Predictive Factors for Improved Renal Function in Renal

Transplantation Recipients
Ikhlas Arief Bramono, Gampo Alam Irdam*, Gerhard Reinaldi Situmorang, Ponco Birowo,
Nur Rasyid, and Arry Rodjani
Department of Urology, Cipto Mangunkusumo Hospital, Faculty of Medicine Universitas Indonesia, Jakarta, Indonesia

ABSTRACT
Objective. The purpose of this study is to analyze varying predictive factors for improved
graft function among renal transplant recipients.
Methods. Two hundred eleven consecutive donor and recipient pairs who underwent
renal transplantation between January 2011 and December 2015 were enrolled in our
study. Factors that affected renal graft function were analyzed. Statistical analyses were
performed using SPSS version 16.0 software (SPSS Inc, Chicago, IL, United States).
Results. The mean age of donors in years was 30 (range, 17-62), with a mean body mass
index (BMI) of 23.20 kg/m2 (range, 16.10-39.50). Mean total warm ischemic time in
minutes was 44.80 (range, 26.10-83.45). The mean age of the recipients in years was 48
(range, 12-78) with a mean BMI of 22 kg/m2 (range, 14.80-37.30). Estimated glomerular
filtration rate at 6 and 12 months post-transplantation were 69 mL per minute per 1.73 m2
(range, 10-137) and 65 (range, 16-110), respectively. Based on several parameters, there
was no significant factor that improved renal graft function at 6 and 12 months after
transplant. Total warm ischemic time almost showed statistical significance in predicting
improved renal graft function after transplant. Future study with a longer period of
observation and a larger sample size should be done for further investigation.
Conclusions. Total warm ischemic time is a promising parameter to predict improved
renal graft function post-transplantation.

C HRONIC kidney disease (CKD) continues to be a

health problem worldwide [1]. CKD is a global prob-
lem of a growing proportions [2]. In 2006, incidence rate of
Furthermore, it can be used as a guideline in treating
patients with ESRD who underwent kidney transplant.

patients with end-stage renal disease (ESRD) who under- METHODS

went hemodialysis in Indonesia were 30.7 per million pop-
ulation. Meanwhile, the prevalence rates of ESRD were
23.4 per million population [1].
Renal transplantation is considered the gold standard in
treating patients with ESRD [1e4]. It offers a better short-
term and long-term survival compared with dialysis treat-
ment [1,2]. The Kidney Disease Improving Global
Outcomes (KDIGO) guidelines recommended measuring
serum creatinine daily for at least 7 days or until hospital
discharge, whichever occurs sooner[5].
In this study, we would like to predict renal function in
renal transplantation recipients based on several parame-
ters. The prediction can help kidney transplantation team to
identify improvement in the renal function of the recipient.
Study Design
Two hundred eleven renal transplant recipients and their donors
who were operated on at our transplantation center between
January 2011 and December 2015 were enrolled. The data was
collected and analyzed retrospectively by medical record review.
Confidentiality of the patients’ identity was guaranteed.
*Address correspondence to Gampo Alam Irdam, Department
of Urology, Cipto Mangunkusumo Hospital, Faculty of Medicine
Universitas Indonesia, Diponegoro No 71, Jakarta 10430,
Indonesia. Tel: þ62-21-3152892; Fax: þ62-21-3145592. E-mail:
gampo.alam@yahoo.com

ª 2019 Published by Elsevier Inc. 0041-1345/19

230 Park Avenue, New York, NY 10169 https://doi.org/10.1016/j.transproceed.2019.11.017

Transplantation Proceedings, 52, 127e132 (2020) 127

128 BRAMONO, IRDAM, SITUMORANG ET AL

Sampling Design Table 1. Baseline Characteristics

Sampling was performed consecutively during the period of April

Variables Mean (Range)
2016 until March 2017.
Recipient
Patient’s Inclusion and Exclusion Criteria Age (y) 48 (12-78)
BMI (kg/m2) 22 (14.80-37.30)
We included donors and recipients of kidney transplantation who
6 mo eGFR (mL/min/1.73 m2)* 69 (10-137)
underwent nephrectomy through laparoscopy procedure at our
12 mo eGFR (mL/min/1.73 m2)* 65 (16-110)
center. We only performed living donor nephrectomy.
Donor
Age (y) 30 (17-62)
Parameters Analyzed
BMI (kg/m2) 23.20 (16.10-39.50)
Factors analyzed included estimated glomerular filtration rate Total warm ischemic time (min) 44.80 (26.10-83.45)
(eGFR) (preprocedure and 6 and 12 months after transplant),
Abbreviations: BMI, body mass index; eGFR, estimated glomerular filtration
recipient age, recipient sex, donor’s age, donor’s sex, donor- rate.
*
recipient relationship, donor’s calculated body mass index (BMI), eGFR was measured using Modification of Diet in Renal Disease equation.
delayed graft function (DGF) in recipient, and total warm ischemic
time. We used the 4-variable Modification of Diet in Renal Disease transplantation, respectively. We found there were no sta-
(MDRD) formula as a creatinine-based eGFR equation to evaluate tistically significant results regarding sex that influenced
renal function in renal transplantation recipients. The MDRD improvement in renal function. Donors and recipients of the
equation is an accurate formula that can predict eGFR from serum same sex did not produce a better result than cross-sex
creatinine concentration [6e11]. The measurement was obtained donor-recipient groups (male to female or female to male).
with the following mathematical calculation: 186  (serum creati- Several factors that were involved in improving renal
nine mg/dL)1.154  (age in years)0.203  (0.742 if female)  (1.21 function of renal transplantation recipients are depicted in
if African American) [6].
Table 2. The study analyzed kidney function during follow-
Statistical Method up at 6 and 12 months after renal transplant. We can see
that at 6 months, factors such as donor age, total warm
Each parameter is categorized into groups. Recipient and donor ischemic time, recipient age, pre-transplant eGFR, DGF,
age was categorized as younger than 45 years and older than 45 and donor-recipient relationship do not correlate signifi-
years [12e14]. BMI of both recipient and donor was grouped as
cantly to the patient’s renal function. However, at 12
underweight, normal, overweight, and obese [15]. Before the pro-
cedure and at 6 and 12 months after the procedure, the eGFR for
months after operation, multivariate analysis showed a
the recipients was divided into 2 categories (above 40 mL/min/1.73 potential protective factor for patients with an eGFR below
m2 and below 40 mL/min/1.73 m2) [13,14]. Pre-transplantation 40 (P ¼ .049), indicating that less total warm ischemic time
eGFR was divided into 2 categories (below 15 mL/min/1.73 m2 and
above 15 mL/min/1.73 m2) [5]. For donors, several additional pa- Table 2. Predictive Factors for Improved Renal Function in Renal
rameters were also categorized. Total warm ischemic time was Transplantation Recipient
divided into less than 45 minutes and more than 45 minutes [16].
The donor-recipient relationship was categorized into related and P Value

not related. Meanwhile, arteries were categorized into single and Follow-up: 6 Mo Follow-up: 12 Mo
multiple artery. The kidney side for the donors was grouped into Factors Bivariate* Multivariate† Bivariate* Multivariate†
left and right, and the DGF was divided into yes and no based on
Donor age (y) .62 .36 .39 .64
the presence of delay [17,18]. We used the statistical software SPSS
Total warm ischemic .41 .99 .05 .049
version 16.0 (IBM Corp, Armonk, NY, United States) to perform
time (min)
c2 testing on each parameter for bivariate analysis. For multivariate
Recipient age (y) .67 .50 .71 .79
analysis, we performed logistic regression. To generate the optimal
Pre-transplant eGFR‡ .62 .54 .93 .13
cut-off value predicting the risk factors that may lead into low
(mL/min/1.73 m2)
eGFR with the highest sensitivity and specificity, we performed
DGF .39 1.00 .36 .05
receiver operating characteristic (ROC) analysis.
Donor-recipient .24 .99 .77 .89
relationship
RESULTS Multiple renal arteries .27 .99 .69 .35
graft
A related kidney donor was found in 34.6% patients. Mul-
tiple arteries were found in 9.5% donors. Baseline charac- All factor parameters were categorized into groups: donor and recipient
aged <45 years and >45 years; total warm ischemic time <45 min and >45 min;
teristics of our patients are depicted in Table 1. More than 4 BMI into underweight, normal, overweight, and obese; pre-transplantation eGFR
out of 5 donor nephrectomies were performed on the left into <15 mL/min/1.73 m2 and >15 mL/min/1.73 m2; DGF into yes and no;
donor-recipient relationship into related and not related; and arteries into single
side (82.9%). Many of our recipients were > 45 years old and double artery.
(60.7%) whereas most of our donors were < 45 years old Abbreviations: BMI, body mass index; DGF, delayed graft function; eGFR,
estimated glomerular filtration rate.
(86.3%). Less than half (48.3%) of total warm ischemic time *
Statistical analysis for bivariate analysis used c2 analysis for categorical
was done in less than 45 minutes. An eGFR of > 40 mL per variables.
†
Statistical analysis for multivariate analysis were used logistic regression
minute per 1.73 m2 was found in 94.79% and 92.41% analysis for categorical variables.
‡
recipients after 6 months and 1 year after renal eGFR was measured using Modification of Diet in Renal Disease equation.
RENAL FUNCTION IN TRANSPLANT RECIPIENT
(< 45 minutes) would lower the probability of reaching an
eGFR below 40 mL per minute per 1.73 m2 (odds ratio ¼
0.123; 95% confidence interval, 0.05-0.99). Other factors do
not offer significant correlation with improved renal func-
tion in renal transplantation recipients in either bivariate or
multivariate analyses. These factors include donor age,
recipient age, DGF, and donor-recipient relationship.
A further investigation with ROC analysis on total warm
ischemia time toward the level of eGFR under 40 mL per
minute per 1.73 m2 was done (Fig 1). Our study found that a
cut-off at above 44.9 minutes of total warm ischemia time
may predict whether the eGFR at 12 months post-transplant
will be below 40 mL per minute per 1.73 m2 with the most
optimal sensitivity and specificity.
DISCUSSION
Since its emergence as an alternative treatment for ESRD,
kidney transplantation has gone through much develop-
ment. It is now established as the best available treatment
for patients with ESRD. Several pre-transplant factors have
129
been established to predict likelihood of success or failure in
5 years. This is largely due to the factors’ effect on
glomerular filtration rate (GFR). Owing to a shortage in
deceased donors, living donors have been increasing in
popularity. Their numbers have increased by 5-fold between
1980 and 2000. In some places, such as Europe, the United
States, and Japan, living donors have surpassed cadaveric
donors in number. Through means of living kidney
donation, donors may not be genetically related to the
recipient [19].
The most popular means to assess kidney function is
through eGFR, though arguably there is not a single
parameter that is adequate in predicting allograft future
function and survival. Overall, the factors could be divided
into immunologic and nonimmunologic factors. Non-
immunologic factors include donor age, donor sex, ethnicity,
BMI, original disease recurrence, total warm ischemic time,
renal function before procedure, and the presence of co-
morbid conditions (eg, hypertension, hepatitis C, viral in-
fections, diabetes, etc). A look at some of the variables will
be discussed.
Fig 1. ROC curve for total warm
ischemic time in reaching
eGFR under 40 mL/min/1.73 m2,
12 months of follow-up. eGFR,
estimated glomerular filtration
rate; ROC, receiver operating
characteristic.
130
In our study, a related donor is found in 34.6% of
patients. However, there was no effect of this relationship in
terms of improved renal function. Another point to consider
was donor’s age since several renal grafts had to be har-
vested from people above 50 years of age due to absence of
siblings in low birth rate countries. Guo et al [19] observed a
similarity in satisfactory graft function between older donor
and younger donor. This is contrary to a previous study
performed in cadaveric donors that showed the factors with
the greatest effect on DGF are donor’s age and cold
ischemic time [18]. A study conducted in the United
Kingdom also echoed this result, showing that donor
age > 60 years is associated with inferior survival of
grafts [20].
Our data showed that all our donors are living donors,
with most aged younger than 45 years (86.3%). They, in
turn, donated their kidney to an older recipient (age at or
older than 45 years; 60.7%). However, our statistical anal-
ysis showed that neither donor age nor recipient age
affected renal graft function at 6 months (P ¼ .62 and
P ¼ .67 for donor and recipient age, respectively) or at 12
months (P ¼ .39 and P ¼ .71, donor and recipient, respec-
tively). This is probably attributed to the fact that donors
who have passed the prerequirements to undergo proced-
ures are of adequate health. The mean age of donors and
recipients in our study was 30 and 48 years. We speculate
that unless the age is extreme (either very young or very
old), patient age in general causes a statistically insignificant
effect.
A preliminary study by Lepeytre et al hypothesized that
recipient age has the greatest effect on renal transplant
success [21]. With male donors, there is a significantly
higher risk for failure in female recipients. There was a
lower risk of failure among women aged > 45 years
compared with their male counterparts in cases of a
female donor, although the younger female age group
seems to have a higher risk for graft failure. It is
hypothesized that several factors affect this, including sex
hormones and differences in medication, body size, and
histocompatibility antigens between the different sexes. In
accordance with this study, sex mismatch was also said to
increase the risk of graft loss by Miller et al in their study
on donor-recipient sex association with failure in kidney
transplantation [22].
Ischemic time was another factor that increased the risk
of acute rejections and lowered survival of the graft. Even a
functioning graft will subsequently decrease in function af-
ter the first or second year. Seo et al showed that graft
survival at 3, 5, and 10 years post-transplantation in patients
with DGF were up to 18% lower than that of the non-DGF
group [23]. Poor warm and cold ischemia time both prove to
be harmful for long-term graft survival and contribute to
DGF. There is a 3-fold increase in graft failure in patients
with poor warm ischemic time that is above 45 minutes [16].
A study by Tirtayasa et al also showed a similar result; in
their study, DGF was higher in longer ischemic time, but in
multivariate analysis it shown no significant results [24].
BRAMONO, IRDAM, SITUMORANG ET AL
Meanwhile, a previous study has mentioned that long
cold ischemic time could be identifiable as DGF. In accor-
dance with these studies, our study showed that total warm
ischemic time is a promising factor affecting transplant
success, which is apparent at 12 months after transplant
(P ¼ .05). The presence of various comorbid conditions in
the donor kidney is a factor that contributes to a longer
ischemic time (particularly cold ischemic time); however,
current standards in organ transplant require further study
for this to be ruled out.
In relation to ischemic time is also the BMI of the
recipient. Hellegering et al in their study observed that
obese recipients will normally have a prolonged ischemic
time (> 40 minutes), especially in right-side kidney trans-
plants [16]. Most of our donors and recipients are normal
weight by the World Health Organization classification.
Interestingly, studies have shown that what matters is not
the BMI of the recipient per se, but the presence of mis-
matching donor kidney weight and recipient body weight. If
the ratio is low, normally this indicates that initial functional
nephron mass is reduced, resulting in a higher chance for
hyperfiltration; however, an increase in donor body weight
does not correspond linearly with nephron number (and
therefore the functional mass of the kidney). This is a
complex relationship of kidney allograft weight and recip-
ient weight ratio, influenced by glomerular volume, body
surface area, and other factors that contribute to the success
of the graft.
We also considered it of clinical importance to presurgi-
cally take multiple arteries into consideration. This is part of
anticipating several problems, such as poor perfusion
resulting in poor preservation of the donor kidney, longer
operation time, and segmental infarction due to thrombosis
of aberrant vessels [25]. There is also anatomic variation to
consider between the sides of the kidney. Right-sided kid-
neys have relatively shorter veins due to their position to-
ward the aorta. Both multiple arteries and shorter veins are
considered since they potentially complicate the technique
involved in removing the kidney in some cases, thereby
increasing ischemic time. Marcelino et al showed both right-
kidney and left-kidney donors had the same operative re-
sults and postoperative outcomes [26].
Zorgdrager et al revealed in their study that a higher risk
of complications and DGF occurred in a multiple renal
arteries graft, but the long-term outcomes for graft and
patient survival were similar between multiple and single
renal artery grafts [27]. Multiple arteries were found in 9.5%
of our donors. More than 4 out of 5 donor nephrectomies
were performed on the left side (82.9%). Salehipour et al
also revealed the same result [17].
We found no statistically significant results in terms of sex
influence in both the donor and recipient groups. There was
no superiority compared with cross-sex donors or recipients
from the same-sex group. Prior research on sex differences
in terms of renal survival showed conflicting results.
Serum creatinine was discovered early to be a means of
calculating the eGFR. However, many confounding factors
RENAL FUNCTION IN TRANSPLANT RECIPIENT
can affect serum creatinine, introducing its inaccuracy po-
tential as an eGFR estimator. Several studies have sug-
gested different calculation methods that estimate serum
creatinine while taking into account age, sex, race, and BMI.
Overall, the Chronic Kidney Disease Epidemiology
Collaboration (CKD-EPI) is felt to be superior in routine
clinical use, among other formulas such as Cockroft-Gault
or simplified MDRD [10]. Keddis et al added that creati-
nine and creatinine-cystatin Cebased eGFR most consis-
tently reflect the same risk factor as measured GFR [28]. A
study by Sabanayagam et al stated that the MDRD formula
has similar results with the CKD-EPI formula in Asian
populations [11].
Of all the aforementioned predictors, some have argued
that eGFR rate at 12 months is the best predictor for long-
term graft function. Although it was mentioned previously
that long-term survival should be measured by GFR at 5
years after transplant, it appears that 1-year GFR can fully
mediate this function to predict success. Given that the
donor organ quality is adequate and early or acute rejec-
tion can be hindered, GFR at 1-year post transplant is
thought to be a standard to evaluate success in the shorter
term [29]. Similarly, a study conducted on more than
150,000 patients in the United States also showed that
events occurring in the first year are of paramount
importance for long-term graft survival, as measured by
their creatinine and creatinine changes [30]. Indeed, our
observation showed that eGFR was an insignificant factor
for transplanted renal graft success (P ¼ .05), apparent at
12 months post-transplantation.
Overall, the limitations of this study are mostly due to it
being retrospective in design. There is a possibility of in-
formation bias, but the recipients and donors were
sampled consecutively, thereby lowering the risk of selec-
tion bias.
CONCLUSIONS
A successful kidney transplant is determined by multiple
factors that affect both short-term and long-term graft
survival. Our study showed that total warm ischemic
time was a promising factor that affects the success of
kidney transplant in our patients. Therefore, future
studies with longer periods of observation and larger
sample sizes should be done to confirm total warm
ischemic time as a predictor for renal function
posttransplantation.
ACKNOWLEDGMENTS
We thank University of Indonesia for providing support in both
facilities and funding during the whole process of this research.
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