Highlights
· Obesity could be categorized as class I, II and III according to body mass index.
· Values of cardiometabolic risk factors worsened with BMI increase.
· Class II and III obesity in Korean youth was associated with an increased prevalence of cardiometabolic risk factors and metabolic syndrome.
Introduction
The prevalence of obesity and metabolic syndrome (MetS) among children and adolescents is increasing, both in Korea and worldwide [1-5]. According to the Korea National Health and Nutrition Examination Survey (KNHANES) data, in children and adolescents 10–19 years of age, the prevalence of overweight and obesity in 1998, 2001, and 2005 was 16.4%, 23.8%, and 24.2%, respectively [2,4,6]. As the prevalence of obesity has increased, the degree of obesity has been classified in greater detail using several criteria. According to recent guidelines, class I obesity in children and adolescents is defined as a body mass index (BMI; weight [kg] divided by height squared [m2]) ≥ 95th percentile; class II/III obesity is defined as a BMI ≥120% of the 95th percentile for age and sex [7-10].
MetS is defined as a combination of cardiometabolic risk factors (CMRFs) including abnormal waist circumference (WC), blood pressure (BP), triglycerides level, high-density lipoprotein cholesterol (HDL-C) level, and glucose level [11]. MetS increases among individuals with obesity; it is a well-known risk factor for cardiovascular disease, type 2 diabetes mellitus, and hypertension in both children and adults [12-14]. Despite the clinical importance of MetS, uniform consensus cutoff values for MetS components in children and adolescents have not been established. Thus, there are differences in the markers and cutoff values based on set of criteria [15].
In several studies, associations with various CMRFs were reported to increase with increasing obesity severity [4,8,9,16]. Although few studies of Korean children and adolescents have been conducted, the data are outdated and do not reflect the latest criteria. Furthermore, there are sparse data regarding the prevalence of MetS based on degree of obesity [17]. Therefore, in this study, data on CMRF and MetS prevalence based on obesity severity in Korean children and adolescents were analyzed using the latest updated criteria of nationally representative data. Additionally, associations with the prevalence of various CMRFs were examined based on obesity severity.
Materials and methods
1. Study participants
Data used in this study were obtained from the fourth to seventh waves of the KNHANES performed between 2007 and 2018. The KNHANES is a cross-sectional survey that involves nationally representative data collection; it has been conducted since 1998 by the Korea Centers for Disease Control and Prevention. The KNHANES was designed using a stratified multi-stage clustered probability sampling method among noninstitutionalized citizens in Korea. The KNHANES consists of a health interview, nutrition survey, and health examination. Detailed methods for KNHANES data collection are described elsewhere [18].
Among the 97,662 individuals enrolled in the KNHANES during 2007−2018, 9,984 (5,305 boys and 4,709 girls) 10–18 years of age with anthropometric data including height, weight, and BMI were considered as candidates for analysis. The participants analyzed in the study are described in Table 1. Participants with no values for total cholesterol (TC), HDL-C, low-density lipoprotein cholesterol (LDL-C), triglycerides, or fasting glucose were excluded. Participants who fasted <8 hours were also excluded. The non-HDL-C level was calculated as the HDL-C level subtracted from the TC level (non-HDL-C = TC−HDL-C). Participants with no values for BP or glycated hemoglobin (HbA1c) were excluded, as were participants with no values for any component of MetS.
2. Anthropometric measurements
Anthropometric measurements, including height, weight, and WC, were performed by trained medical personnel. Height was measured to the nearest 0.1 cm using a stadiometer (Seca 225; Seca, Hamburg, Germany). Weight was measured to the nearest 0.1 kg using an electronic balance (GL-6000-20; G-tech, Seoul, Korea). BMI was calculated as weight (kg) divided by height squared (m2). Height, weight, and BMI were transformed to percentile values using the 2017 Korean National Growth Chart [19]. WC was measured using a flexible tape to the nearest 0.1 cm at the midpoint between the lowermost margin of the rib and the uppermost margin of the iliac crest during the expiratory phase of respiration (Seca 220; Seca). BP was measured three times on the right arm using a mercury sphygmomanometer with a cuff appropriate for arm circumference after the participant had rested for at least 5 minutes in a sitting position (Baumanometer Desk model 0320 in 2007–2012 and Baumanometer Wall Unit 33 [0850] in 2013–2018; W.A. Baum, Copiague, NY, USA). The mean values of the second and third systolic and diastolic BP measurements were used for analyses in this study.
3. Laboratory tests
Blood samples were collected by trained medical personnel. Fasting blood samples obtained from venipuncture were transported to the Central Laboratory for analysis within 24 hours. Plasma glucose, TC, HDL-C, LDL-C, and triglycerides levels were measured using a Hitachi Automatic Analyzer 7600 (Hitachi, Tokyo, Japan). HbA1c level was measured via highperformance liquid chromatography (HPLC-723G7, Tosoh, Tokyo, Japan), which is the method certified by the National Glycohemoglobin Standardization Program.
4. Definitions of obesity severity, CMRFs, and MetS
The degree of obesity was categorized based on BMI percentile for corresponding sex and age: normal weight as BMI <85th percentile; overweight as BMI ≥85th and <95th percentile; class I obesity as BMI ≥95th and <120% of the 95th percentile; and class II obesity as BMI ≥120% of the 95th percentile or ≥30 kg/m2; and class III obesity as BMI ≥140% of the 95th percentile or ≥35 kg/m2 [19,20].
The definitions of abnormal CMRF values are described in Table 1: TC ≥200 mg/dL, HDL-C <40 mg/dL, LDL-C ≥130 mg/dL, triglycerides ≥150 mg/dL, non-HDL-C ≥145 mg/dL [21,22], systolic BP ≥95th percentile or diastolic BP ≥95th percentile for sex, age, and height [23], fasting glucose ≥100 mg/dL, and HbA1c ≥5.7% [24].
MetS was defined using 2 sets of criteria (Table 1). Using the International Diabetes Federation (IDF) criteria, MetS was defined as central obesity, which is a WC ≥90th percentile for age and sex with 2 or more of the following 4 criteria: triglycerides ≥150 mg/dL, HDL-C <40 mg/dL (boys 10–18 years of age and girls 10–15 years of age) or <50 mg/dL (girls ≥16 years of age), systolic BP ≥130 mmHg or diastolic BP ≥85 mmHg, and/or fasting glucose ≥100 mg/dL [25]. Using the modified National Cholesterol Education Program-Adult Treatment Panel (NCEP-ATP) III criteria, MetS was defined as 3 or more of the 5 following criteria: WC ≥90th percentile for age and sex; triglycerides ≥110 mg/dL; HDL-C <40 mg/dL; systolic or diastolic BP ≥90th percentile for age, sex, and height; and/or fasting glucose ≥110 mg/dL [26].
5. Statistical analyses
Statistical analyses were performed using Stata 16.1 (StataCorp LP, College Station, TX, USA). The svy commands and sample weights were used for all analyses. Results are expressed as either the weighted mean (standard error, SE) or the number of participants (weighted %). TC, HDL-C, LDL-C, triglycerides, and non-HDL-C levels were log-transformed for analyses because they exhibited skewed distributions; they are presented as the geometric mean (SE). Student t-test was used to compare continuous variables between groups. Chi-squared tests were used to compare proportions between groups. Multiple logistic regression analysis was performed to calculate the sex- and age-adjusted odds ratio (OR) with 95% confidence intervals (CIs) for possible associations between CMRFs or MetS and degree of obesity. Multiple regression analysis was performed to determine associations between the prevalence of each CMRF and degree of obesity. A 2-tailed P-value <0.05 was considered statistically significant.
Results
1. Demographic and clinical characteristics of study participants
Table 2 shows demographic and clinical characteristics of study participants. In total, 9,984 individuals were analyzed in this study: 5,289 (53.04%) were boys and 4,695 (46.96%) were girls. The mean values for TC, HDL-C, LDL-C, triglycerides, and non-HDL-C levels were higher in girls (P<0.001), while the mean values for systolic and diastolic BP, as well as fasting glucose, were higher in boys (P<0.001).
The proportion of participants with overweight, class I obesity, class II, or class III obesity was higher in boys than in girls (20.91% for boys and 18.26% for girls, P<0.001). The prevalence of MetS did not differ according to sex, irrespective of definition.
According to IDF criteria, prevalence was higher in girls than in boys (P=0.650); conversely, according to the modified NCEPATP III criteria, the prevalence was higher in boys than in girls (P=0.086).
The proportion of participants with class I, class II, or class III obesity showed an increasing trend between 2007 and 2018 (P=0.025, P=0.105, and P=0.508 in total, boys, and girls, respectively) (Supplementary Table 1).
2. Prevalence of CMRFs and MetS based on BMI category
Table 3 and Fig. 1 showed the prevalence of abnormal CMRFs and MetS by BMI category. Supplementary Table 2 shows the mean values for each CMRF based on BMI category and sex. Mean CMRF values were higher with increasing obesity severity, except for mean HDL-C, which was lower with increasing obesity severity.
3. Adjusted ORs for CMRFs and MetS based on BMI category
Table 4 shows adjusted ORs and 95% CIs for CMRFs and MetS based on BMI category. The ORs of high TC, low HDL-C, high LDL-C, high triglycerides, high non-HDL-C, high BP, and prevalence of MetS were greater among children and adolescents with class II/III obesity than among participants with normal weight; these factors showed tendencies to increase with increasing BMI category. Adjusted OR (95% CI) for TC for class II/III obesity in all participants was 4.11 (2.58–6.55), and adjusted OR (95% CI) for BP for class II/III obesity in all participants was 9.44 (6.53–13.66). In analyses of all participants, the OR for MetS according to IDF criteria was 950.3 (321.6–2,808.3), and the OR for MetS according to modified NCEP-ATP III criteria was 126.8 (77.9–206.5). There were few significant differences in these variables based on BMI category among girls; however, all differences were statistically significant among boys. Overweight children and adolescents had lower ORs for most CMRFs compared with obese participants.
Discussion
In this study, KNHANES data from 9,984 Korean children and adolescents (10–18 years of age) were analyzed to examine the associations between obesity severity and CMRFs and MetS. The prevalence of abnormal CMRFs and MetS increased with obesity severity. Notably, class II/III obesity in children and adolescents was associated with high mean values and CMRF prevalence. Additionally, the ORs for CMRFs and prevalence of MetS were higher in children and adolescents with class II/III obesity than in children and adolescents with normal weight.
Recently, several proposals have been suggested regarding the classification of obesity based on BMI. Classification of children and adolescents based on obesity severity provides a more detailed approach to patients at risk of potential complications and health problems [27-29]. According to representative KNHANES data collected from 2007–2018, the prevalence of overweight, class I obesity, and class II/III obesity was 9.52%, 7.73%, and 2.42% in children and adolescents 10–18 years of age, respectively. In the United States, the prevalence of overweight, class I obesity, and class II/III obesity was 14.8%, 11.3%, and 5.1%, respectively, in children and adolescents 2–19 years of age [7]. Although the prevalence of obesity is lower in Korea than in the United States, the prevalence in Korean children and adolescents is increasing compared with results from a Korean study conducted from 2007–2014 [17].
According to Freedman and colleagues, CMRFs (e.g., dyslipidemia, hypertension, and hyperinsulinemia) were more common in children with a BMI in the 99th percentile than in children with a BMI in the 95th percentile. In children and adolescents with a BMI in the 95th percentile (5–17 years), 70%, 39%, and 18% had at least 1, 2, or 3 CMRFs, respectively. Furthermore, in children and adolescents with a BMI in the 99th percentile (defined as severe obesity in this study), 84%, 59%, and 33% had at least 1, 2, or 3 CMRFs, respectively. In the Bogalusa cohort study, the number of CMRFs increased based on BMI percentile in children and adolescents. Among children and adolescents with a BMI in the 95th percentile according to the Centers for Disease Control growth charts, 39% had at least 2 CMRFs. Among individuals with a BMI in the 99th percentile, 59% had at least 2 CMRFs. Based on a previous study of KNHANES data analyzed between 2007 and 2014, the incidence of abnormal CMRFs was higher among individuals with more severe obesity than individuals with less severe obesity [17]. Therefore, it is important to understand the prevalence of CMRFs based on obesity severity classification. Moreover, early recognition and management of obesity based on its severity are important for preventing MetS and complications associated with obesity.
In this study, MetS prevalence differed based on a set of criteria used for obesity evaluation. Unlike adults, children and adolescents have increased insulin resistance because of physiological changes during puberty; therefore, the adult MetS definitions cannot be used for children and adolescents. Currently, there is no established uniform consensus to evaluate risk in children and adolescents [25,30,31]. However, based on these study results, according to both sets of MetS criteria, a relationship was observed between MetS and obesity severity, consistent with our CMRF findings. MetS prevalence increased with increasing obesity severity in both boys and girls.
Early onset of obesity is associated with insulin resistance and MetS in both children and adults and can lead to cardiovascular diseases during adulthood [30,32-34]. Furthermore, obesity is a wellknown cause of MetS, dyslipidemia, type-2 diabetes mellitus, cardiovascular diseases, nonalcoholic fatty liver disease, and mental disorders in both children and adolescents [4,9,27,35]. Consequently, early detection and management of obesity and MetS in children and adolescents are important to prevent cardiovascular disease development in adulthood and associated health consequences [30,31,36,37].
Although this study was conducted using a nationally representative dataset, it had several limitations. First, the sample size was small for some ages, and data for children under 10 years old were not included. Therefore, caution is needed when applying these results to younger children. Second, because of the small sample size, class III obesity (i.e., BMI ≥95th and ≥140% of the 95th percentile) could not be subdivided and analyzed. Third, while only CMRFs and MetS were investigated, other factors associated with obesity development (e.g., birth body weight, family history, physical activity, and detailed dietary habits) were not considered [38]. Therefore, the causal relationships of these associated factors could not be determined.
A study was previously performed based on data obtained from KNHANES for Korean children and adolescents between 2007 and 2014. However, the study findings are outdated, and moreover, they do not reflect the current standards for obesity and hypertension [17]. To our knowledge, this is the first study to investigate CMRF prevalence and associations with obesity in a large, nationally representative sample of Korean children and adolescents. This study is meaningful because CMRF and MetS prevalence was analyzed based on obesity severity in Korean children and adolescents using nationally representative data. This study used the most recent BMI reference data from the Korean population (published in 2018) and the latest definitions of abnormal CMRF values to present current statuses of obesity and its comorbidities. Therefore, these results could be applied to establish screening and management guidelines in clinical practice.
In conclusion, this study demonstrated the prevalence of obesity in Korean children and adolescents. The prevalence of abnormal CMRFs and MetS increased with increasing obesity severity, especially in participants with class II/III obesity. The study results indicate the importance of measuring CMRFs in obese children and adolescents, as well as the need to establish a screening guideline based on obesity severity. Furthermore, guidelines should include obesity severity within clinical criteria for effective medical screening and appropriate management of children and adolescents nationwide.
Ethical statement
Informed consent was obtained from all participants in the KNHANES. The KNHANES protocol was approved by the Institutional Review Board of the Korea Centers for Disease Control and Prevention (2007-02CON-04-P, 2008-04EXP-01-C, 2009-01CON-03-2C, 2010-02CON-21-C, 2011-02CON-06-C, 2012-01EXP-01-2C, 2013-07-CON-03-4C, and 2013-12EXP-03-5C). Since 2015, the KNHANES has not required approval by the Institutional Review Board because surveys performed by the government for public welfare in Korea have been exempt from review by an ethics committee. This study was approved by the Institutional Review Board of Seoul National University Bundang Hospital (X-2105/683-902).
PDF Links
PubReader
ePub Link
XML Download
Full text via DOI
Full text via PMC
Download Citation
CrossRef TDM
Supplement1
Print
