Original article

https://doi.org/10.6065/apem.2346044.022
Ann Pediatr Endocrinol Metab 2024;29:29-37

Comparison of anthropometric, metabolic, and body

compositional abnormalities in Korean children
and adolescents born small, appropriate, and large
for gestational age: a population-based study from
KNHANES V (2010–2011)
Tae Kwan Lee1, Purpose: The impacts of growth restriction and programming in the fetal stage on
Yoo Mi Kim2,3, metabolic and bone health in children and adolescents are poorly understood.
Han Hyuk Lim1,2 Moreover, there is insufficient evidence for the relationship between current
growth status and metabolic components. Herein, we compared the growth status,
1
Department of Pediatrics, Chungnam metabolic and body compositions, and bone mineral density in Korean children
National University Hospital, Daejeon, and adolescents based on birth weight at gestational age.
Korea Methods: We studied 1,748 subjects (272 small for gestational age [SGA], 1,286
2
Department of Pediatrics, Chungnam appropriate for gestational age [AGA], and 190 large for gestational age [LGA];
National University College of Medi­ 931 men and 817 women) aged 10–18 years from the Korean National Health
cine, Daejeon, Korea and Nutrition Examination Survey (KNHANES) V (2010–2011). Anthropometric
3
Department of Pediatrics, Chungnam
measurements, fasting blood biochemistry, and body composition data were
National University Sejong Hospital,
Sejong, Korea analyzed according to birth weight and gestational age.
Results: The prevalence of low birth weight (14.7% vs. 1.2% in AGA and 3.2% in LGA,
P<0.001) and current short stature (2.237 [1.296–3.861] compared to AGA, P=0.004)
in SGA subjects was greater than that in other groups; however, the prevalence of
overweight and obesity risks, metabolic syndrome (MetS), and MetS component
abnormalities was not. Moreover, no significant differences were found in age- and
sex-adjusted lean mass ratio, fat mass ratio, truncal fat ratio, bone mineral content,
or bone density among the SGA, AGA, and LGA groups in Korean children and
adolescents.
Conclusion: Our data demonstrate that birth weight alone may not be a
determining factor for body composition and bone mass in Korean children and
adolescents. Further prospective and longitudinal studies in adults are necessary to
confirm the impact of SGA on metabolic components and bone health.
Received: 14 February, 2023
Revised: 27 March, 2023
Accepted: 17 May, 2023 Keywords: Small for gestational age, Obesity, Metabolic syndrome

Address for correspondence:

Han Hyuk Lim
Department of Pediatrics, Chungnam
National University Hospital, Depart­
ment of Pediatrics, Chungnam
National University College of Medi­
cine, 282, Munhwa-ro, Jung-gu,
Daejeon, 35015, Korea
Email: damus@cnuh.co.kr
https://orcid.org/0000-0002-5297-
5913
Highlights
· We studied whether the impact of birth weight on current growth, metabolic alterations,
body composition, and bone mineral density in korean children and adolescents.
· Children and adolescents born small for gestational age had increased risk of short stature
and underweight, not metabolic component abnormalities, compared to those born
appropriate gestational age.
· The birth weight at gestational age alone may not be a determinant factor for the

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http:// ISSN: 2287-1012(Print)
creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any ISSN: 2287-1292(Online)
medium, provided the original work is properly cited.

©2024 Annals of Pediatric Endocrinology & Metabolism

TK Lee, et al. • Growth, metabolism, and body composition in SGA children
achievement of body composition and bone mass for
growing Korean children and adolescents. Rather, current
body weight could be more important.
Introduction
Children born small for gestational age (SGA) are known
to have long-term metabolic effects. Many studies have
demonstrated that weight gain during the fetal, perinatal, and
infant periods is associated with cardiometabolic parameters
in childhood and adolescents. Intrauterine growth restriction
and fetal programming are known to influence cardiometabolic
health in childhood and adolescents. In observational studies
of adults, a larger number of metabolic abnormalities, such as
hypertension, diabetes, and dyslipidemia, have been observed in
individuals born SGA.1-4) Furthermore, during the last decade,
the prevalence of metabolic syndrome (MetS) has increased
with increasing calorie-dense food intake in Korean children
and adolescents.5)
A few studies have revealed that the SGA group with obesity
has more severe problems with obesity than the non-SGA
group, even with the same state of high body mass index (BMI),
suggesting that birth weight has an impact on adult bone mass.
Some studies showed that birth weight is positively associated
with greater bone mineral content (BMC). In SGA infants, rapid
postnatal catch-up growth is a risk factor for many problems,
such as body composition alteration, later obesity, and MetS.
Both children born SGA and large for gestational age (LGA)
have obesity and obesity-related morbidities; however, the
evidence for whether this association is only mediated by
adiposity is conflicting.6,7)
In growing children, there are little data on the relationship
between current growth status and metabolic components based
on birth weight at gestational age. The potential impact of birth
size on bone accrual and its interaction with body composition
in SGA children is under debate. Several studies have revealed
that, compared to children born appropriate for gestational age
(AGA), SGA infants are lighter and have less body fat. However,
other studies have shown that SGA individuals are more likely
to experience obesity during childhood, particularly when they
exhibit catch-up growth. Stefan et al. found that the known
cardiovascular risks among infants born SGA, AGA, and LGA
are not reflected in metabolic consequences at the ages of 6–12
years.8,9)
In this study, we examined the effect of birth weight at
gestational age on current growth, metabolic alterations, bone
mineral density (BMD), and body composition in children and
adolescents using Korean population data.
Materials and methods
1. Subjects
This study used data from the Korean National Health and
Nutrition Examination Survey (KNHANES) V (2010–2011).
The KNHANES is a nationally representative, periodically
30 www.e-apem.org
conducted, cross-sectional survey conducted by the Division
of Chronic Disease Surveillance of the Korea Centers for
Disease Control and Prevention and the Korean Ministry of
Health and Welfare (https://knhanes.kdca.go.kr/). Procedures
performed in the KNHANES adhered to ethical guidelines. In
total, 2,018 children and adolescents aged 10–18 years were
enrolled. Among the participants, 270 participants without
anthropometric or laboratory data were excluded. A total
of 1,748 participants (931 men and 817 women) finally was
included in the analysis, representing the total population of
4,328,424 individuals aged 10–18 years in Korea. Subjects
were categorized into 3 groups according to birth weight by
gestational age (BWGA) and sex based on a study using Korean
statistics10) and by definition11): SGA (BWGA < 10th percentile),
AGA (10th percentile ≤ BWGA ≤ 90th percentile), and LGA
(BWGA > 90th percentile).
2. Data collection
Demographic characteristics were age, sex, height, weight,
BMI, waist circumference (WC), blood pressure (BP), birth
weight, gestational age, delivery type, household income,
physical activity, current smoking and alcohol status, and daily
calorie and food intake. The percentiles of height, weight,
BMI, WC, and BP were calculated based on the 2007 Korean
National Growth Chart.12) Household income was stratified
into quartiles as 1–4. Physical activity was defined as moderate
or vigorous exercise. Dietary data were evaluated via a 24-hour
recall nutrition survey. Biochemical samples were obtained
after ≥8 hours of fasting. Fasting plasma glucose (FPG), lipid
profiles, and liver enzyme levels were measured using a Hitachi
Automatic Analyzer 7600 (Hitachi, Tokyo, Japan). Fasting
insulin levels were evaluated using an immunoradiometric
assay (INS-IRMA; Biosource, Nivelles, Belgium) with a 1470
Wizard gamma counter (PerkinElmer, Turku, Finland). The
homeostasis model assessment of insulin resistance (HOMA-
IR) result was assessed as follows: fasting insulin (mU/L) × FPG
(mmol/L)/22.5.
Body composition and BMD were measured using whole-
body dual-energy x-ray absorptiometry with a QDR Discovery
fan-beam densitometer (Hologic Inc., Bedford, MA, USA).
BMD z-scores for the lumbar spine (LS), femur neck (FN), and
whole bone except the head (WB) were calculated according to
the reference values for Korean children and adolescents.12,13)
3. Definition of the metabolic component abnormalities
and MetS in children and adolescents
Underweight status was defined as BMI <10th percentile by
age and sex, while overweight and obesity were defined as 85th
percentile ≤BMI <95th percentile and BMI ≥95th percentile,
respectively. For diagnosis of MetS in Korean children and
adolescents, both the International Diabetes Federation (IDF)
and the modified National Cholesterol Education Program—
Adult Treatment Panel III (NCEP-ATP III) criteria were used.14)
 TK Lee, et al. • Growth, metabolism, and body composition in SGA children

For diagnosing MetS, the IDF criteria includes central obesity
(WC ≥90 cm in boys or ≥80 cm in girls or ≥90th percentile)
and at least 2 of the following characteristics: (1) triglyceride
(TG) level ≥150 mg/dL; (2) high-density lipoprotein (HDL)-
cholesterol level ≤40 mg/dL (or, in adolescents aged >16 years,
≤40 mg/dL in boys and ≤50 mg/dL in girls); (3) systolic BP
≥130 mmHg or diastolic BP ≥85 mmHg; and (4) FPG ≥100
mg/dL. For diagnosing MetS, the modified NCEP-ATP-III
criteria include the presence of 3 or more of the following
characteristics: (1) WC ≥90th percentile; (2) TG ≥110 mg/dL;
(3) HDL cholesterol ≤40 mg/dL; (4) systolic BP or diastolic BP
≥ 90th percentile; and (5) FPG ≥110 mg/dL.15) The metabolic
abnormality score was calculated as a total score of 5 points
across the 5 parameters (central obesity, high TG, low HDL-C,
high BP, high FPG), with each contributing 1 point.
4. Statistical analyses
For continuous variables, the numerical data are presented
as mean±standard deviation, while categorical variables are
presented as percentage and frequency. One-way analysis of
variance with post hoc analysis (Tukey test) and the chi-square
test were used to identify significant differences among the
3 groups (SGA, AGA, and LGA). Multiple logistic regression

Table 1. Auxologic and laboratory information of subjects

Variable SGA (N=272) AGA (N=1,286) LGA (N=190) P-value*
Age (yr) 13.8±2.6 13.6±2.5 13.8±2.5 0.333
Male sex 139 (50.9) 700 (54.3) 92 (48.4) 0.230
Height (cm) 157.8±12.0a) 159.6±11.7a) 162.4±10.4b) <0.001
Weight (kg) 50.5±13.7a) 52.7±14.1b) 55.8±13.9c) <0.001
2 a) a,b)
BMI (kg/m ) 20.0±3.7 20.4±3.7 20.9±3.5b) 0.024
WC (cm) 67.4±10.0a) 68.7±10.1a,b) 70.0±9.1b) 0.020
SBP (mmHg) 105.6±9.8 105.6±11.0 105.9±9.4 0.912
DBP (mmHg) 64.9±9.9 65.7±9.1 66.1±9.0 0.316
TG (mg/dL) 82.1±40.2 82.8±50.7 77.7±41.0 0.435
TC (mg/dL) 155.8±24.7 158.6±26.9 159.8±25.0 0.236
HDL-C (mg/dL) 53.6±9.7 54.3±10.6 55.7±11.2 0.138
ALT (IU/L) 13.9±10.2 15.4±15.8 14.0±10.1 0.248
FPG (mg/dL) 88.9±6.7 89.1±9.6 88.9±5.3 0.925
Insulin (μIU/mL) 13.4±5.6 14.0±6.8 13.4±5.6 0.546
HOMA-IR 3.0±1.4 3.1±1.5 3.0±1.3 0.701
Birth history
Birth weight (g) 2644.3±265.3a) 3278.3±318.7b) 3927.1±534.8c) <0.001
a)
Macrosomia 0 (0)a 6 (5.4) 105 (94.6)b) <0.001
LBW 40 (14.7)a) 16 (1.2)b) 6 (3.2)b) <0.001
VLBW 2 (0.7) 2 (0.2) 1 (0.5) 0.215
GA (wk) 39.5±1.3a) 39.6±1.4a) 39.0±2.9b) <0.001
Premature 11 (4.0)a) 36 (2.8)a) 18 (9.5)b) <0.001
Postmature 3 (1.1) 43 (3.4) 7 (3.7) 0.125
Maternal age (yr) 27.7±4.1 28.2±4.1 28.4±4.0 0.078
C/Sec 95 (34.8) 472 (36.6) 77 (40.5) 0.445
Household income (1–4)† 2.8±1.0 2.9±1.0 2.9±1.0 0.218
Physical activity, none 140 (51.3) 684 (53.2) 94 (49.7) 0.602
Current smoking 12 (3.7) 64 (5.0) 16 (8.4) 0.108
Current alcohol‡ 50 (24.2) 184 (15.3) 38 (25.7) 0.211
Calorie intake (kcal/day) 2156.3±856.0 2176.1±860.2 2217.3±860.3 0.772
Food intake
Carbohydrate (g/day) 331.9±128.0 336.6±124.0 340.9±129.8 0.785
Protein (g/day) 77.3±38.0 78.4±42.2 79.0±39.5 0.905
Fat (g/day) 58.2±37.9 57.3±36.5 59.0±38.5 0.815
Values are presented as mean±standard deviation or number (%).
SGA, small for gestational age; AGA, appropriate for gestational age; LGA, large for gestational age; BMI, body mass index; WC, weight
circumference; SBP, systolic blood pressure; DBP, diastolic blood pressure; TG, triglyceride; TC, total cholesterol; HDL-C, high-density
lipoprotein-cholesterol; ALT, alanine transaminase; FPG, fasting plasma glucose; HOMA-IR, homeostasis model of assessment–insulin
resistance; LBW, low birth weight; VLBW, very low birth weight; GA, gestational age; C/sec, cesarean section.
*Statistics are calculated by 1-way analysis of variance with post hoc analysis (Tukey), and upper small letters (a, b, c) mean significant
differences. †Household income: 1, low; 2, low-middle; 3, middle-high; 4, high. ‡Data from subjects aged >12 year-old.

www.e-apem.org 31
TK Lee, et al. • Growth, metabolism, and body composition in SGA children

analysis was used to assess the odds ratios (ORs) of the
prevalence of short stature, underweight status, and metabolic
changes in the SGA and LGA groups compared to the AGA
group. Graphs were arranged using GraphPad Prism version 6
for Windows (GraphPad Software Inc., San Diego, CA, USA).
IBM SPSS Statistics ver. 22 (IBM Corp., Armonk, NY, USA) was
used to analyze data, and P<0.05 was considered statistically
significant.
5. Ethical statement
This study was approved by the Institutional Review Board of
Chungnam National University Hospital (approval No. 2023-
02-096).
Results
1. Clinical and laboratory characteristics
Anthropometric and laboratory characteristics are summari­
zed in Table 1. The prevalence rates of SGA, AGA, and LGA
were 15.5% (n=272), 73.6% (n=1,286), and 10.9% (n=190),
respectively. In the SGA group, the height, weight, BMI, WC,
birth weight, and gestational age were significantly less than
those in the AGA or LGA groups. However, age, sex, BP, lipid
profile, alanine transaminase, fasting glucose, insulin, HOMA-
IR score, maternal age, delivery type, socioeconomic status,
physical activity, lifestyle behaviors, and food intake were not
significantly different among the 3 groups.
2. Comparison of current growth status according to
BWGA
The prevalence rates of short stature (height <3rd percentile)
and near-short stature (height <10th percentile) in children and
adolescents born SGA were 2.6% and 9.2%, respectively, which
were higher than those in subjects born AGA (1.0%, P=0.187;
3.7%, P<0.001, respectively) or LGA (0%, P=0.045; 1.6%,
P<0.001).16) In the case of height <10th percentile, SGA births
were most common at 9.2%, while AGA births composed 2.7%
and LGA births composed 1.6% of all individuals with height
<10th percentile (P<0.001). The prevalence of underweight
in those born SGA (16.5%) was also greater than that of those
born AGA (10.3%, P=0.009) or LGA (9.5%, P=0.046) (Fig. 1A).
However, the prevalence of overweight and obesity was not
significantly different among subjects born SGA, AGA, and
LGA (Fig. 1B).
Multiple logistic regression analysis was used to estimate
the risk of current short stature or underweight according to
BWGA. Children and adolescents born SGA had increased risk
of short stature (OR, 2.237; 95% confidence interval [CI], 1.296–
3.861; P=0.004), underweight (OR, 1.669; 95%, CI 1.133–2.458;
P=0.010), and short stature with underweight (OR, 4.376; 95%
CI, 1.317–14.542; P=0.016) compared to those born AGA, after
adjusting for confounding factors (Table 2).
3. Comparison of metabolic abnormalities according
to BWGA in children and adolescents with/without
overweight or obesity
The metabolic abnormality score and the prevalence of
metabolic component abnormalities and MetS did not differ
significantly among subjects born SGA, AGA, or LGA (Fig. 2A1,
A2). Moreover, no significant differences were found in subjects
with overweight or obesity according to BWGA (Fig. 2B1, B2).
4. Comparison of body composition and BMD according
to BWGA
Weight (P=0.010), lean mass (P=0.014), fat mass (P=0.016),
and truncal fat (P=0.036) in SGA girls were lower than those

Total SGA AGA LGA Total SGA AGA LGA

** *
** **
10 20
NS

8
Prevalence (%)

Prevalence (%)

15
6
10 NS

4 *

5
2

0 0
(A) Height (<3p) Height (<10p) (B) Underweight Overweight Obesity

Fig. 1. Prevalence of growth abnormalities. Comparison of the prevalence of growth abnormalities according to birth
weight at gestational age. (A) Current short stature <3rd percentile and <10th percentile for age and sex among the
SGA, AGA, and LGA groups. (B) Current underweight status (BMI <10th percentile), overweight status (85th percentile
≤BMI <95th percentile), and obesity (BMI ≥95 percentile) among the SGA, AGA, and LGA groups. Data are represented
as mean±standard error of the mean. SGA, small for gestational age; AGA, appropriate for gestational age; LGA, large
for gestational age; NS, not significant. *P<0.05, **P<0.01.

32 www.e-apem.org
 TK Lee, et al. • Growth, metabolism, and body composition in SGA children

in LGA girls. Body composition, including lean mass ratio, fat weight (SGA<AGA<LGA); however, there were no significant
mass ratio, and truncal fat ratio, were not significantly different differences among the groups (Table 3).
between the sexes, according to BWGA. The BMD z-scores
of LS, FN, and WB showed an increasing trend with birth

Table 2. Multiple logistic regression analysis

Model 1 Model 2 Model 3
Variable Prevalence, n (%)
OR (95% CI) P-value OR (95% CI) P-value
P-value OR (95% CI)
Short stature (height <10th percentile)
SGA (N=272) 25 (9.2) 2.610 (1.580–4.314) <0.001 2.509 (1.512–4.165) <0.001 2.237 (1.296–3.861) 0.004
AGA (N=1,286) 48 (3.7) 1 1 1
LGA (N=190) 3 (1.6) 0.414 (0.128–1.342) 0.142 0.386 (0.119–1.254) 0.113 0.118 (0.118–1.259) 0.115
Underweight (BMI <10th percentile)
SGA (N=272) 45 (16.5) 1.719 (1.191–2.480) 0.004 1.695 (1.173–2.451) 0.005 1.669 (1.133–2.458) 0.010
AGA (N=1,286) 133 (10.3) 1 1 1
LGA (N=190) 18 (9.5) 0.907 (0.541–1.522) 0.712 0.889 (0.529–1.495) 0.658 0.882 (0.523–1.487) 0.638
Short stature+underweight
SGA (N=272) 6 (2.2) 4.805 (1.538–15.013) 0.007 4.582 (1.459–14.392) 0.009 4.376 (1.317–14.542) 0.016
AGA (N=1,286) 6 (0.5) 1 1 1
LGA (N=190) 2 (1.1) 2.275 (0.456–11.353) 0.316 2.127 (0.424–10.684) 0.359 2.239 (0.445–11.256) 0.328
The odds ratios of short stature and underweight in Korean children and adolescents according to birth weight at gestational age from
multiple logistic regression analysis.
Model 1, nonadjusted; model 2, adjusted for age and sex; model 3, adjusted for age, sex, low birth weight, and prematurity; OR, odds
ratio; CI, confident interval; SGA, small for gestational age; AGA, appropriate for gestational age; LGA, large for gestational age; BMI, body
mass index.

15 NS NS
Metabolic abnormality score

0.5 Total
NS
SGA
Prevalence (%)

0.4 AGA
10 NS NS
LGA
0.3

0.2 5 NS
NS
NS
0.1

0.0 0
Total SGA AGA LGA Central High Low High High MetS MetS
obesity TG HDL-C BP FPG by IDF by NCEP
(A1) (A2)

60
Metabolic abnormality score

1.5 NS Total
NS
SGA
AGA
Prevalence (%)

1.0 40 LGA
NS NS

0.5 20
NS
NS NS

0.0 0
Total SGA AGA LGA Central High Low High High MetS MetS
(B1) (B2) obesity TG HDL-C BP FPG by IDF by NCEP

Fig. 2. Metabolic component abnormalities and metabolic syndrome. Comparison of metabolic component abnormalities and metabolic
syndrome in Korean children and adolescents according to birth weight at gestational age. (A1, A2) Metabolic abnormality score and the
prevalence of metabolic component abnormality and metabolic syndrome in all subjects. (B1, B2) Metabolic abnormality score and the
prevalence of metabolic component abnormality and metabolic syndrome in subjects with overweight and obesity statuses. Metabolic
abnormality score: total (5)=central obesity (1) + high TG (1) + low HDL-C (1) + high BP (1) + high FPG (1). Metabolic component
abnormalities and metabolic syndrome defined by the IDF and modified NCEP-ATP III for children and adolescents. Data are represented as
mean±standard error of the mean. SGA, small for gestational age; AGA, appropriate for gestational age; LGA, large for gestational age; TG,
triglyceride; low HDL-C, high-density lipoprotein-cholesterol; BP, blood pressure; FPG, fasting plasma glucose; MetS, metabolic syndrome;
IDF, International Diabetes Federation; NCEP, National Cholesterol Education Program-Adult Treatment Panel III (NCEP-ATP III); NS, not
significant.

www.e-apem.org 33
TK Lee, et al. • Growth, metabolism, and body composition in SGA children

Discussion was observed for BMI and waist/hip ratio.22,23)

This study revealed that (1) children and adolescents born
SGA had increased risk of short stature, underweight and short
stature with underweight compared to those born AGA; (2) the
metabolic abnormality score and the prevalence of metabolic
component abnormalities and MetS did not differ significantly
among subjects born SGA, AGA or LGA; and (3) there was no
significant difference in body composition or bone density in
Korean children and adolescents among the groups.
Our study examined anthropometric measures and growth
status, metabolic and body component proportions, and BMD
among Korean children and adolescents born SGA, AGA,
and LGA from Korean population data. The prevalence rates
of SGA, AGA, and LGA births were 15.5%, 73.6%, and 10.9%,
respectively, which are similar to those in other countries (e.g.,
the United States, Norway).17,18)
A significant risk factor for onset of MetS is low birth weight,
which increases the risk of morbidity in adulthood. Byberg
et al.19) observed that BWGA has a negative association with
insulin resistance, truncal fat, and hypertension over a long-
term period. In another study, no correlations were found
between low birth weight and MetS in children and young
adults.20,21) Height and weight at birth were positively correlated
with adult height and weight; however, only a weak correlation
In the current study, we found no significant differences in
the prevalence of metabolic abnormality scores, component
abnormalities, or MetS. Moreover, we found no differences
in BWGA in the overweight and obesity groups. Our results
showed that SGA with obesity did not induce larger increased
metabolic alterations with obesity than AGA or LGA in Korean
children and adolescents. There is a need for additional research
on the association between low birth weight and metabolic risk.
Being born SGA may facilitate excessive abdominal fat
accumulation in children and could be a significant factor of
MetS. These children have less subcutaneous fat but the same
amount of visceral fat as AGA children, with an increased
ratio of visceral to subcutaneous fat.24-27) SGA individuals had
significantly more total abdominal fat mass along with higher
proportions of truncal and abdominal fat mass.28) Some studies
have revealed that adiposity in SGA subjects is the adaptive
mechanism to increase energy balance or leptin resistance.29)
LGA infants are more likely to become overweight or obese
children, adolescents, and young adults. They also have an
increased risk of MetS in later life. Despite their larger bodies,
children born LGA have a balanced body composition and fat
distribution. Conversely, regardless of body size, children born
SGA have increased central adiposity.30)
However, data from previous studies on the correlation

Table 3. Body composition and bone density

Male (N=642) Female (N=550)
Variable
SGA (n=102) AGA (n=473) LGA (n=67) P-value* SGA (n=87) AGA (n =401) LGA (n=62) P-value*
Anthropometric parameter
Age (yr) 13.6±2.5 13.6±2.5 13.6±2.5 0.968 13.7±2.6 13.5±2.5 13.6±2.6 0.816
Height (cm) 161.4±14.2 161.9±13.1 164.1±13.3 0.406 154.5±7.3a) 156.4±8.8a) 159.5±7.0b) 0.002
Weight (kg) 54.0±15.2 55.2±15.6 56.1±13.6 0.678 46.6±10.1a) 49.7±11.5a,b) 52.2±11.4b) 0.010
BMI (kg/m2) 20.4±3.8 20.7±3.9 20.5±3.0 0.758 19.4±3.3 20.1±3.5 20.4±3.7 0.144
Body composition
Lean mass (kg) 40.6±10.9 41.1±11.1 41.9±10.7 0.749 31.6±5.3 33.2±6.3 34.5±5.2 0.014
Lean mass ratio† (%) 75.6±8.1 75.2±8.3 74.7±6.4 0.757 68.8±5.9 67.6±5.5 67.2±7.0 0.185
LMI (kg/m2) 15.2±2.2 15.4±2.2 15.3±2.1 0.867 13.2±1.5 13.5±1.6 13.5±1.4 0.280
Fat mass (kg) 13.1±6.7 13.6±7.1 13.7±5.0 0.783 14.6±5.4a) 16.1±5.9a,b) 17.4±7.1b) 0.016
Fat mass ratio‡ (%) 23.7±8.4 24.1±8.4 24.5±6.7 0.832 30.4±5.8 31.6±5.5 32.4±7.1 0.098
FMI (kg/m2) 5.0±2.4 5.2±2.6 5.1±1.9 0.836 6.0±2.1 6.5±2.1 6.8±2.6 0.095
Truncal fat (kg) 5.6±3.6 5.8±3.7 5.7±2.6 0.830 6.0±2.7a) 6.8±3.3a,b) 7.4±3.7b) 0.036
Truncal fat ratio§ (%) 40.9±5.4 41.0±5.5 40.3±4.9 0.603 40.2±4.6 41.0±5.0 41.1±5.2 0.365
BMCWB (kg) 1.8±0.5 1.9±0.6 1.9±0.6 0.672 1.6±0.4 1.7±0.4 1.8±0.3 0.076
Bone mineral density
LS z-score 0.01±1.11 -0.56±1.02 0.01±0.95 0.778 -0.22±1.02 -0.01±1.05 0.09±0.88 0.177
FN z-score -0.13±0.96 -0.05±1.04 -0.01±0.84 0.722 -0.20±0.96 -0.02±1.02 0.07±0.92 0.226
WB z-score -0.10±0.98 -0.01±0.94 0.02±0.83 0.612 -0.18±0.93 0.00±0.93 0.08±0.77 0.162
Values are presented as mean±standard deviation.
Comparison of body composition and bone density in Korean children and adolescents according to birth weight at gestational age
SGA, small for gestational age; AGA, appropriate for gestational age; LGA, large for gestational age; BMI, body mass index; LMI, lean body
mass index; FMI, fat mass index, BMCWB, whole-body bone mass; LS, total lumbar spine; FN femur neck; WB, whole-body bone.
*Statistics are calculated by 1-way analysis of variance with post hoc analysis (Tukey), and upper small letters (a, b, c) mean significant
differences. †Lean mass ratio=lean mass/body weight×100; ‡Fat mass ratio=fat mass/body weight×100; §Truncal fat ratio=truncal fat/
whole-body fat×100.

34 www.e-apem.org
 TK Lee, et al. • Growth, metabolism, and body composition in SGA children
between BWGA and current fat mass in adolescents and young
adults are conflicting. Several studies have reported a correlation
between birth weight for gestational age and childhood body fat
in adolescents and young adults.31,32) Meanwhile, other studies
have revealed a negative association.33,34) It is unclear whether
such a correlation might be the result of rapid postnatal catch-
up growth, a low birth weight, or the combination of the two.
In the current study comparing body composition, our data
showed that body composition, including lean mass ratio, fat
mass ratio, and truncal fat ratio, did not significantly differ
according to BWGA. A study on Brazilian adolescents reported
an association between fat mass and postnatal weight gain.35)
Leunissen et al. 36) reported that childhood weight gain is a
significant factor in young adult body composition, but that
birth size is less important. The heterogeneity of the SGA group
might be a contributing factor to the discrepancy between these
results.
In preterm and SGA children, low birth weight negatively
influences BMD and BMC. In AGA infants, postnatal growth
patterns have been linked to bone mineral accumulation.37,38)
However, the effect of catch-up growth in infancy on bone
accumulation in SGA infants has not been consistently studied.
Previous studies on SGA bone health have suggested that SGA
infants born with rapid catch-up growth encounter negative
effects of bone development. BMD accrual during infancy and
later was correlated with the rates of free fat mass, fat mass, and
weight gain during the first month of life. It remains unknown
whether birth size is always a major component of bone mass in
adolescence and later life, though fat mass and postnatal growth
are normal.39) Deodati et al.40) suggested that SGA children with
compensatory catch-up growth achieve body composition and
bone mass similar to those born AGA.
In our study, we recorded no significant differences in age-
and sex-adjusted lean body mass ratio, fat mass ratio, truncal
fat ratio, BMC, and bone density in Korean children and
adolescents between the SGA, AGA, and LGA groups. Our data
demonstrated that birth weight at gestational age alone might
not be a determining factor for body composition and bone
density during growth in Korean children and adolescents.
Therefore, we suggest that current low body weight and short
stature may be more important factors than birth size, affecting
bone health in the AGA, LGA, and SGA groups.
This investigation was a cross-sectional study conducted only
from 2010–2011 and had limitations, as information on sexual
maturity, catch-up growth, bone age, and genetic background
was not provided and is subject to recall bias of dietary records.
Although it is strengthened by a large-scale nationwide study,
it has other limitations because studies conducted periodically
have not been merged.
In conclusion, our data demonstrate that birth weight at
gestational age alone may not determine body composition,
including metabolic alterations and bone density, during growth
in Korean children and adolescents. Rather, current body
weight could be more important. It is advised that SGA children
should be regularly followed up by pediatricians to monitor
catch-up growth, body composition, and metabolic parameters.
Prospective longitudinal studies in childhood and adolescence
are necessary to confirm the impact of SGA on metabolic
components and bone health. Overall, our study could help
support the effective management of SGA infants for better
long-term metabolic consequences.
Notes
Conflicts of interest: No potential conflict of interest relevant
to this article was reported.
Funding: This study received no specific grant from any
funding agency in the public, commercial, or not-for-profit
sectors.
Data availability: The data that support the findings of this
study can be provided by the corresponding author upon
reasonable request.
Author contribution: Conceptualization: TKL; Data curation:
YMK, HHL; Methodology: TKL, YMK, HHL; Writing - original
draft: TKL; Writing - review & editing: TKL
ORCID
Tae Kwan Lee: 0000-0002-6667-9875
Yoo Mi Kim: 0000-0002-8440-5069
Han Hyuk Lim: 0000-0002-5297-5913
References
1. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman
JI, Donato KA, et al. Harmonizing the metabolic syndrome:
a joint interim statement of the International Diabetes
Federation Task Force on Epidemiology and Prevention;
National Heart, Lung, and Blood Institute; American
Heart Association; World Heart Federation; International
Atherosclerosis Society; and International Association for
the Study of Obesity. Circulation 2009;120:1640-5.
2. Eckel RH, Grundy SM, Zimmet PZ. The metabolic
syndrome. Lancet 2005;365:1415-28.
3. Al-Hamad D, Raman V. Metabolic syndrome in children
and adolescents. Transl Pediatr 2017;6:397-407.
4. Vanlancker T, Schaubroeck E, Vyncke K, Cadenas-Sanchez
C, Breidenassel C, González-Gross M, et al. Comparison of
definitions for the metabolic syndrome in adolescents. Eur
J Pediatr 2017;176:241-52.
5. Park SI, Suh J, Lee HS, Song K, Choi Y, Oh JS, et al. Ten-
year trends of metabolic syndrome prevalence and
nutrient intake among Korean children and adolescents: a
population-based study. Yonsei Med J 2021;62:344-51.
6. Chiavaroli V, Derraik JG, Hofman PL, Cutfield WS. Born
large for gestational age: bigger is not always better. J Pediatr
2016;170:307-11.
7. Hong YH, Chung S. Small for gestational age and obesity
related comorbidities. Ann Pediatr Endocrinol Metab
2018;23:4-8.
www.e-apem.org 35
TK Lee, et al. • Growth, metabolism, and body composition in SGA children
8. Kuhle S, Maguire B, Ata N, MacInnis N, Dodds L. Birth
weight for gestational age, anthropometric measures,
and cardiovascular disease markers in children. J Pediatr
2017;182:99-106.
9. Crume TL, Scherzinger A, Stamm E, McDuffie R, Bischoff
KJ, Hamman RF, et al. The long-term impact of intrauterine
growth restriction in a diverse U.S. cohort of children: the
EPOCH study. Obesity 2014;22:608-15.
10. Lim JS, Lim SW, Ahn JH, Song BS, Shim KS, Hwang IT. New
Korean reference for birth weight by gestational age and
sex: data from the Korean Statistical Information Service
(2008-2012). Ann Pediatr Endocrinol Metab 2014;19:146-
53.
11. Olsen IE, Groveman SA, Lawson ML, Clark RH, Zemel BS.
New intrauterine growth curves based on United States
data. Pediatrics 2010;125:e214-24.
12. Korea Center for Disease Control and Prevention; Korean
Pediatric Society Committee for the Development of
Growth Standard for Korean Children and Adolescents.
2007 Korean children and adolescents growth standard:
commentary for the development of 2007 growth chart
[Internet]. Cheongju (Korea): KCDC, Division of Chronic
Disease Surveillance; c2019 [cited 2022 Dec 11]. Available
from: http://www.cdc.go.kr/.
13. Kang MJ, Hong HS, Chung SJ, Lee YA, Shin CH, Yang SW.
Body composition and bone density reference data for
Korean children, adolescents, and young adults according
to age and sex: results of the 2009-2010 Korean National
Health and Nutrition Examination Survey (KNHANES). J
Bone Miner Metab 2016;34:429-39.
14. Zimmet P, Alberti K Gerrge MM, Kaufman F, Tajima N,
Silink M, et al. The metabolic syndrome in children and
adolescents. Pediatr Diabetes 2007;8:299-306.
15. Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel
RH, Franklin BA, et al. Diagnosis and management of the
metabolic syndrome. An American Heart Association/
National Heart, Lung, and Blood Institute Scientific
Statement: executive summary. Crit Pathw Cardiol
2005;4:198-203.
16. Kim JH, Kim DH, Lim JS. Growth status of children and
adolescents born small for gestational age at full term in
Korea: data from the KNHANES-V. J Pediatr Endocrinol
Metab 2020;33:743-50.
17. Finken MJJ, van der Steen M, Smeets CCJ, Walenkamp
MJE, de Bruin C, Hokken-Koelega ACS, et al. Children
born small for gestational age: differential diagnosis,
molecular genetic evaluation, and implications. Endocr Rev
2018;39:851-94.
18. Giabicani E, Pham A, Brioude F, Mitanchez D, Netchine
I. Diagnosis and management of postnatal fetal growth
restriction. Best Pract Res Clin Endocrinol Metab 2018;32:
523-34.
19. Byberg L, McKeigue PM, Zethelius B, Lithell HO. Birth
weight and the insulin resistance syndrome: association
of low birth weight with truncal obesity and raised
36 www.e-apem.org
plasminogen activator inhibitor-1 but not with abdominal
obesity or plasma lipid disturbances. Diabetologia
2000;43:54-60.
20. Hirchler V, Bugna J, Roque M, Gilligan T, Gonzalez C. Does
low birth weight predict obesity/overweight and metabolic
syndrome in elementary school children? Arch Med Res
2008;39:796-802.
21. Ramadhani MI, Grobbee DE, Bots ML, Castro Cabezas M,
Vos LE, Oren A, et al. Lower birth weight predict metabolic
syndrome in young adult: the Atherosclerosis Risk in Young
Adults (ARYA) study. Atherosclerosis 2006;184:21-7.
22. Euser AM, Dekker FW, Hallan SI. Intrauterine growth
restriction: no unifying risk factor for the metabolic
syndrome in young adults. Eur J Cardiovasc Prev Rehabil
2010;17:314-20.
23. Pilgaard K, Færch K, Poulsen P, Larsen C, Andersson EA,
Pisinger C, et al. Impact of size at birth and prematurity
on adult anthropometry in 4744 middle-aged Danes: the
Inter99 study. J Dev Orig Health Dis 2010;1:319-28.
24. Ibáñez L, Ong K, Dunger DB, de Z egher F. Early
development of adiposity and insulin resistance after catch-
up weight gain in small for gestational age children. J Clin
Endocrinol Metab 2006;91:2153-8.
25. Ibáñez L, López-Bermejo A, Díaz M, Marcos MV, Casano
P, de Zegher F. Abdominal fat partitioning and high-
molecular-weight adiponectin in short children born small
for gestational age. J Clin Endocrinol Metab 2009;94:1049-
52.
26. Van der Steen M, Smeets CC, Kerkhof GF, Hokken-Koelega
AC. Metabolic health of young adults who were born
small for gestational age and treated with growth hormone,
after cessation of growth hormone treatment: a 5-year
longitudinal study. Lancet Diabetes Endocrinol 2017;5:106-
16.
27. Rasmussen EL, Malis C, Jensen CB, Jensen JE, Storgaard H,
Poulsen P, et al. Altered fat tissue distribution in young adult
men who had low birth weight. Diabetes Care 2005;28:151-
3.
28. Mericq V, Martinez-Aguayo A, Uauy R, Iñiguez G, Van der
Steen M, Hokken-Koelega A. Long-term metabolic risk
among children born premature or small for gestational
age. Nat Rev Endocrinol 2017;13:50-62.
29. Miras M, Ochetti M, Martín S, Silvano L, Sobrero G, Castro
L, et al. Serum levels of adiponectin and leptin in children
born small for gestational age: relation to insulin sensitivity
parameters. J Pediatr Endocrinol Metab 2010;23:463-71.
30. Andersen LG, Holst C, Michaelsen KF, Baker JL, Sørensen
TI. Weight and weight gain during early infancy predict
childhood obesity: a case cohort study. Int J Obes (Lond)
2012;36:1306-11.
31. Hong YH, Lee JE. Large for gestational age and obesity-
related comorbidities. J Obes Metab Syndr 2021;30:124-31.
32. Mullett MD, Cottrell L, Lilly C, Gadikota K, Dong L, Hobbs
G, et al. Association between birth characteristics and
coronary disease risk factors among fifth graders. J Pediatr
 TK Lee, et al. • Growth, metabolism, and body composition in SGA children
2014;164:78-82.
33. Biosca M, Rodríguez G, Ventura P, Samper MP, Labayen I,
Collado MP, et al. Central adiposity in children born small
and large for gestational age. Nutr Hosp 2011;26:971-6.
34. Dolan MS, Sorkin JD, Hoffman DJ. Birth weight is inversely
associated with central adipose tissue in healthy children
and adolescents. Obesity(Silver Spring) 2007;15:1600-8.
35. Wells JC, Dumith SC, Ekelund U, Reichert FF, Menezes AM,
Victora CG, et al. Associations of intrauterine and postnatal
weight and length gains with adolescent body composition:
prospective birth cohort study from Brazil. J Adolesc
Health 2012;51(6 Suppl):S58-64.
36. Leunissen RW, Stijnen T, Hokken-Koelega AC. Influence
of birth size on body composition in early adulthood:
the programming factors for growth and metabolism
(PROGRAM)-study. Clin Endocrinol (Oxf) 2009;70:245-
51.
37. Longhi S, Mercolini F, Carloni L, Nguyen L, Fanolla A,
Radetti G. Prematurity and low birth weight lead to
altered bone geometry, strength, and quality in children. J
Endocrinol Investig 2015;38:563-8.
38. Baird J, Kurshid MA, Kim M, Harvey N, Dennison
E, Cooper C. Does birth weight predict bone mass
in adulthood? A systemic review and meta-analysis.
Osteoporosis Int 2011;22:1323-34.
39. Buttazzoni C, Rosengren B, Tveit M, Landin L, Nilsson JÅ,
Karlsson M. Preterm children born small for gestational
age are at risk for low adult bone mass. Calcif Tissue Int
2016;98:105-13.
40. Deodati A, Manco M, Mariani M, Bocchini S, Högler W,
Cappa M, et al. Bone density and body composition in
small for gestational age children with adequate catch up
growth: a preliminary retrospective case control study.
Bone 2021;153:116114.
www.e-apem.org 37