy considering the longer survival and better

quality of life [4,5,6]. Despite this, access to the benefits of this therapy is limited for patients with diabetes,

considering the age and comorbidities associated, which limits admission to the waiting list [7]. Kervinen et

al, demonstrated that patients with DM2 had a relative probability of kidney transplantation of 0.51 compared

to patients with DM1, and 0.59 compared to patients without diabetes, after adjustment for age, sex,

laboratory values and comorbidities [8].

Significant divergences exist in post-transplant outcomes reported in this population. Previous publications

show that overall and graft survival at 5 years in patients with DM is lower compared to non-DM (69 vs. 93%

for overall survival and 70 vs. 96% for graft survival, respectively) [9,10], which is possibly associated with

older age of the recipient, higher body mass index (BMI) and greater cardiovascular disease [10]. However,

some recent data have shown a significant decrease in the 5-year mortality risk in patients with diabetes (HR

0.883; CI 95% 0.817-0.954), with similar survival in both groups (88% diabetic vs. 93% non-diabetic) at 5

years post-transplantation [8,11].

There are no data published in the literature assessing the long-term outcomes of transplantation in Latin

American patients with diabetes. The aim of the present study is to evaluate the differences in overall and

kidney graft survival in patients with DM undergoing transplantation compared to adults without diabetes, in

a cohort of patients managed in a kidney transplant referral center in Colombia.

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Methods

A survival analysis was performed on a prospective cohort that included all patients over 18 years of age who

underwent kidney transplantation at the Hospital Universitario San Ignacio, Bogota (Colombia) between

December 2004 and January 2022. Those with combined pancreas and kidney transplantation and with a

follow-up time of less than 3 months were excluded. The protocol was approved by the Research and Ethics

Committee of the Pontificia Universidad Javeriana and the Hospital Universitario San Ignacio in Bogota ( act

number: MI 056-2022).

Data were collected in a standardized database, in which information was systematically recorded at each

consultation. Information evaluated included recipient data: age, BMI, gender, cause of Chronic kidney

disease (CKD), type of dialysis, date of admission to the waiting list, date of initiation of dialysis,

comorbidities, serostatus for hepatitis and cytomegalovirus(CMV); donor data: age, type (deceased or living);

transplant data: date, number of transplants, ischemia time, HLA mismatch, induction therapy, BK

polyomavirus infection, cellular rejection, delayed graft function; and follow-up data (date of last follow-up,

date and cause of graft loss, date and cause of mortality). When missing information was identified, we

reviewed the institutional electronic medical record. In patients with loss of follow-up, the vital status was

consulted in the electronic page of the administrator of the resources of the general system of social security

in health - ADRES, in which the information of the affiliates to the Colombian health system is registered in a

mandatory way.

The diagnosis of diabetes was determined at the time of transplant, the delayed graft function was defined as

acute dysfunction of the transplanted kidney that required dialysis during the first week after transplantation.

BK polyomavirus infection was ruled out in the first months after transplantation and diagnosis was made by

molecular testing (PCR in blood). All patients received CMV prophylaxis with valganciclovir for 90 days,

except those at high risk who received management for 180 days. The diagnosis of CMV infection was

4
confirmed by blood or tissue PCR. Cellular rejection was diagnosed by biopsy according to the Banff criteria

[12].

Absolute and relative frequency were used to describe categorical variables. Continuous variables were

expressed as median and interquartile range since there were no variables that met the assumption of normal

distribution according to the Shapiro-Wilk test. The difference between diabetic and non-diabetic patients was

evaluated with the chi-square test for categorical variables, and with the Mann-Whitney U test for continuous

variables. To evaluate overall and graft survival functions, the Kaplan-Meier method was used. Patients who

died with functional graft were censored for the calculation of kidney graft survival. Curves were compared

using the log-rank test.

Cox regression model was used to evaluate the effect of diabetes on overall and graft survival controlling for

recipient age, donor age, sex, donor type, heart failure, coronary artery disease, delayed graft function, cold

ischemia time, type of dialysis, number of HLA mismatch, and BK polyomavirus infection. Bivariate analysis

followed by a multivariate analysis. Values p<0.05 were considered significant. The Cox proportional hazard

assumption was evaluated with Schoenfeld residuals analysis, and confirmed with the graphical analysis of

log(-log(S(t))) vs. t or log(t), finding parallelism between the groups with and without diabetes. Statistical

analyses were performed using STATA® software (Stata Statistical Software: Release 16. College Station,

TX: StataCorp LLC).

Results

The cohort included 392 transplanted patients. Seventeen patients were excluded, 9 for graft loss before three

months of transplantation (6 for acute renal vein thrombosis, 3 for hyperacute rejection) and 8 for mortality

before completing 3 months post-transplantation (5 for sepsis, 2 for cardiovascular causes and 1 for COVID-

19). A total of 375 patients were analyzed. The recipient and donor characteristics are presented in Table 1.

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60 (16%) had diabetes (82% type 2 and 18% type 1), the median age in recipients with diabetes was higher

(60.7 vs 45.1 years, p < 0.001), as was the proportion of men (81.7% vs 56%) and BMI (Median 26 vs 23

kg/m2, p < 0.001). The main cause of CKD in the non-diabetic population was idiopathic, followed by

hypertensive, glomerulonephritis (the most common were IgA nephropathy and focal and segmental

glomerulopathy) and congenital in which the main causes were polycystic kidney disease (45.6%) and Alport

syndrome (22.8%).

The median time on dialysis for the population with diabetes was 5.6 versus 4.4 years (p<0.001). There was

no difference between groups regarding time on waiting list, type of dialysis, CMV infection, kidney

retransplantation and induction therapy. Patients with diabetes had a higher percentage of arterial

hypertension, heart failure and coronary artery disease (Table 1).

The median age of the donor was higher in the group with diabetes (45 vs. 39 years, p<0.001). Eight percent

of the population received living donor transplantation; there was no difference in the type of transplantation,

neither in HLA mismatch between groups.

Cold ischemia time, delayed graft function and BK virus infection were similar between the two groups. The

main cause of graft loss was IFTA (interstitial fibrosis and tubular atrophy) (37.2%), followed by chronic

antibody-mediated rejection (29.41%), with no significant differences between groups. The main cause of

death in both groups was infection (22 patients due to septic shock of bacterial etiology, 2 due to candidemia,

1 due to histoplasmosis and 1 due to meningeal cryptococcosis). Cardiovascular mortality was higher in the

diabetes group (27.3 vs 8.2%, p= 0.021). There was no difference in mortality due to COVID-19 (Table 2).

The median follow-up per patient was 84.3 months, with a minimum of 3 and a maximum of 120 months.

Kaplan-Meier curves for death-censored graft survival are shown in Figure 1. There was no significant

difference between recipients with and without diabetes (log rank test p =0.783).

6
Death-censored graft survival for patients with and without diabetes was 96.7% versus 93.3% at 5 years

(P=0.324), and 91.7% versus 88.0% at 10 years (P=0.783).

In both univariate and multivariate Cox regression analysis, diabetes was not associated with differences in

graft survival. We only found association with BK polyomavirus infection (HR 5.17, 95%CI 2.43-11.0,

p<0.01) (Table 3).

The overall survival curves are shown in Figure 2. A significant difference was found between recipients with

diabetes compared to those without diabetes (log rank test p<0.001).

Overall survival in patients with diabetes was lower at 5 (75.0 vs 90.8%, p<0.001) and 10 years (55.0% vs

86.7%, p<0.001). In the univariate analysis the factors associated with mortality were: DM (HR 4.12; 95%CI

2.53-6.68; p<0.001) male sex, coronary artery disease, heart failure, delayed graft function, recipient and

donor age. In the multivariate analysis the significant predictors for overall mortality were DM (HR = 2.11,

95%CI 1.23-3.60; p= 0.006), recipient age, delayed graft function and donor age (Table 4).

Discussion

CKD affects more than 10% of the world population [13], diabetes is one of its main causes. Of all patients

with DM, 40% develop CKD [14]. In this population the requirement for kidney replacement therapy is

increasing [15], with an increase in the risk of mortality [3]. Kidney transplantation is the treatment of choice

showing a decrease in mortality when compared to dialytic therapy [4,5,16]. In transplanted diabetic patients

there are reports of worse outcomes compared to non-diabetic patients, which has led to a decrease in the

admission of these patients to the waiting list and to receive a kidney transplant [15,17]. We found significant

differences in overall survival, but not in graft survival at 10-year follow-up.

In our study, the first cause of CKD was idiopathic, followed by arterial hypertension and in third position

diabetes mellitus. In patients with kidney transplantation and diabetes mellitus, the presence of other co-

7
morbidities such as hypertension, heart failure and coronary artery disease was more prevalent, the last two

being almost double that reported in patients without diabetes. The systematic review by Einarson et al [18],

showed that patients with DM are twice as likely to develop cardiovascular disease (CVD) and die, which

occurred in 32.2% of patients with type 2 DM and was the cause of death in 9.9% (50.3% of all deaths).

Our cohort of patients with kidney transplantation and DM had a higher mean age at the time of

transplantation compared to non-diabetics (60.7 years vs. 45.1 years), with a longer time on dialysis and no

difference in the time on the waiting list between the two groups. This may be related to the late admission of

diabetic patients to the waiting list, probably due to higher comorbidity. A French study evaluated 549

patients with advanced CKD, and documented an association between DM and lower rates of pre-transplant

evaluation and admission to the waiting list [19]. Likewise, they are more likely to be inactivated from the

waiting list as demonstrated by Schold et al [20]. Ningyan et al [21], evaluated 1265 patients and found that

38.8% of patients were removed from the waiting list for CVD, with diabetes being a factor associated with

increased risk of CVD (HR 5.13).

In our study, overall survival is lower in transplanted patients with diabetes compared to those without DM,

both at 5 and 10 years (75% and 55% respectively compared to 90.8% and 86.7% in non-diabetic patients).

Kronson et al [22] found a survival of 61% at 5 years in diabetic kidney transplant patients. Rocha et al, [9]

evaluated 124 transplanted patients, with survival at 5 and 10 years of 69% and 50% for diabetics versus 96%

and 84% for non-diabetics. However, more recent studies report an improvement in the survival of

transplanted diabetic patients [11], without finding differences in graft or patient survival when compared to

the non-diabetic transplanted population, probably due to the effect of new treatments that can impact

cardiovascular risk and improve glycemic control [23].

Despite the decrease in overall survival observed in our study in the diabetic population, it is still better when

compared with survival data from hemodialysis patients. In the survival analysis published by M Vijayan et al

[24], patients with diabetes on hemodialysis presented a survival of 20% at 5 years, similar to that reported by

8
the 2014 United States Renal Data system reporting a survival of 37.2 % at 5 years after initiation of

hemodialysis [1], much lower than the survival achieved in our study of 75% at 5 years

Among the causes of mortality in the transplanted population with diabetes, cardiovascular disease ranks first

[10,23]. In our study, infection was the leading cause of death in both patients with diabetes (30.3%) and

without diabetes (32.6%). However, cardiovascular disease in diabetics accounted for 27.27% of all causes of

mortality compared to 8% in non-diabetics. Other publications have also shown an increased risk of infection

in transplanted diabetic patients explained by altered immunity [25].

In the multivariate analysis, the predictors of overall mortality were DM, recipient age, delayed graft function

and donor age. These findings confirm diabetes as an independent risk factor for mortality in this population.

This is explained by the cardiovascular risk that diabetes confers by presenting endothelial damage, cellular

dysfunction, increased oxidation, mitochondrial dysfunction, neurohormonal activation with increased

fibrosis and cardiomyocyte hypertrophy [26].

Regarding graft survival censored by death, no difference was found between the two groups, either at 5 years

or 10 years after transplantation. In the univariate and multivariate analysis, BK polyomavirus infection was

the only factor associated with graft loss. Other studies have reported similar results, finding no impact of

diabetes on graft survival [9,23]. This may be related to the new immunosuppressive regimens that decrease

the probability of rejection, which is the first reported cause of graft loss in the kidney transplant population

[27]. However, Tsai JP et al [28] found an increase of IFTA in kidney biopsies with a higher probability of

graft failure in diabetic patients. In our population, no differences were found between the causes of graft loss

between patients in both groups, including IFTA, BK polyomavirus and rejection.

Our study has limitations, since we did not record information related to changes in the treatment received for

diabetes over time, neither compliance with glycemic control goals, which could explain the differences

found in cardiovascular mortality in the population with diabetes. New prospective studies will be required to

9
evaluate whether changes in these variables over time can explain the differences observed in comparison

with other transplant groups.

Conclusion

Death-censored graft survival was similar in patients with and without diabetes. On the other hand, survival of

patients with DM was lower, possibly attributed to older age and comorbidities, suggesting the need for close

monitoring of cardiovascular disease. Kidney transplantation offers better survival of the diabetic patient

compared to dialysis, therefore, diabetes, should not be a limitation or contraindication to receive kidney

transplantation.

Declarations:

Ethical aspects: The conduct of this research work had as ethical guidelines the international considerations

of international consensuses such as the Helsinki declaration, and its complementary documents. The study

was approved by the Research and Ethics Committee of the Pontificia Universidad Javeriana and the Hospital

Universitario San Ignacio in Bogotá.

Conflicts of interest: The authors declare that they have no potential conflicts of interest with respect to the

research, authorship or publication of this article.

Funding: The authors received no financial support for the research, authorship, or publication of this article.

Authors contributions: All authors contributed to the conception and design of the study. Material

preparation, data collection and analysis were performed by Paola Karina Garcia Padilla, Diana Carolina

Vargas, Oscar Mauricio Muñoz, Valentina Dávila Ruales, Diana Carolina Hurtado, Mayra Alejandra Jurado.

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 The first version of the manuscript was written by Valentina Dávila Ruales and Diana Carolina Hurtado and

all authors commented on earlier versions of the manuscript. All authors read and approved the final

manuscript.

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Tabla 1. Characteristics of the donor and recipient according to the diagnosis of diabetes mellitus
Characteristic DM Non DM p-value
(n 60) (n 315)
Recipient
Type of DM (n, %)
DM1 11(2,93)
DM2 49(13,07) - -
HbA1c 3 months postrasplante (median,IQR) 7(6,9-8) -
Recipient age (y) (median,IQR) 60,7(63,7-64,8) 45,1(34,2-52,3) <0,001
Waiting time (Mo) (median,IQR) 16,4(5,9-39,5) 16(5,6-29,9) 0,680
Recipient gender (males, %) 49(81,7) 179(56,83) <0,001
Recipient BMI, Kg/m2 (median,IQR) 25,9(23,6-28,9) 23,3(20,96-25,6) <0,001
Duration of dialysis (Y) (median,IQR) 5,6(2,98-9,33) 4,41(2,20-6,46) 0,007
Type of dialysis
HD 39(65) 210(66,67)
Both 6 (10) 41(13,02)
Peritoneal 15(25) 48(15,24)
No dialysis 0(0) 16(5) 0.098
Positive CMV serostatus (n,%) 55(91,67) 287(91,4) 0,946
Retrasplantation (n,%) 4(4,7) 29(9,21) 0,524

Comorbidities (n,%)
Viral Hepatitis 1(1,67) 9(2,86) 0,600
Arterial Hypertension 57(95,0) 255(80,9) 0,008
Heart failure 24(40,0) 70(22,2) 0,004
Coronary heart disease 24(40,0) 70(22,2) 0,004
Stroke/TIA 2(3,33) 17(5,4) 0,504

Cause of CKD
DM 59(99,3) 0
Arterial Hypertension 0 74(23,5)
<0,001
SLE 0 20(6,35)
Vasculitis 0 3(0,95)
GMN 1(1,67) 54(17,14)
Congenital 0 57(18)
Other 0 19(6)
Idiopathic 0 88(27,94)
Induction theraphy (n,%)
Basiliximab 40(66,7) 180(57,14)
Daclizumab 0(0) 6(1,90)
rATG 18(30) 122(38,73) 0,360
Donor
Living donor (n,%) 4(6,67) 26(8,25) 0,678
Donor Age (y) (median,IQR) 45(33-53) 39 (26-50) 0,006
HLA mismatch 5-6 ± SD 6(10,0) 53 (16,8) 0,183
*Waiting time: time on waiting list for transplant. BMI, body mass index; TIA, transient ischemic attack; HD,
hemodialysis; both,
peritoneal dialysis and hemodialysis, CKD, chronic kidney disease; IQR, interquartile range, rATG, rabbit anti-
thymocyte globulin.

14
Tabla 2. Characteristics of kidney transplantation and outcomes according to the diagnosis of diabetes
mellitus

Characteristic DM Non DM p-value

(n 60) (n 315)
Cold ischaemia (h) (median,IQR) 12 (9-16) 13(9-16) 0,798
Delayed graft function (n, %) 13(22,0) 52 (16,5) 0,304
BK polyomavirus * (n,%) 4(6,67) 20(6,37) 0,924
Cause of graft lost (n,%)
IFTA 4(57,14) 15(34)
BK polyomavirus 1(14,3) 4(9)
Acute rejection 0 2(4,55) 0,177
Humoral rejection 1(14,3) 14(31,8)
Other 1(14,3) 9(20,45)
Cause of death (n,%)
Cardiovascular disease 9(27,27) 4(8,16)
Idiopathic 4(12,2) 6(12,24)
Infection 10(30,3) 16(32,65) 0,021
COVID19 8(24,24) 15(30,61)
Cancer 2(6) 0
Other 0 8(16,33)
* CV in the first year as screening and those with compromised renal function, IQR, interquartile range,
IFTA, Interstitial Fibrosis and Tubular Atrophy

15
Table 3. Univariate and multivariate Cox regression analysis of graft loss in kidney transplant patients

Covariate Univariate analysis Multivariate analysis

HR 95% CI P-value HR 95% CI P-value
DM 0,87 (0,34-2,23) 0,78 1,25 (0,458-3,45) 0,65
Recipient age 0,98 (0,96-1,00) 0,13 0,97 (0,94-0,995) 0,02
Recipient 1,22 (0,67-2,23) 0,51 -
gender
Type of dialysis 1,03 (0,72-1,47) 0,86 -
Heart failure 1,44 (0,75-2,76) 0,27 -
Coronary 1,44 (0,75-2,76) 0,27 -
disease
Type of donor 0,32 (0,04-2,33) 0,26 -
Mismatch 1,09 (0,95-1,26) 0,21 -
DGF 0,70 (0,27-1,77) 0,45 -
Cold ischemiae 0,99 (0,93-1,06) 0,96 -
Donor age 1,02 (0,99-1,04) 0,07 1,02 (0,998-1,04) 0,62
BK 5,18 (2,47-10,8) <0,001 5,17 (2,43-11,01) <0,001
polyomavirus

HR, hazard ratio; CI, confidence interval; DFG, delayed graft function

16
 Table 4. Univariate and multivariate Cox regression analysis of overall mortality in kidney transplant
patients

Covariate Univariate analysis Multivariate analysis

HR 95% CI P-value HR 95% CI P-value
DM 4,12 (2,53-6,68) <0,001 2,11 (1,23-3,60) 0,006
Recipient age 1,07 (1,05-1,10) <0,001 1,05 (1,02-1,08) <0,001
Recipient 0,67 (0,40-1,12) 0,13 -
gender
Type of dialysis 0,96 (0,71-1,29) 0,80 -
Heart failure 2,36 (1,46-3,80) <0,001 -
Coronary 2,36 (1,46-3,80) <0,001 -
disease
Type of donor 0,37 (0,09-1,52) 0,16 -
Mismatch 1,01 (0,89-1,14) 0,85 -
DGF 2,42 (1,45-4,01) <0,001 2,07 (1,24-3,46) 0,005
Cold ischemiae 1,03 (0,98-1,08) 0,19 -
Donor age 1,05 (1,03-1,07) <0,001 1,03 (1,01-1,05) 0,002
BK 0,82 (0,29-2,24) 0,69 -
polyomavirus

HR, hazard ratio; CI, confidence interval; DFG, delayed graft function

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Fig 1.Kaplan-Meier analysis of censored graft survival. KT, Kidney transplant

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Fig 2.Kaplan-Meier analysis of global Survival. KT, kidney transplant

19