Factors affecting mortality during the waiting time for kidney transplantation: A nationwide population-based cohort study using the Korean Network for Organ Sharing (KONOS) database
Factors affecting mortality during the waiting time for kidney transplantation: A nationwide population-based cohort study using the Korean Network for Organ Sharing (KONOS) database
Sunhwa Lee 0 3
Kyung Don YooID 1 3
Jung Nam An 2 3
Yun Kyu Oh 2 3
Chun Soo Lim 2 3
Yon Su Kim 0 3
Jung Pyo LeeID 2 3
0 Department of Internal Medicine, Seoul National University Hospital , Seoul , Republic of Korea
1 Department of Internal Medicine, Dongguk University College of Medicine , Gyeongju , Republic of Korea
2 Department of Internal Medicine, Seoul National University Boramae Medical Center , Seoul , Republic of Korea, 4 Department of Critical Care Medicine, Seoul National University Boramae Medical Center , Seoul , Republic of Korea, 5 Department of Internal Medicine, Seoul National University College of Medicine , Seoul , Republic of Korea
3 Editor: Ping-Hsun Wu, Kaohsiung Medical University Hospital , TAIWAN
Data Availability Statement: The repository data
for public release is not available because of the
personally identifiable information. The data set
includes information such as name, home address,
social security number, clinic centers in which they
routinely attend, insurance condition, etc.
Concerning privacy risks, therefore, the data is
managed by authorized executive supervisor. If one
researcher asks to access data, the person in
charge releases data with blind identification for the
discrete requirements. Contact information for a
Of the 24,296 wait-listed subjects on dialysis, 5,255 patients received kidney transplants
from deceased donors, with a median waiting time of 4.5 years. Longer waiting times had
distinct deleterious effects on overall survival after transplantation. While waiting for a
transplant, patients with diabetes were more likely to die before transplantation (HR 1.515, 95%
CI 1.388?1.653, p<0.001). Age was another significant risk factor for mortality. Only 56% of
people aged 65 years survived after 10 years of waiting, whereas 86% of people aged 35
years survived after 10 years. Moreover, women on the waiting list were more likely to live
longer than men on the list.
data access committee is listed as follows: Center:
Center for Korean Network for Organ Sharing,
Division: Organ donation support, Tel:
82-02-26283619, Fax: 82-02-2628-3629, E-mail:
. Official internet site of
jsp) also provide rough statistics of kidney organ
donors and candidates.
Funding: This research received no specific grant
from any funding agency in the public, commercial,
or not-for-profit sectors.
More attention should be focused on patients with a higher risk of mortality while waiting for
a deceased donor kidney transplant, such as patients with diabetes, those of advanced age,
and those who are male.
The number of patients with end-stage renal disease (ESRD) is increasing rapidly at a rate of
5?7% per year [
]. In South Korea, the total number of patients receiving renal replacement
therapy (RRT) has increased from 746 to 1,464 patients per million population during the past
10 years (from 2006 to 2016), whereas kidney transplantation cases have increased from 550 to
1,112 patients per million population. Although kidney transplantation is the treatment of
choice due to its superior outcomes in terms of survival rate [
], quality of life and cost
], the discrepancy between the supply and demand of kidneys continues to grow. As of
December 2017, 19,807 patients were on the Korean Network for Organ Sharing (KONOS)
waiting list for kidney transplantation. During the last decade in Korea, a 22.4% annual
increase in the kidney transplantation waiting list was recorded. Consequently, the waiting
time for kidney transplantation is an issue of growing importance.
In South Korea, if a patient with ESRD who should undergo renal replacement therapy
prefers to undergo deceased donor kidney transplantation, each authorized clinic center evaluates
the patient for recent malignancy, mental illness, drug addiction, severe liver disease, severe
lung disease, active and untreated current opportunistic infection, or active ischemic heart
]. If there are no contraindications for registration, they can be registered to the
government-affiliated transplant waiting list (K-net, organ donation information system) managed
by the Korea Centers for Disease Control and Prevention (KCDC) KONOS. After enrollment
in the waiting list, the patients? priority score is provided according to their waiting time, age
(higher score for the those aged 18 years), leukocyte antigen and ABO blood type match,
history of kidney transplantation, experience of living donation, and any prior kidney transplant
refusal without evident medical reasons (S1 Table). Recipients who have identical ABO blood
type or compatible blood type for transfusion obtain additional scores. Patients with higher
scores preferentially obtain a chance for transplantation. In contrast, there are no detailed
criteria for determining candidates who receive expanded criteria donor kidneys, which satisfy
one or more of the following conditions: age 60 years, GFR 60 mL/min/1.73m2 or serum
creatinine level 3.0 mg/dL, hypotensive episode 3, proteinuria (++) 2, and non-heart
beating donor [
]. The waiting time of candidates is determined according to the above
allocation system in South Korea.
Longer waiting times on dialysis can negatively affect overall mortality and graft outcomes
]. Accordingly, preemptive transplantation is preferred in this context . However,
although living donor kidney transplantation is preferred over deceased donor kidney
transplantation due to superior graft and survival outcomes [
], deceased donor kidney transplant
recipients with an ESRD time of less than 6 months showed equivalent survival rates compared
to those of living donor kidney transplant recipients who spent 2 years on the waiting list [
In other words, minimizing the waiting time for kidney transplantation is critical. Achieving
this goal, however, is challenging due to a shortage of donor organs. If kidney transplant
recipient candidates must wait for donor organs, then understanding the risk factors for adverse
events and controlling them during that waiting period are essential.
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Patients who are on the waiting list for deceased donor kidney transplantation are generally
younger and healthier than patients who are not on the list [
]. Therefore, the survival of
potential transplant recipient patients who remain on dialysis is better than that of patients on
dialysis overall. In the 2016 United States Renal Data System (USRDS) report, the most recent
2014 mortality record showed that patients on dialysis overall showed an annual mortality rate
of 135.6 per 1,000 dialysis patient years, whereas patients who remain on dialysis while on the
kidney transplant waiting list had a mortality rate of 53.7 per 1,000 dialysis patient years [
Because patients on the waiting list have different characteristics than those of patients on
dialysis overall, understanding their unique characteristics and risk factors is essential. In this
study, based on a complete enumeration survey in Korea, we investigated risk factors for
mortality by waiting time. Moreover, the transplant probability according to various clinical factors
was also explored.
Materials and methods
The KONOS is a government-affiliated organization under the Centers for Disease Control
(CDC) that manages deceased donor organ transplantation exclusively in South Korea. The
study sample consisted of patients with ESRD who were enrolled on waiting lists for deceased
or living donor kidney transplantation in 27 medical centers around the country since January
2000. Among these incident cohort patients, we included adult patients older than 18 years of
age who were active on the waiting list or had already undergone deceased donor kidney
transplantation. All patients were monitored from the time of registration until death or until the
study end date of January 2015. Patients who became medically unsuitable for transplantation
or refused a transplant remained on the waiting list until death. Patient demise was obtained
from national statistics collected from information recorded at death registration.
At the time of registration, demographic and clinical data were entered into the KONOS
database, including age, gender, height, body weight, start date of dialysis, cause of ESRD,
ABO and Rh blood type, human leukocyte antigen (HLA) type (A, B, or DR), panel reactive
antibody (PRA) positivity, and any prior kidney transplant experience.
The original data files from KONOS database are not available for public use because of the
personally identifiable information. Concerning privacy risks, the data is managed only by
authorized executive supervisor. The authors could perform this study after research
agreement from KONOS. The raw data was provided after de-identification so that informed
consent from each patients were not required. All analysis performance has never included any
identifying process of patients? personal information.
Normally distributed continuous variables were expressed as the mean ? standard deviation
(SD) and were compared using Student?s t-test. For non-normally distributed continuous
variables, the median and inter-quartile range were used to express the center of the distribution,
and Mann-Whitney tests were applied to compare two groups. Chi-square tests were
performed to compare percentages.
For risk analysis during the waiting time, the primary outcome of our study was patient
death. Comparisons between the survival curves of wait-listed patients and transplant
recipients were performed using the log rank test. Moreover, we adopted time-dependent Cox
regression analysis to eliminate a time-to-treatment bias when analyzing the overall mortality
risk of deceased donor kidney transplant recipients according to waiting time. No patients
were lost to follow-up for the primary outcome of the study, resulting in no censored cases. To
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analyze the risk factors during the waiting time for kidney transplant, a multivariate Cox
proportional hazards model was used. The Cox proportional hazard models were adjusted for age,
gender, blood type, causes of ESRD, and previous kidney transplant experience.
The probability of kidney transplantation among wait-listed patients was also analyzed.
Multivariate Cox regression was adopted to examine the effects of various clinical factors on
transplant probability. The primary outcome was the transplant rate, and time was censored at
the transplantation date.
The statistical analysis was performed using STATA version 11.0 (StataCorp LP, College
Station, TX, USA) and SPSS 18 (SPSS, Chicago, IL), and statistical significance was defined as
a p value less than 0.05.
Of the 24,296 wait-listed dialysis subjects, 5,255 patients underwent deceased donor kidney
transplantation, and 19,041 patients remained on dialysis. Table 1 shows the baseline
characteristics of the enrolled patients according to transplant status.
Regarding patient demographics, kidney transplant recipients were younger than the
patients who remained on dialysis (46.36 ? 10.84 vs 51.97 ? 11.32 years, p<0.001). The
probability of undergoing deceased donor kidney transplantation after a 10-year wait differed
according to age quartile: 1st quartile (35.2 ? 5.7 years) 75.2%, 2nd quartile (47.2 ? 2.6 years)
56.1%, 3rd quartile (54.9 ? 2.0 years) 43.9%, and 4th quartile (64.6 ? 4.8 years) 30.9%. On the
other hand, the gender ratio did not show a significant difference between the groups.
Total (N = 24,296)
48.46 ? 0.23
Recipients (n = 5,255)
46.36 ? 10.84
Dialysis (n = 19,041)
51.97 ? 11.32
Abbreviations: ESRD, end-stage renal disease; GN, glomerulonephritis; PKD, polycystic kidney disease; PRA, panel reactive antibody; HLA, human leukocyte antigen;
BMI, body mass index.
The causes of ESRD in the two groups were as follows: chronic glomerulonephritis (GN)
(18.7%), diabetes (15.2%), and hypertension (14.9%) for the transplant recipients, and diabetes
(21.4%), chronic GN (18.7%), and hypertension (10.1%) for the remaining patients.
The proportions of ABO blood types in the two groups were also different: type A (35.1%),
type B (27.7%), type O (22.5%), and type AB (14.6%) in the transplant recipients, and type A
(32.8%), type O (29.8%), type B (27.2%), and type AB (10.1%) in the remaining patients.
Although 28% of the patients on the overall waiting list had blood type O, these patients
accounted only for 22.5% of the deceased donor kidney recipients. Compared with patients
with blood type O, the probability of undergoing deceased donor kidney transplantation was
1.49-times higher for patients with blood type A, 1.41-times higher for patients with blood
type B, and 2.08-times higher for patients with blood type AB. In other words, patients with
blood type O must wait much longer to receive deceased donor kidney transplantation
compared to patients with other blood types.
PRA positivity and body mass index (BMI) were available only in kidney transplant
recipients. Only approximately a quarter (25.3%) of the recipients had information for PRA
Overall survival in patients with deceased donor kidney transplants and in
those who remained on dialysis
The median waiting time for kidney transplantation from a deceased donor was 4.5 ? 2.7
years. Ten-year overall survival was 81.3% in deceased donor kidney transplant recipients and
68.1% in patients who remained on dialysis (log rank p<0.001) (Fig 1). When we evaluated the
impact of waiting time for deceased donor kidney transplantation on overall mortality, a
longer waiting time increased the overall mortality risk. Time-dependent Cox regression with
waiting time showed that subjects in the 4th quartile of waiting time (8.13 ? 1.53 years)
presented a hazard ratio (HR) of 2.934 with a 95% confidence interval (CI) ranging from 1.808 to
4.763, with a p value lower than 0.001 in a comparison to subjects in the 1st quartile (1.22 ?
0.71 years) (Table 2).
After adjusting for recipient age, gender, waiting time, blood type, prior kidney transplant
status, and cause of ESRD, we determined that older age and longer waiting time adversely
influenced mortality outcomes.
Fig 1. Kaplan-Meier plots comparing overall survival in patients with deceased donor kidney transplants with
those who remained dialysis. The survival curves were compared using the log rank test (p<0.001).
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Risk factors during waiting time
During waiting time, various demographic and clinical factors were associated with increased
mortality. Table 3 shows the results of univariate and multivariate Cox regression analyses of
the overall mortality risk during waiting time. The statistically significant variables were old
age, male gender, Rh-negative blood type, and diabetic nephropathy as the cause of ESRD.
Abbreviations: Q1, 1st quartile; Q2, 2nd quartile; Q3, 3rd quartile; Q4, 4th quartile; ESRD, end-stage renal disease; DM, diabetic mellitus; GN, glomerulonephritis; PKD,
polycystic kidney disease.
After adjusting for these variables, we found that patients with diabetes were more likely to die
before transplantation (HR 1.65, 95% CI 1.51?1.80, p<0.001). Moreover, the 4th quartile
group of a mean age of 64.5 years had a 3.5-times higher mortality ratio than that of the 1st
quartile group of age 35.2 years; in other words, aging was another significant risk factor for
mortality during waiting time. Female gender groups were less likely to die during waiting
time than male groups. ABO Blood type and prior kidney transplant experience did not have a
significant impact on overall mortality during waiting time.
Probability of undergoing transplantation
We performed multivariate regression analysis on the success rate of receiving a kidney
transplant according to various demographic variables to analyze which patients received deceased
donor kidney allografts earlier (Table 4). Our analysis showed that patients who were of
advanced age, had diabetes, had blood type O, or had undergone previous transplantation
tended to receive deceased donor kidneys later (Fig 2).
In the present study, we performed risk factor analysis based on waiting time for 24,296
individuals with ESRD on the waiting list for renal transplantation. Longer waiting periods had an
obvious negative effect on overall mortality after transplantation. During that time, patients
who were male, of advanced age, or had diabetes were vulnerable to death. We also found that
patients who were of advanced age, had diabetes, had blood type O, or had prior kidney
transplant experience received donor kidneys later than others on the list.
Younger and healthier patients tend to receive kidney transplantation earlier, and longer
waiting times should therefore be associated with higher mortality rates. However, in our
analysis, we adjusted for demographic and clinical factors, such as age and the cause of ESRD. As a
result, longer waiting time was identified as an independent risk factor for post-transplant
mortality, which has also been shown in previous studies [
This study mainly showed which risk factors may affect mortality or kidney transplantation
rates during waiting times. The prevalence of mortality is known to increase significantly with
age or diabetes in patients with ESRD [
]. Although patients with diabetes account for
48.4% of new patients with ESRD in Korea [
], the proportion of these patients on the waiting
list is 20.1%. Because of the high morbidity of these patients with diabetes, they may have a
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reduced likelihood of being enrolled on the waiting list. Although relatively healthy patients
with diabetes are on the registry, they show a higher mortality rate during the waiting time
than do patients with any other ESRD causes. The Korean Society of Nephrology (KSN)
registry data also showed that the 5-year survival rate of patients with diabetes and ESRD was 53%,
whereas other patients with ESRD and chronic glomerulonephritis or hypertensive
nephrosclerosis had survival rates of 78% and 69.8%, respectively [
]. On our KONOS waiting list,
the 5-year survival rate during the waiting time was 77% for patients with diabetes, 91% for
patients with hypertensive nephrosclerosis, and 93% for patients with glomerulonephritis.
In general, women have a survival advantage over men in the general population. Even in
patients with chronic kidney disease, women tend to progress to ESRD at a slower rate than
men do, regardless of disease etiology [
]. However, in the dialysis population, women lost
this benefit [
] and showed survival rates similar to those in men. Even if kidney
transplantation is performed, this survival benefit cannot be recovered in women [
young women with ESRD (under age 35 years) tend to have higher overall or
non-cardiovascular mortality rates than do men on dialysis. This pattern was not different in the Korean
dialysis population [
]. However, although no gender advantage was observed for the overall
mortality rate after deceased donor kidney transplantation in our study, men were 1.25-times
more likely to die than women are during waiting time. This result may have been affected by
influences other than clinical factors. Some studies have shown that the statistical significance
of mortality rates during waiting times may be influenced by insurance status, income, family
support, and socioeconomic status [
]. Unfortunately, this personal information was not
provided by the KONOS to protect personal identification information. Although the reason
why men are more likely to die during waiting time than are women is unclear (unlike the
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Fig 2. Cumulative probability to undergo deceased donor kidney transplantation on the waiting list according to age quartile (A), gender (B), ABO blood type
(C), Rh blood type (D), cause of ESRD (E), and prior kidney transplant experience (F). Abbreviations: Q1, first quartile, age of 18 to 42; Q2, second quartile, age of 43
to 51; Q3, third quartile, age of 52 to 58; Q4, fourth quartile, age of 59 to 96; PKD, polycystic kidney disease; HTN, hypertension; CGN, chronic glomerulonephritis; DM,
survival benefit of women in the general dialysis population), we propose that socioeconomic
conditions may contribute to this difference.
In our study, we determined that patients with blood type O or prior kidney transplant
experience were disadvantaged in terms of receiving a deceased donor kidney in a timely
manner. Patients with advanced age or diabetes may acquire more comorbidities as waiting time
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progresses, so a reduced probability of undergoing transplantation over time is expected.
However, patients with blood type O suffer from a disadvantage in the prioritization of
receiving deceased donor kidney allografts due to biological differences. ABO-compatible kidney
transplantation rules allocate blood type O kidneys to non-blood type O recipients;
consequently, patients with blood type O on dialysis who can only receive kidneys from the same
blood type have a lesser likelihood of receiving these organs. According to the annual statistical
report by the KONOS, 4~7% of deceased donor kidney transplantations were performed on
non-identical?but ABO-compatible?blood types in the last 5 years [
]. As a result, wait-listed
patients with blood type O wait longer to receive deceased donor kidneys than patients with
other blood types, leading to worse outcomes. A similar blood type O problem has been
described in the Eurotransplant Kidney Allocation System, and some studies have reported
that the current allocation system should be revised [
]. On the other hand, in the United
States, the Organ Procurement and Transplantation Network already accounts for this concept
in its allocation system. A restriction mandates that kidneys from donors with blood type B or
O are allocated to recipients with identical blood types, except in zero-HLA mismatch category
]. In the United States, blood type B candidates have the longest waiting time (6
years in 2014) compared to those with other blood types (type A, 3 years; type AB, 2 years; type
O, 5 years) , while in South Korea, blood type O candidates have the longest waiting time
(type O, 5.2 years; type A, 4.4 years; type B 4.6 years; type AB, 3.4 years; in 2014). Because the
United States is under special condition wherein a majority of deceased kidney donors are
white, of whom only 9% of them have blood type B, there exist disparities for blood type B
candidates in access to transplantation [
]. Therefore, to protect blood group B candidates, of
whom a majority are ethnic minorities, the national kidney allocation system assigns A2/A2B
kidney to B recipients preferentially. Although it comprises a minor portion, A2/A2B !B
deceased donor kidney transplantations increased from 14 (1.95%) to 53 (8.93%) among blood
group B deceased donor kidney transplantation [
]. In South Korea, the fairness of our organ
allocation system warrants re-evaluation to avoid reverse discrimination based on biological
In addition, not only patients with blood type O or history of kidney transplantation were
less likely to undergo deceased donor kidney transplant in a timely manner but also those with
causes of ESRD other than DM tended to undergo deceased kidney at a later time. Table 4
shows that candidates with hypertensive and diabetic ESRD are ranked first and second for
transplantation probability during waiting time, whereas chronic glomerulonephritis or other
causes were ranked next, although the Korean kidney allocation system does not include
causes of ESRD as rating criteria. If we look into the proportion of ABO blood type in each
cause of ESRD, diabetic patients have lesser portion of blood type O population compared to
non-diabetic ESRD patients (S2 Table). Recent research reported that people with blood type
O have a lower risk of developing type 2 diabetes mellitus [
]. Because, blood type O
candidates tend to wait longer to receive a deceased kidney, any group composed of a larger
proportion of blood type O candidates will likely to wait longer. Therefore, this is the possible reason
patients with causes of ESRD other than diabetes are less likely to undergo transplantation.
In our study, the analysis was limited in at least three respects. First, missing or unknown
data represented 36% of the data on ESRD causes. Another limitation was knowledge
regarding the origin of kidney disease in all patients with ESRD because kidney biopsy was not
performed in all patients to determine the cause of ESRD. Nevertheless, the fact that more than
one-third of the data were unknown or missing causes an interpretation bias. Second,
socioeconomic status was not provided for the wait-listed candidates. In Korea, at least 10 thousand
dollars per patient is required for kidney transplantation surgery, even if these patients benefit
from national health services [
]. Therefore, barriers to entry on the transplant waiting list
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exist for economically disadvantaged individuals. Moreover, family support or insurance status
may affect mortality during waiting time or may affect transplantation rates; however, such
parameters were not included in this analysis. Third, comorbidities such as diabetes and
ischemic heart disease were not adjusted for in survival and transplant probability analyses.
Although these are highly influential factors for the outcome, we do not have this information
from the KONOS.
In conclusion, this study indicated the risk factors of mortality during waiting time for
deceased donor kidney transplantation and the characteristics of patients who received
deceased donor kidney transplantation after longer waiting times. Considering the deleterious
effect of longer waiting time on mortality, identifying vulnerable patients during the waiting
time and providing more intensive care for these patients are important.
S1 File. Extracted raw data of KONOS database.
S1 Table. Deceased donor kidney allocation scoring system in South Korea.
S2 Table. The proportion of ABO blood type of diabetic and non-diabetic ESRD patients
in the waiting list in our study group.
We acknowledge Korean Organ Network for Organ Sharing (KONOS) for providing database
for this analysis. This data was not published elsewhere except a poster presentation at the
annual meeting of American Society of Nephrology (ASN) Kidney Week 2015.
Conceptualization: Jung Pyo Lee.
Data curation: Sunhwa Lee, Kyung Don Yoo, Jung Nam An, Jung Pyo Lee.
Formal analysis: Sunhwa Lee, Kyung Don Yoo, Jung Nam An.
Investigation: Sunhwa Lee, Jung Nam An, Yun Kyu Oh, Chun Soo Lim, Yon Su Kim, Jung
Methodology: Yun Kyu Oh, Chun Soo Lim.
Project administration: Jung Pyo Lee.
Resources: Kyung Don Yoo, Jung Nam An.
Software: Kyung Don Yoo.
Supervision: Yun Kyu Oh, Chun Soo Lim, Yon Su Kim, Jung Pyo Lee.
Validation: Yun Kyu Oh, Chun Soo Lim, Yon Su Kim.
Visualization: Sunhwa Lee.
Writing ? original draft: Sunhwa Lee.
Writing ? review & editing: Sunhwa Lee, Chun Soo Lim, Yon Su Kim, Jung Pyo Lee.
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