Metabolic Syndrome and Chronic Kidney Disease in an Adult Korean Population: Results from the Korean National Health Screening
et al. (2014) Metabolic Syndrome and Chronic Kidney Disease in an Adult Korean Population: Results from the
Korean National Health Screening. PLoS ONE 9(5): e93795. doi:10.1371/journal.pone.0093795
Metabolic Syndrome and Chronic Kidney Disease in an Adult Korean Population: Results from the Korean National Health Screening
Yong Un Kang 0
Ha Yeon Kim 0
Joon Seok Choi 0
Chang Seong Kim 0
Eun Hui Bae 0
Seong Kwon Ma 0
Soo Wan Kim 0
Giovanni Targher, University of Verona, Ospedale Civile Maggiore, Italy
0 Department of Internal Medicine, Chonnam National University Medical School , Gwangju , Korea
Background: This study was aimed to examine the prevalence of metabolic syndrome (MS) and chronic kidney disease (CKD), and the association between MS and its components with CKD in Korea. Methods: We excluded diabetes to appreciate the real impact of MS and performed a cross-sectional study using the general health screening data of 10,253,085 (48.86613.83 years, men 56.18%) participants (age, $20 years) from the Korean National Health Screening 2011. CKD was defined as dipstick proteinuria $1 or an estimated glomerular filtration rate 2 (eGFR) ,60 ml/min/1.73 m . Results: The prevalence of CKD was 6.15% (men, 5.37%; women, 7.15%). Further, 22.25% study population had MS (abdominal obesity, 27.98%; hypertriglyceridemia, 30.09%; low high-density cholesterol levels, 19.74%; high blood pressure, 43.45%; and high fasting glucose levels, 30.44%). Multivariate-adjusted analysis indicated that proteinuria risk increased in participants with MS (odds ratio [OR] 1.884, 95% confidence interval [CI] 1.867-1.902, P,0.001). The presence of MS was associated with eGFR,60 mL/min/1.73 m2 (OR 1.364, 95% CI 1.355-1.373, P,0.001). MS individual components were also associated with an increased CKD risk. The strength of association between MS and the development of CKD increase as the number of components increased from 1 to 5. In sub-analysis by men and women, MS and its each components were a significant determinant for CKD. Conclusions: MS and its individual components can predict the risk of prevalent CKD for men and women.
Funding: This research was supported by a fund under the Korea Centers for Disease Control and Prevention (2012-E33024-00), by the National Research
Foundation of Korea (NRF) grant (MRC for Gene Regulation, 2011-0030132) funded by the Korea government (MSIP), and by Basic Science Research Program
through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and future Planning (2013R1A2A2A01067611). The funders had
no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
Metabolic syndrome (MS) includes various metabolic
abnormalities that have been associated with cardiovascular disease,
stroke, and all-cause mortality in the general population . The
components of MS include central obesity, elevated blood
pressure, and impaired fasting glucose and high triglyceride (TG)
and low high-density lipoprotein (HDL) cholesterol levels, and
these components are present in approximately 20% adults in
USA . In Korea, recent changes in lifestyle and diet have
resulted in an increased prevalence of MS, becoming an important
public health concern. The prevalence of MS has been reported to
be about 14.2% in men and 17.7% in women in the general
population . Another study suggested that the prevalence of MS
has increased to approximately 19.0% .
The burden of chronic kidney disease (CKD) has also been
increasing worldwide over the last decade and is expected to
increase further . The increased incidence of CKD in recent
years paralleled with an increasing prevalence of MS [6,7].
Previous observational studies have reported an independent
association between MS and microalbuminuria or proteinuria and
CKD [8,9]. In a large cohort survey, both MS and
microalbuminuria had strong adverse effects on the estimated glomerular
filtration rate (eGFR), and this relationship was even more
pronounced in the presence of both factors . However, a
few studies have shown statistically insignificant association
between MS and low eGFR after adjustment for albuminuria .
Additionally, the reported studies used varying definitions for
MS and studied different populations. Thus, the data on MS or its
relationship with CKD in large population-based studies are
limited. Therefore, we aimed to assess the prevalence of MS and
CKD, and the association between MS and its components with
CKD in an adult Korean population.
Materials and Methods Study Population
Korean National Health Screening is an annual health
examination to improve the health of people and reduce
healthcare costs by preventing cardiocerebrovascular diseases affected by
lifestyle habits, such as hypertension, diabetes, dyslipidemia, and
by detecting five major forms of cancer at an early stage. General
Health Screening was the first-step screening test for an early
detection. We performed a cross-sectional study using the general
health screening data of 11,828,803 participants (age$20 years)
from the 2011 Korean National Health Screening database. Of
these, 10,549,230 subjects with information on renal function,
such as serum creatinine and urine analysis, and all parameters
related to MS were included in this analysis. 296,145 subjects with
diabetes were excluded to appreciate the real impact of MS.
Finally, 10,253,085 subjects were recruited in our study to assess
the prevalence and association between MS and CKD.
This study was approved by the institutional review board of
Chonnam National University Hospital, Gwangju, Republic of
Korea. This institutional review board waived the need for consent
given the retrospective design of the project. The study was
performed in accordance with the Helsinki Declaration of 1975, as
revised in 2000.
Health examination included data for anthropometric
measurement, blood pressure, and blood chemistry tests. Information
on sex, age, and other pertinent medical data were obtained.
Anthropometric measurements, including height, weight, and
waist circumference, were determined, and the body mass index
(BMI) was calculated by dividing the weight in kilograms by height
in meters squared. Trained nurses measured blood pressure at the
health screening facilities using a standard protocol. Blood samples
were collected in the morning after an overnight fast of at least
8 h. Plasma glucose levels were measured using a hexokinase
enzyme reference method. At the health screening facilities, serum
HDL cholesterol and TG levels were measured enzymatically by
using a commercially available reagent mixture, and serum
creatinine was measured using the modified Jaffe kinetic reaction.
MS was defined using the current criteria in the National
Cholesterol Education Program Adult Treatment Panel III (ATP
III) (NCEP) guidelines with a modification for waist
circumference. Specifically, elevated blood pressure was defined as systolic
or diastolic blood pressure of 130/85 mmHg or higher and the
current use of antihypertensive medication. Elevated blood glucose
level was defined as a fasting blood glucose level of $100 mg/dL
or use of glucose level-lowering medicine. Low HDL cholesterol
level was defined as that ,40 mg/dL in men and ,50 mg/dL in
women. Hypertriglyceridemia was defined as a serum TG level of
$150 mg/dL. Abdominal obesity was defined as a waist
circumference .90 cm in men and .80 cm in women according
to the Asia-Pacific criteria. MS was defined as the presence of
three or more of these five components .
Diabetes mellitus (DM) was defined as a self-reported history of
a previous diagnosis of diabetes or a fasting plasma glucose level of
$126 mg/dL. Hypertension (HT) was defined as self-reported
history of a previous diagnosis of HT or systolic blood pressure $
140 mmHg or diastolic blood pressure $90 mmHg. eGFR was
calculated using The Chronic Kidney Disease Epidemiology
Collaboration (CKD-EPI) equation . The definition of
proteinuria was based on a dipstick urinalysis score of 1+ or
more. CKD was defined as an eGFR,60 mL/min/1.73 m2 or
dipstick proteinuria ($1+) .
The prevalence of CKD, MS, and its individual components
(abdominal obesity, high blood pressure, and high TG, low HDL
cholesterol, and high fasting glucose levels) was determined for the
overall population. Data were presented as the mean 6 SD for
continuous variables and as proportions for categorical variables.
The characteristics of the subjects were compared using the
chisquared test for categorical variables. Students t-test was used for
continuous variables. Multivariate logistic regression was used to
estimate odds ratio (OR), and 95% confidence interval (CI) was
used for determining the relationship between MS and proteinuria
or eGFR,60 mL/min/1.73 m2. Covariates considered as
potential confounders (age and sex) were included in multivariable
models. Model 1 was unadjusted, model 2 included age and sex.
For the eGFR analysis, model 3 included age, sex, and
proteinuria. The associations between MS components and
CKD were analysed using multivariate logistic regression models
after adjustments for age and sex. Statistical analysis was
performed with the SAS (Version 8.2, SAS Institute Inc., Cary,
NC, USA). A P-value of ,0.05 was considered statistically
We studied 10,253,085 (56.18% men) participants (mean age,
48.86613.83 years). Women had significantly older age, higher
proportion of hypertension, total cholesterol levels, low-density
lipoprotein cholesterol levels, HDL cholesterol levels, and
proportion of eGFR,60 mL/min/1.73 m2 but lower BMI, waist
circumference, TG levels, systolic blood pressure, diastolic blood
pressure, fasting glucose levels, eGFR, and serum creatinine levels
than men. However, proportion of proteinuria was not different
between men and women (Table 1).
Prevalence of MS and CKD
The overall prevalence of CKD was 6.15% (men, 5.37%;
women, 7.15%). The prevalence of CKD according to the stage
was 0.81% in stage 1, 0.86% in stage 2, 3.52% in stage 3, and
0.96% in stage 4 or 5 (Table 2). We identified 2,281,675 (22.25%)
subjects who met the current ATP III criteria. Among all subjects,
27.98% had abdominal obesity, 30.09% had hypertriglyceridemia,
19.74% had low HDL cholesterol levels, 43.45% had high blood
pressure, and 30.44% had high fasting glucose levels. Women had
significantly higher proportion of abdominal obesity and low HDL
cholesterol but lower that of hypertriglyceridemia, high blood
pressure, and high fasting glucose than men (Table 1).
Subjects with MS had a higher prevalence of CKD than those
without MS (10.48% vs. 4.91%, P,0.001). 37.93% of the
participants with total CKD (n = 239,137) had MS (40.04% for
abdominal obesity; 34.46% for hypertriglyceridemia; 27.1% for
low HDL cholesterol; 62.74% for high blood pressure; and
43.61% for high fasting glucose). The prevalence of MS increased
with an increase in CKD stage. On the other hand, that of MS in
CKD stage 4 or 5 was the lowest compared to those with other
CKD stages. High blood pressure was the most common MS
component in each CKD stage (Figure 1).
Association between MS and CKD
In multivariate logistic regression models, the participants with
MS had a 1.884-fold increased OR (95% CI 1.8671.902, P,
Number of subjects
Body mass index (kg/m2)
Waist circumference (cm)
LDL cholesterol (mg/dL)
HDL cholesterol (mg/dL)
Systolic blood pressure (mmHg)
Diastolic blood pressure (mmHg)
Fasting glucose (mg/dL)
eGFR (mL/min/1.73 m2)
Serum creatinine (mg/dL)
eGFR,60 mL/min/1.73 m2 (%)
Chronic kidney disease (%)
Metabolic syndrome (%)
Individual component (%)
Low HDL cholesterol
High blood pressure
High fasting glucose
Abbreviations: TC, total cholesterol; LDL, low-density lipoprotein; HDL, high-density lipoprotein; eGFR, estimated glomerular filtration rate.
0.001) for proteinuria compared with those without MS. In
addition, the presence of MS was a significant determinant of
eGFR,60 mL/min/1.73 m2 (OR 1.364, 95% CI 1.3551.373,
P,0.001) and CKD (OR 1.526, 95% CI 1.5181.535, P,0.001)
compared with those without MS. In sub-analysis by men and
women, the presence of MS was also a significant determinant for
proteinuria, eGFR,60 mL/min/1.73 m2, and CKD compared
with those without MS (Table 3).
Association between MS Components and their Risk for
Development of CKD
In models adjusted for age and sex, we further examined the
associations of individual components of MS and the risk of CKD
by dividing each components of MS, in quartiles and making the
groups accordingly. Increasing component levels of MS showed a
positive association with the development of CKD compared with
the lowest quartile for men and women, respectively. On the other
hand, decreasing HDL cholesterol levels was linked clearly to
CKD compared with the lowest quartile for men and women,
respectively. The OR for CKD for high fasting glucose as an MS
component was higher than that for other MS components
(Table 4). The prevalence of markers of CKD was higher with
increasing number of MS components (Figure 2). The participants
with 15 component of MS had an increased OR for CKD: 1.062
(95% CI 1.0531.071), 1.281 (95% CI 1.2701.292), 1.575 (95%
CI 1.5611.590), 1.942 (95% CI 1.9211.962), and 2.367 (95% CI
2.3292.406) compared with those with no MS components (P,
0.001). In sub-analysis for men and women, the strength of
association between MS and the development of CKD also
appeared to increase as the number of components increased from
1 to 5 (Table 4).
The results of our study identified a strong, positive relationship
between MS and the prevalence of CKD. A rise in the incidence
of CKD in recent years has been associated with an increasing
prevalence of MS [6,7]. The prevalence of MS is about 24.7% of
adults in USA . A recent study demonstrated that the
prevalence of MS has increased to approximately 19.0% in Korea
. Although we excluded subjects with diabetes to appreciate the
real impact of MS, the present study reported an even higher
prevalence of MS (22.25%), reflecting a rapidly increasing
prevalence in Korea. The identification of MS is important in
patients with a high risk of developing end-stage renal disease
Chen et al.  demonstrated a significant correlation between
the number of MS traits and both albuminuria and eGFR,
60 mL/min/1.73 m2. In a prospective cohort survey, Luk et al.
 reported that the presence of MS independently predicted the
development of CKD in subjects with type 2 diabetes. According
to the National Health and Nutrition Examination survey, MS is
independently associated with CKD in the general population and
in non-diabetic adults [4,15]. Palaniappan et al.  showed a
higher risk for microalbuminuria in men and women with MS.
These data support the importance of MS in the development of
CKD. In a recent meta-analysis, although the results for
proteinuria outcomes were debated because of the small number
of prospective cohort studies, MS and its components were
associated with the development of eGFR,60 mL/min/1.73 m2
and microalbuminuria or overt proteinuria . All of these
studies confirmed a relationship between MS and CKD. Also, our
study results showed a strong relationship between MS and CKD
in non-diabetic adult Korean population. In sub-analysis by men
and women, MS was a significant determinant for CKD. These
findings have important clinical and public health implications
because the prevalence of the MS is rapidly increasing in Korea.
Our findings revealed each component of MS was an
independent predictor of CKD. We analysed individual
components to explore their differential effect in the presence of MS, and
thus, the risk estimates were interpreted in the context of MS. In
addition, the number of MS components and the risk for CKD
showed a graded association. Moreover, the prevalence of markers
of CKD increased with an increasing number of MS components.
Therefore, therapeutic strategies that targeted individual MS
components seem highly reasonable for preventing CKD.
Obesity is a significant risk factor for CKD. Visceral obesity is
highly correlated with insulin resistance, and indices of visceral
obesity may be more sensitive predictors of kidney disease than
BMI . Adipose tissue is a significant source of inflammatory
and immunomodulatory factors; the interaction between
adipocytes and macrophages may contribute to insulin resistance and
many of the features that characterise MS . Obesity occurs
probably via the mechanisms associated with renal hyperfiltration
and hyperperfusion as focal glomerulosclerosis and other
histological changes have been observed in kidneys of obese patients
[22,23]. Previous studies reporting obesity as a significant risk
factor for eGFR,60 ml/min/1.73 m2 used waist circumference
criteria (a better measure of central adiposity) rather than BMI
[24,25]. Our study results indicated a 69.1% and 37.6% higher
risk of developing CKD with abdominal obesity compared with
the lowest quartile for men and women, respectively.
Dyslipidemia is also an important risk factor for proteinuria and
decline of renal function . In a prospective study of 12,728
subjects, high TG and low HDL cholesterol levels predicted an
increased risk of renal dysfunction . According to Ryu et al.
 both high TG and low HDL cholesterol levels were associated
with a significantly increased risk of CKD. These results remained
unchanged, even after additional adjustment for incident HT and
DM. The mechanisms underlying the contribution of lipids to
renal injury are not completely understood. Dyslipidemia is
associated with glomerular capillary endothelial and mesangial cell
as well as podocyte injury, which further leads to mesangial
sclerosis [29,30]. The accumulation of lipoproteins in the
glomerular mesangium can stimulate matrix production and
glomerulosclerosis . Although hypertriglyceridemia and low
HDL cholesterol levels have been previously associated with an
increased risk for CKD , these factors are often overlooked
in clinical practice. Our results suggest that these could be
potential targets for reducing the risk of CKD.
DM and HT are the most common risk factors for ESRD ,
and MS is frequently associated with these factors. The PAMELA
(Pressioni Arteriose Monitorate E Loro Associazioni) population
study revealed high normal blood pressure values and HT in 80%
individuals with MS [32,33]. According to the results of a previous
study, insulin resistance and central obesity have been considered
the main factors involved in hypertension pathophysiology
associated with MS . Recent community-based prospective
observational cohort studies reported a significant risk for impaired
fasting glucose and development of eGFR,60 mL/min/1.73 m2
in Asia [35,36]. Evidence has shown that hyperinsulinemia occurs
well before the onset of glucose intolerance, and this evidence
suggests insulin resistance at levels of the muscle and liver, which is
not directly indicated in the NCEP-ATP III criteria for MS. Thus,
insulin resistance and subsequent hyperinsulinemia in addition to
mild hyperglycemia may be accountable for the association
between impaired fasting glucose level and CKD [37,38]. In our
analysis, we excluded subjects with diabetes to appreciate the real
impact of MS. both high blood pressure and high fasting glucose
levels were associated with significantly increased risk of CKD for
men and women.
The present study has several limitations. First, the
crosssectional study design makes it difficult to infer causality between
MS and the risk of developing CKD. Second, laboratory tests,
specifically estimation of serum creatinine levels were performed in
each hospital. Therefore, inter-laboratory variability may be
present. A systematic difference in creatinine measurements
Description of model covariates
Model 1: unadjusted
Model 2: adjusted for age, sex
eGFR,60 mL/min/1.73 m2
Model 1: unadjusted
Model 2: adjusted for age, sex
Model 3: adjust for age, sex, proteinuria
Chronic kidney disease
Model 1: unadjusted
Model 2: adjusted for age, sex
Abbreviations: eGFR; estimated glomerular filtration rate; CI, confidence interval.
aAll P value for trend,0.001.
Odds ratio (95% CI)
Low HDL cholesterola
Systolic blood pressurea
Diastolic blood pressurea
High fasting glucosea
Number of components modelb
Odds ratio (95% CI)
Note: Adjusted for factors included in age and sex.
Abbreviations: CI, confidence interval; HDL, high-density lipoprotein.
aReference group is lowest quartile (Q1) for each set of quartiles of factors.
bReference group is 0 component for number of componants model.
cP value for trend.0.05.
dP value for trend,0.05.
eP value for trend,0.001.
between laboratories could have affected the association between
MS and CKD. Third, CKD was defined as an eGFR,60 mL/
min/1.73 m2 or dipstick proteinuria ($1+). This definition didnt
include another kidney damages (e.g. abnormal urine sediment,
abnormal blood and urine chemistry, abnormal imaging studies)
and repeated measurements of creatinine levels and proteinuria
were not performed. These factors could have led to
underestimation or overestimation of the prevalence of CKD. Finally, other
parameters associated with obesity and glucose metabolism, such
as physical activity and alcohol consumption, were not evaluated
in the present study. However, we believe most of these potential
limitations should be consistently attenuated by the large sample
size of the study.
In conclusion, our study confirmed MS and its individual
components as a strong and independent risk factor for men and
women with CKD. In addition, we found a graded relationship
between the number of MS components and the risk for CKD.
Our results emphasise that individuals with metabolic risk factors
should be identified that an early stage and should undergo
multidisciplinary interventions, particularly lifestyle modifications,
to impede the development of CKD.
Conceived and designed the experiments: YUK SWK. Performed the
experiments: YUK HYK JSC CSK. Analyzed the data: YUK EHB SKM
SWK. Contributed reagents/materials/analysis tools: YUK HYK JSC
CSK. Wrote the paper: YUK SWK.
Figure 2. The prevalence of markers of chronic kidney disease according to number of metabolic syndrome components. (A) Overall.
(B) Men. (C) Women.
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