Age trends of bone mineral density and percentile curves in healthy Chinese children and adolescents

Abstract

The clinical utility of dual-energy X-ray absorptiometry (DXA) measurement requires appropriate normative values, designed to be diverse with respect to age, gender and ethnic background. The purpose of this study was to generate age-related trends for bone density in Chinese children and adolescents, and to establish a gender-specific reference database. A total of 1,541 Chinese children and adolescents aged from 5 to 19-years were recruited from southern China. Bone mineral density (BMD), bone mineral content (BMC), and bone area (BA) were measured for the total body (TB) and total body less head (TBLH). The height-for-age, height-for-BA, and BMC-for-BA percentile curves were developed using the least mean square method. TB BMD and TBLH BMD were highly correlated. After 18 years, TB BMD was significantly higher in boys than girls. For TB BMC and TBLH BMC, gender differences were found in age groups 12 years and 16-19 years; however, the TBLH BMD was significantly different between genders >16 years. The head region accounted for 13-52 and 16-49 % of the TB BMC in boys and girls, respectively. Furthermore, the percentages were negatively correlated with age and height. This study describes a gender-specific reference database for Chinese children and adolescents aged 5-19 years. These normative values could be used for clinical assessment in this population.

Full text

ORIGINAL ARTICLE
Age trends of bone mineral density and percentile curves
in healthy Chinese children and adolescents
Bin Guo •Yi Xu •Jian Gong •
Yongjin Tang •Hao Xu
Received: 4 May 2012 / Accepted: 14 October 2012 / Published online: 30 January 2013
ÓThe Japanese Society for Bone and Mineral Research and Springer Japan 2013
Abstract The clinical utility of dual-energy X-ray
absorptiometry (DXA) measurement requires appropriate
normative values, designed to be diverse with respect to
age, gender and ethnic background. The purpose of this
study was to generate age-related trends for bone density in
Chinese children and adolescents, and to establish a gen-
der-specific reference database. A total of 1,541 Chinese
children and adolescents aged from 5 to 19-years were
recruited from southern China. Bone mineral density
(BMD), bone mineral content (BMC), and bone area (BA)
were measured for the total body (TB) and total body less
head (TBLH). The height-for-age, height-for-BA, and
BMC-for-BA percentile curves were developed using the
least mean square method. TB BMD and TBLH BMD were
highly correlated. After 18 years, TB BMD was signifi-
cantly higher in boys than girls. For TB BMC and TBLH
BMC, gender differences were found in age groups 12
years and 16–19 years; however, the TBLH BMD was
significantly different between genders [16 years. The
head region accounted for 13–52 and 16–49 % of the TB
BMC in boys and girls, respectively. Furthermore, the
percentages were negatively correlated with age and
height. This study describes a gender-specific reference
database for Chinese children and adolescents aged
5–19 years. These normative values could be used for
clinical assessment in this population.
Keywords Bone mineral density Children DXA 
Normal reference
Introduction
Osteoporosis is increasingly recognized as a common
health problem worldwide. It is generally accepted that
proper development of bone mineral during childhood and
adolescence is a key for skeletal health. Failure to achieve
optimal peak bone mass (PBM) is associated with an
increased risk of osteoporosis and fractures in adulthood
[1]. Pediatric patients with skeletal disorders, such as cystic
fibrosis, inflammatory bowel disease, and type 1 diabetes
mellitus, are associated with low bone mass and increased
risk of fracture [2]. Due to its speed, high precision,
accuracy, safety, low cost, low radiation exposure and
widespread availability, dual-energy X-ray absorptiometry
(DXA) has become the gold standard for measuring bone
mineral density (BMD) and bone mineral content (BMC)
in children and adolescents throughout the world [3].
To evaluate skeletal status in children, the most accurate
and reproducible skeletal sites for performing BMC and
areal BMD measurements in this population are postero-
anterior (PA) spine and total body less head (TBLH) as
recommended by the International Society of Clinical
Densitometry (ISCD) [4]. For BMD reporting, Zscores,
rather than Tscores should be used for this population.
However, Zscores are based on a sample of the general
healthy population sufficiently large enough to characterize
the normal variability in bone measurements that takes into
consideration gender, age, race/ethnicity and other factors
[5] as suggested by the ISCD [6]. Several pediatric nor-
mative databases from different geographies have been
published [7]. To date, there has been no complete study
covering children and adolescents in the Chinese
B. Guo J. Gong Y. Tang H. Xu (&)
Department of Nuclear Medicine, First Affiliated Hospital,
Jinan University, No. 613 West Huangpu Road, Guangzhou
510630, China
e-mail: txh@jnu.edu.cn
Y. Xu
Department of Clinical Medicine, Medical College,
Jinan University, Guangzhou 510630, China
123
J Bone Miner Metab (2013) 31:304–314
DOI 10.1007/s00774-012-0401-1

population. We have previously reported DXA normative
data for children aged 5–13 years based on data from 505
boys and 372 girls [8]; however, a broader range of sub-
jects are needed.
In this study, we report age- and sex-specific means and
standard deviations (SDs) for BMC and BMD of the total
body (TB) and the TBLH in Chinese children and ado-
lescents aged 5–19 years using the Lunar Prodigy DXA
system (GE Healthcare, Madison, WI, USA). This data
could provide researchers and clinicians with appropriate
information to evaluate the bone status in Chinese children
and adolescents.
Materials and methods
Healthy subjects
A total of 1,541 healthy school children (777 boys, 764
girls) were recruited from 4 local schools in Guangzhou
district and 1 school in Jiaxing district in southern China.
The age range was 5.0–19.9 years for both boys and girls.
All participating children were of Chinese ethnicity.
Participants included in the study were between 3rd and
97th percentile for height and weight on current growth
reference curves [9,10]. Children were excluded from the
study if they had (1) a history of metabolic disease or
other medical disorders affecting bone growth and
metabolism; (2) a history of use of medications affecting
bone growth and metabolism; and (3) a history of frac-
ture. Informed consent was obtained from all participants
and their parents. This study was approved by the Ethics
Committee of the First Affiliated Hospital, Jinan
University.
Anthropometric and DXA measurements
Anthropometric and DXA measurements were obtained for
the children and adolescents during the same visit. Weight
was measured using platform digital scales with a precision
of 0.1 kg, and height was recorded with a stadiometer to
the nearest 0.1 cm. TB composition including BMC, lean
mass (LM) and fat mass (FM) was measured with a Lunar
Prodigy DXA bone densitometer (GE Healthcare), and data
were analyzed using enCORE software (ver. 10.0, stan-
dard-array mode). DXA measured parameters included
BMD, BMC, and BA. The TBLH variables were deter-
mined with the head region of interest removed from
analysis. The precision for TB BMD was 0.5 % (expressed
as the root-mean-square percent coefficient of variation),
determined by duplicate scans with repositioning between
each measurement in 30 volunteer subjects. Daily quality
assurance scan was conducted by scanning an aluminum
spine phantom according to the manufacturer’s instruc-
tions. All DXA measurements were performed by a well-
trained technologist throughout the study.
Statistical analysis
Descriptive statistics were used to analyze baseline
characteristics and measurements. Paired-sample ttests
were performed to compare the BMD of the TB and the
TBLH for each gender and age group. Two sample ttests
were used to find possible differences in various param-
eters between boys and girls of the same age group.
Pearson’s correlation coefficients (r) were calculated to
assess correlations among different variables. The height-
for-age, height-for-BA, and BMC-for-BA percentile
curves (3rd, 25th, 50th, 75th, and 97th) were developed
by using the least mean square (LMS) method as
described by Cole and Green [11]. The LMS method
summarizes the changing distribution by 3 curves repre-
senting the median (M), coefficient of variation (S), and
the skewness (L) expressed as a Box-Cox power. These 3
values were estimated, and the curves were calculated
using the formula:
Measurement percentile ¼Mð1þLSZÞ1=L
where Zis the Zscore corresponding to a given percentile.
The percentile curves were constructed using the lms-
ChartMaker program (ver. 2.3; Medical Research Council,
UK). All the tests were 2-tailed, and a pvalue of\0.05 was
considered statistically significant.
Results
Table 1summarizes the baseline characteristics of the
participating subjects. Bone measurements (i.e., BMD,
BMC, and BA) of the subjects are shown in Tables 2and 3.
TB BMD and TBLH BMD were highly correlated
(r=0.762–0.981 in boys, r=0.758–0.968 in girls,
p\0.001) for each age group in Table 4. After 18 years,
TB BMD was significantly higher in boys than girls. For
TB BMC, significant gender differences were found in age
groups 12 years and 16–19 years; the gender differences in
these age groups were also observed for TBLH BMC.
However, the TBLH BMD was significantly different
between genders from age 16 onwards. Tables 5and 6
present the percentile distribution of BMD of the TB and
subcranial skeleton. The percentile distribution of TB and
subcranial skeleton BMC is shown in Tables 7and 8.
The head region accounted for 13–52 and 16–49 % of
the TB BMC in boys and girls for each age group,
respectively. Furthermore, the percentages were negatively
correlated with age (r=-0.895 in boys, r=-0.819 in
J Bone Miner Metab (2013) 31:304–314 305
123

Table 1 Baseline characteristics of the participating subjects by gender and age group [mean (SD)]
Age nBoys nGirls
Age (years) Height (cm) Weight (kg) BMI (kg/m
2
) LM (kg) FM (kg) Age (years) Height (cm) Weight (kg) BMI (kg/m
2
) LM (kg) FM (kg)
5 66 5.4 (0.3) 113.8 (4.9) 19.0 (2.9)
a
14.6 (1.9) 15.6 (1.6)
c
2.4 (1.5) 63 5.4 (0.3) 112.9 (5.6) 17.9 (2.7) 14.0 (1.7) 14.3 (1.7) 2.5 (1.1)
6 85 6.3 (0.3) 117.5 (5.5) 20.6 (3.5)
a
14.8 (1.7)
a
16.9 (2.1)
c
2.5 (1.6)
a
68 6.4 (0.3) 117.1 (4.5) 19.9 (3.1) 14.5 (1.6) 15.5 (1.6) 3.1 (1.6)
7 36 7.3 (0.3) 122.3 (6.3) 23.5 (3.8)
a
15.6 (1.4)
a
18.4 (2.1)
c
3.1 (2.0) 41 7.4 (0.2) 121.1 (7.5) 21.6 (3.0) 14.8 (1.7) 16.7 (1.6) 3.3 (1.7)
8 66 8.6 (0.3) 127.9 (0.6) 25.5 (3.7) 15.5 (1.7) 20.5 (1.9)
b
3.1 (1.9)
b
62 8.5 (0.3) 128.5 (6.6) 25.4 (5.6) 15.3 (2.4) 19.2 (2.2) 3.3 (1.6)
9 68 9.4 (0.3) 131.9 (5.2) 27.3 (6.3) 15.6 (2.8)
a
21.7 (2.4) 4.6 (4.3) 51 9.5 (0.3) 131.4 (6.0) 25.9 (3.7) 15.0 (1.4) 19.8 (2.3) 4.4 (1.8)
10 91 10.5 (0.3) 137.8 (7.6)
a
30.8 (6.3)
a
16.1 (2.1)
c
23.7 (3.1)
b
5.5 (3.6) 71 10.4 (0.3) 138.6 (6.9) 28.9 (4.7) 14.9 (1.9) 22.2 (3.0) 4.9 (2.1)
11 70 11.3 (0.3) 143.0 (6.9) 33.7 (7.3) 16.3 (2.5) 25.8 (3.8) 5.9 (4.0) 61 11.4 (0.3) 145.7 (7.6) 34.4 (6.9) 16.1 (2.3) 25.5 (3.6) 6.6 (3.2)
12 55 12.4 (0.3) 145.6 (8.2)
a
35.3 (8.2) 16.5 (2.6) 27.6 (4.7) 6.5 (4.7) 41 12.4 (0.3) 149.5 (6.2) 36.2 (6.2) 16.1 (2.0) 27.6 (3.5) 7.3 (3.4)
13 28 13.4 (0.3) 153.5 (9.1) 39.5 (4.2) 16.7 (2.3) 32.4 (6.1) 5.6 (3.7)
b
26 13.5 (0.3) 155.8 (7.5) 41.7 (7.1) 17.1 (1.9) 31.4 (3.9) 8.7 (3.9)
14 41 14.5 (0.3) 165.7 (8.1)
c
49.4 (7.6) 17.9 (1.9) 41.2 (6.6)
c
5.3 (2.8)
c
43 14.4 (0.3) 158.7 (6.0) 47.0 (7.6) 18.6 (2.3) 32.7 (4.3) 11.4 (4.7)
15 34 15.4 (0.2) 166.4 (6.7)
c
52.1 (6.4)
a
18.8 (2.1) 42.7 (4.9)
c
6.8 (3.3)
c
31 15.3 (0.3) 159.4 (5.8) 47.7 (7.5) 18.7 (2.3) 32.5 (4.2) 13.2 (5.4)
16 41 16.6 (0.3) 168.3 (5.4)
c
55.4 (6.3)
c
19.6 (1.9) 45.3 (4.8)
c
6.2 (3.2)
c
38 16.6 (0.3) 157.1 (5.8) 49.4 (6.6) 20.0 (2.4) 32.1 (3.4) 14.0 (4.5)
17 39 17.5 (0.3) 168.4 (5.0)
c
56.2 (7.0)
c
19.8 (2.1) 45.5 (5.3)
c
7.0 (3.0)
c
72 17.5 (0.3) 157.1 (6.2) 48.5 (7.2) 19.6 (2.4) 32.0 (3.5) 13.4 (3.8)
18 38 18.2 (0.2) 169.5 (4.2)
c
57.0 (6.3)
c
19.8 (2.3) 46.5 (4.3)
c
6.6 (4.5)
c
55 18.3 (0.3) 157.5 (5.3) 48.4 (6.6) 19.5 (2.0) 32.2 (4.9) 12.9 (3.4)
19 19 19.4 (0.3) 172.1 (6.1)
c
60.1 (8.8)
c
20.2 (2.3) 46.9 (4.0)
c
9.6 (5.4)
b
41 19.6 (0.3) 159.5 (7.2) 50.2 (7.7) 19.7 (2.3) 32.9 (3.8) 14.2 (5.5)
BMI body mass index, SD standard deviation, LM lean mass, FM fat mass
a
p\0.05,
b
p\0.01,
c
p\0.001 compared with girls of the same age group (unpaired-sample ttests)
306 J Bone Miner Metab (2013) 31:304–314
123

girls, p\0.001) and height (r=-0.875 in boys,
r=-0.929 in girls, p\0.001).
The gender-specific height-for-age and height-for-BA
percentile curves are displayed in Fig. 1. In general, the
percentile curves for the 2 genders were similar in shape.
The BA-dependent percentile curves for BMC (Fig. 2)
showed that BMC was closely associated with BA for both
TB and TBLH.
Table 2 BMD, BMC, and BA of total body by gender and age group [mean (SD)]
Age nBoys nGirls
BMD (g/cm
2
) BMC (g) BA (cm
2
) BMD (g/cm
2
) BMC (g) BA (cm
2
)
5 66 0.767 (0.048) 631.05 (96.83) 819.43 (92.42)
a
63 0.761 (0.040) 599.45 (86.92) 785.98 (89.65)
6 85 0.786 (0.045) 698.41 (121.12) 884.37 (116.36) 68 0.778 (0.040) 664.06 (107.28) 850.77 (103.94)
7 36 0.796 (0.049) 770.48 (138.39) 964.04 (137.13) 41 0.797 (0.041) 745.02 (122.66) 930.83 (116.79)
8 66 0.815 (0.041) 869.55 (120.84) 1064.58 (117.64) 62 0.810 (0.049) 862.83 (160.70) 1059.63 (149.57)
9 68 0.817 (0.047) 932.71 (155.85) 1136.91 (145.94) 51 0.817 (0.053) 909.36 (157.38) 1107.50 (134.76)
10 91 0.841 (0.046) 1061.12 (174.92) 1255.84 (156.22) 71 0.830 (0.049) 1013.65 (179.80) 1215.26 (161.47)
11 70 0.869 (0.057) 1199.16 (215.10) 1373.00 (181.18) 61 0.872 (0.056) 1215.02 (219.09) 1387.19 (188.15)
12 55 0.864 (0.053) 1224.16 (244.02)
a
1409.07 (211.92) 41 0.889 (0.070) 1333.02 (250.38) 1490.35 (185.55)
13 28 0.896 (0.058) 1415.66 (257.94) 1571.98 (211.91) 26 0.925 (0.077) 1538.22 (282.12) 1653.78 (206.47)
14 41 0.975 (0.098) 1921.20 (437.81) 1948.6 (277.59)
a
43 1.008 (0.087) 1862.99 (354.58) 1835.50 (216.77)
15 34 1.004 (0.084) 2032.87 (367.44) 2011.48 (216.24)
a
31 1.025 (0.072) 1943.84 (312.03) 1888.67 (202.24)
16 41 1.070 (0.074) 2307.24 (327.72)
c
2146.10 (185.26)
c
38 1.048 (0.080) 1964.39 (295.05) 1867.08 (177.74)
17 39 1.070 (0.077) 2338.91 (315.51)
c
2178.78 (173.76)
c
72 1.047 (0.078) 1970.83 (299.99) 1875.64 (188.99)
18 38 1.114 (0.112)
b
2473.95 (418.15)
c
2207.39 (167.34)
c
55 1.059 (0.083) 2010.35 (320.38) 1888.98 (176.19)
19 19 1.122 (0.048)
b
2546.93 (327.44)
c
2264.10 (219.77)
c
41 1.055 (0.082) 2042.86 (354.43) 1927.26 (233.91)
BMD bone mineral density, BMC bone mineral content, BA bone area, SD standard deviation
a
p\0.05,
b
p\0.01,
c
p\0.001 compared with girls of the same age group (unpaired-sample ttests)
Table 3 BMD, BMC, and BA of TBLH by gender and age group [mean (SD)]
Age nBoys nGirls
BMD (g/cm
2
) BMC (g) BA (cm
2
) BMD (g/cm
2
) BMC (g) BA (cm
2
)
5 66 0.598 (0.039) 366.10 (72.63) 607.66 (86.91) 63 0.594 (0.037) 349.40 (68.40) 584.01 (83.04)
6 85 0.621 (0.046) 420.00 (96.93) 669.51 (109.30) 68 0.617 (0.039) 400.87 (84.66) 644.98 (97.02)
7 36 0.637 (0.044) 478.95 (112.39) 744.89 (127.57) 41 0.642 (0.035) 466.65 (92.92) 722.44 (108.05)
8 66 0.663 (0.037) 561.52 (100.34) 842.24 (114.06) 62 0.672 (0.047) 573.51 (135.51) 845.28 (144.20)
9 68 0.682 (0.046) 629.69 (136.59) 915.29 (141.64) 51 0.685 (0.054) 618.30 (129.85) 894.69 (126.98)
10 91 0.720 (0.052) 745.76 (158.85) 1026.43 (152.48) 71 0.713 (0.053) 717.54 (158.45) 997.26 (153.66)
11 70 0.750 (0.058) 864.05 (193.87) 1141.11 (175.07) 61 0.769 (0.058) 904.99 (202.66) 1166.57 (182.80)
12 55 0.760 (0.063) 907.18 (232.59)
a
1180.36 (208.68)
a
41 0.786 (0.069) 1006.07 (222.30) 1267.71 (182.36)
13 28 0.804 (0.061) 1083.43 (243.66) 1333.85 (203.14) 26 0.824 (0.073) 1187.68 (251.82) 1427.35 (202.10)
14 41 0.904 (0.103) 1566.25 (395.87) 1706.73 (268.63) 43 0.901 (0.076) 1459.74 (297.34) 1607.01 (207.33)
15 34 0.933 (0.081) 1661.59 (324.31) 1766.77 (209.97)
a
31 0.907 (0.069) 1513.70 (281.56) 1658.73 (197.53)
16 41 0.984 (0.077)
c
1885.63 (301.93)
c
1904.63 (182.54)
c
38 0.918 (0.074) 1514.13 (253.86) 1640.47 (169.40)
17 39 0.983 (0.075)
c
1909.12 (287.31)
c
1932.33 (168.37)
c
72 0.914 (0.070) 1514.68 (256.09) 1648.97 (180.87)
18 38 1.025 (0.100)
c
2026.97 (353.29)
c
1964.63 (162.91)
c
55 0.921 (0.080) 1542.57 (282.67) 1663.11 (172.47)
19 19 1.024 (0.050)
c
2069.96 (292.01)
c
2016.05 (212.39)
c
41 0.923 (0.076) 1582.83 (316.62) 1704.40 (229.35)
BMD bone mineral density, BMC bone mineral content, BA bone area, TBLH total body less head, SD standard deviation
a
p\0.05,
b
p\0.01,
c
p\0.001 compared with girls of the same age group (unpaired-sample ttests)
J Bone Miner Metab (2013) 31:304–314 307
123

Discussion
In this study, we presented gender-specific reference data
for Chinese children and adolescents aged 5–19 years. The
percentile curves generated using the LMS method can be
used to determine a child’s percentile rank for whole body
BMC and BMD, similar to evaluating a child’s growth
using height and weight growth charts. In addition, Zscore
could be reported based on the normal reference database
established.
China is a large country of high population migration, so
it is difficult to distinguish differences between southern
and northern Chinese children and adolescents. The sub-
jects were enrolled only from the southern part of China.
No previous reports have shown BMD and BMC differ-
ences between southern and northern Chinese children and
adolescents. A wider range of subjects covering broader
geographic regions may be required. In this study, partic-
ipants were between 3rd and 97th percentile for height and
weight on current standardized growth charts, roughly
consistent with the mean values for Chinese children and
adolescents. Therefore, we believe the data presented can
reflect BMD and BMC reference values for a healthy
population but do not necessarily represent optimal values.
Various studies have reported that ethnic factors are
significant determinants of bone mineral accrual [12–17]
during childhood. Wang et al. [15] reported significant
ethnic differences in bone mass in a cross-sectional study
of 423 Asian, Black, Hispanic, and non-Hispanic White
American youths aged 9–25 years. Boot et al. [12] found
ethnicity had a significant influence on TB BMD in girls,
but not in boys, after studying 500 children and adolescents
aged 4–20 years from various ethnic backgrounds,
including Caucasian, Black and Asian. At most age groups
in our study, boys and girls had significantly lower TB
BMD and BMC compared with children from Poland and
the Netherlands [17,18], but higher TB BMD and BMC as
Table 4 Pearson’s rvalues for the correlations between total body
BMD and TBLH BMD by age group
Age Boys Girls
nr p nr p
5 66 0.762 \0.001 63 0.758 \0.001
6 85 0.824 \0.001 68 0.828 \0.001
7 36 0.772 \0.001 41 0.818 \0.001
8 66 0.823 \0.001 62 0.841 \0.001
9 68 0.833 \0.001 51 0.914 \0.001
10 91 0.867 \0.001 71 0.869 \0.001
11 70 0.860 \0.001 61 0.858 \0.001
12 55 0.886 \0.001 41 0.942 \0.001
13 28 0.877 \0.001 26 0.958 \0.001
14 41 0.981 \0.001 43 0.968 \0.001
15 34 0.974 \0.001 31 0.958 \0.001
16 41 0.970 \0.001 38 0.962 \0.001
17 39 0.937 \0.001 72 0.937 \0.001
18 38 0.978 \0.001 55 0.930 \0.001
19 19 0.934 \0.001 41 0.933 \0.001
nnumber of subjects
Table 5 Percentile distribution of BMD (g/cm
2
) for total body and subcranial skeleton by age group in boys
Age nTotal body Subcranial skeleton
a
Min 3rd 25th 50th 75th 97th Max Min 3rd 25th 50th 75th 97th Max
5 66 0.683 0.686 0.739 0.767 0.798 0.878 0.882 0.519 0.520 0.570 0.595 0.632 0.671 0.689
6 85 0.704 0.710 0.751 0.785 0.816 0.871 0.937 0.505 0.547 0.583 0.616 0.654 0.711 0.740
7 36 0.722 0.722 0.759 0.788 0.831 0.904 0.905 0.560 0.560 0.613 0.630 0.660 0.732 0.732
8 66 0.709 0.729 0.791 0.822 0.841 0.901 0.910 0.580 0.586 0.641 0.669 0.686 0.732 0.766
9 68 0.707 0.716 0.785 0.813 0.850 0.902 0.915 0.599 0.601 0.645 0.684 0.709 0.773 0.793
10 71 0.719 0.739 0.812 0.845 0.875 0.930 0.958 0.593 0.624 0.684 0.716 0.749 0.829 0.838
11 70 0.760 0.764 0.830 0.865 0.913 0.996 1.001 0.636 0.652 0.704 0.742 0.792 0.881 0.895
12 55 0.754 0.774 0.818 0.860 0.900 0.976 0.997 0.647 0.663 0.711 0.743 0.793 0.885 0.896
13 28 0.782 0.782 0.842 0.896 0.945 0.997 0.997 0.715 0.715 0.762 0.789 0.847 0.941 0.941
14 41 0.770 0.778 0.914 0.975 1.044 1.204 1.219 0.689 0.689 0.852 0.907 0.969 1.114 1.121
15 34 0.865 0.865 0.927 1.024 1.072 1.203 1.206 0.778 0.779 0.862 0.939 0.992 1.133 1.137
16 41 0.862 0.871 1.045 1.073 1.108 1.215 1.216 0.768 0.774 0.946 0.986 1.038 1.139 1.142
17 39 0.926 0.93 1.009 1.071 1.138 1.221 1.231 0.841 0.841 0.925 0.986 1.031 1.153 1.158
18 38 0.859 0.868 1.059 1.093 1.206 1.316 1.319 0.836 0.838 0.970 1.006 1.103 1.204 1.205
19 19 1.021 1.021 1.096 1.189 1.164 1.200 1.200 0.935 0.935 0.981 1.029 1.071 1.101 1.101
BMD bone mineral density, ROI region of interest
a
Total body with the head ROI removed from analysis
308 J Bone Miner Metab (2013) 31:304–314
123

Table 6 Percentile distribution of BMD (g/cm
2
) for total body and subcranial skeleton by age group in girls
Age nTotal body Subcranial skeleton
a
Min 3rd 25th 50
th
75th 97th Max Min 3rd 25th 50th 75th 97th Max
5 63 0.651 0.695 0.730 0.756 0.788 0.849 0.855 0.514 0.524 0.567 0.590 0.624 0.672 0.675
6 68 0.672 0.692 0.750 0.779 0.799 0.862 0.876 0.560 0.560 0.587 0.607 0.643 0.707 0.737
7 41 0.711 0.718 0.766 0.793 0.823 0.899 0.909 0.578 0.581 0.612 0.637 0.664 0.725 0.734
8 62 0.713 0.726 0.770 0.819 0.844 0.894 0.916 0.587 0.592 0.632 0.670 0.708 0.762 0.766
9 51 0.705 0.705 0.783 0.824 0.850 0.944 0.961 0.562 0.573 0.650 0.685 0.719 0.791 0.792
10 91 0.719 0.743 0.793 0.823 0.868 0.937 0.955 0.578 0.612 0.673 0.711 0.744 0.822 0.862
11 61 0.753 0.774 0.832 0.870 0.914 0.999 1.033 0.661 0.664 0.730 0.765 0.806 0.929 0.943
12 41 0.765 0.768 0.833 0.891 0.952 1.042 1.044 0.648 0.655 0.731 0.783 0.839 0.942 0.951
13 26 0.747 0.747 0.890 0.920 0.979 1.087 1.087 0.681 0.681 0.787 0.832 0.862 1.001 1.001
14 43 0.810 0.828 0.956 1.007 1.081 1.152 1.155 0.736 0.747 0.852 0.892 0.966 1.025 1.027
15 31 0.887 0.887 0.968 1.009 1.064 1.194 1.194 0.768 0.768 0.861 0.902 0.941 1.108 1.108
16 38 0.895 0.902 0.993 1.035 1.111 1.235 1.243 0.799 0.804 0.862 0.904 0.975 1.117 1.134
17 72 0.895 0.918 0.992 1.045 1.086 1.220 1.267 0.796 1.157 0.797 0.870 0.911 0.959 1.064
18 55 0.909 0.921 1.004 1.049 1.110 1.265 1.286 0.736 0.753 0.863 0.919 0.968 1.136 1.200
19 41 0.862 0.877 0.981 1.073 1.105 1.228 1.237 0.754 0.764 0.865 0.925 0.967 1.085 1.092
BMD bone mineral density, ROI region of interest
a
Total body with the head ROI removed from analysis
J Bone Miner Metab (2013) 31:304–314 309
123

Table 7 Percentile distribution of BMC (g) for total body and subcranial skeleton by age group in boys
Age nTotal body Subcranial skeleton
a
Min 3rd 25th 50th 75th 97th Max Min 3rd 25th 50th 75th 97th Max
5 66 390.49 455.07 559.74 617.47 711.22 812.33 830.61 194.66 243.22 312.12 366.71 416.90 504.88 529.93
6 85 443.32 522.83 600.91 684.15 782.90 9334.56 1076.47 222.64 270.42 340.09 406.74 475.90 629.05 675.03
7 36 556.77 557.39 657.47 748.80 831.65 1137.59 1143.33 301.18 303.78 401.58 453.68 535.70 791.75 796.68
8 66 596.03 637.91 800.57 863.07 943.87 1137.69 1282.26 372.64 382.77 485.39 558.20 624.87 798.68 904.15
9 68 624.38 694.97 801.28 924.81 1060.47 1226.10 1237.82 378.64 432.94 530.36 624.02 712.10 905.17 949.64
10 71 641.63 740.67 925.84 1059.79 1186.60 1429.05 1494.27 395.70 470.32 630.80 736.41 834.15 1092.91 1187.05
11 70 752.52 819.93 1052.59 1147.11 1303.74 1676.17 1725.72 513.84 541.67 712.70 808.35 944.49 1318.42 1352.17
12 55 819.42 881.09 1056.06 1169.97 1388.73 1829.54 1887.11 533.59 602.92 742.99 839.80 1035.52 1475.46 1541.80
13 35 1072.00 1073.49 1190.37 1403.07 1744.58 2139.07 2152.99 708.12 713.65 915.13 1083.23 1367.49 1804.77 1819.59
14 41 1000.62 1022.47 1672.58 1865.65 2191.50 2896.75 2928.52 739.94 741.38 1354.14 1556.06 1800.62 2445.37 2493.67
15 34 1443.55 1443.97 1751.77 1997.66 2342.07 2794.42 2801.06 1128.27 1128.42 1432.90 1638.48 1915.92 2380.50 2387.56
16 41 1378.28 1468.85 2108.64 2290.92 2566.13 2895.22 2903.18 1051.31 1122.31 1674.43 1857.67 2080.34 2425.85 2449.46
17 39 1647.22 1670.42 2096.24 2402.46 2573.19 2957.00 2700.00 1263.62 1290.05 1728.11 1923.02 2070.15 2500.53 2502.00
18 38 1631.19 1653.64 2239.40 2388.02 2774.76 3279.74 3301.48 1395.81 1398.16 1813.57 1920.39 2270.07 2690.80 2691.36
19 19 2033.21 2033.21 2276.61 2547.49 2856.23 3003.69 3003.69 1598.53 1598.53 1821.30 2080.37 2325.11 2488.60 2488.60
BMC bone mineral content, ROI region of interest
a
Total body with the head ROI removed from analysis
310 J Bone Miner Metab (2013) 31:304–314
123

Table 8 Percentile distribution of BMC (g) for total body and subcranial skeleton by age group in girls
Age nTotal body Subcranial skeleton
a
Min 3rd 25th 50th 75th 97th Max Min 3rd 25th 50th 75th 97th Max
5 63 378.14 428.64 538.41 587.28 678.30 774.79 782.37 204.80 221.13 300.45 343.7 404.54 508.95 528.19
6 68 480.36 488.98 588.89 643.94 732.39 901.33 1048.19 247.30 263.06 343.41 384.01 457.65 626.96 705.38
7 41 552.59 558.52 656.45 715.11 813.25 1091.78 1119.02 324.61 330.11 402.72 444.82 531.55 716.65 740.45
8 62 591.67 600.44 747.46 847.97 957.77 1229.49 1303.57 370.04 383.48 479.77 542.69 642.70 867.85 986.04
9 51 525.98 620.09 802.98 905.97 1003.43 1263.25 1296.00 328.53 380.83 529.70 609.60 708.04 895.92 902.90
10 91 606.38 712.59 867.82 992.73 1132.22 1416.06 1559.05 380.22 470.45 584.49 705.24 806.81 1086.55 1219.38
11 61 716.74 772.7 1092.11 1192.46 1338.70 1872.90 2003.92 480.81 546.74 757.87 907.98 1007.35 1534.7 1592.18
12 49 844.99 904.35 1169.7 1320.06 1533.49 2060.16 2118.49 570.51 620.13 857.77 997.01 1225.78 1659.96 1691.83
13 39 960.21 1020.8 1453.62 1623.02 1912.13 2338.67 2347.25 728.57 770.60 1104.53 1289.97 1432.61 1870.92 1874.82
14 43 1302.65 1323.16 1610.53 1784.41 2115.07 2613.13 2655.66 1013.02 1031.23 1261.97 1369.17 1664.67 2135.4 2169.57
15 31 1489.48 1489.48 1717.81 1977.66 2110.77 3004.67 3004.67 1107.92 1107.92 1316.53 1504.26 1674.59 2520.31 2520.31
16 38 1389.60 1420.00 1707.65 1953.01 2183.58 2639.2 2664.90 1053.53 1068.37 1304.67 1486.24 1688.10 2135.52 2161.79
17 72 1342.27 1510.5 1781.31 1913.47 2121.09 2721.95 2778.32 1060.97 1117.79 1356.98 1462.61 1624.84 2212.90 2260.74
18 55 1457.1 1523.75 1779.48 1929.71 2164.15 2936.21 2960.63 1008.49 1063.28 1349.45 1519.65 1678.03 2425.76 2463.78
19 41 1345.41 1384.74 1789.13 2024.54 2446.10 2859.37 2897.73 954.77 993.79 1360.21 1540.62 1745.73 2324.81 2363.14
BMC bone mineral content, ROI region of interest
a
Total body with the head ROI removed from analysis
J Bone Miner Metab (2013) 31:304–314 311
123

compared to children from India [19]. It is generally
accepted that different normal reference curves for differ-
ent ethnic background are necessary for the accurate rep-
resentation of specific ethnic group.
A significant increase in BMC/BMD for TB and TBLH
was found during growth. Our findings are similar to those
in other studies [8,20–27]. Reports of gender difference in
BMD and BMC during childhood and adolescents are
largely inconsistent [22,24,28]. In our study, we found
significant gender differences starting at 18 years of age in
TB BMD, and 16 years of age in TBLH BMD. Girls have
higher BMC in TB and TBLH than boys in the 12-15 age
group, and boys have higher BMC in TB and TBLH from
16 years of age onwards. These results may reflect a dif-
ference in age of onset of puberty in males and females,
and the later increased height in males. In a cross-sectional
study, Zanchetta et al. [22] found gender difference con-
cerning TB BMC maximum mean value in Argentinian
children (2–20 years) starting at age 16, and becoming
significant at age 17. In a study of Canadian children aged
8–17 years, Faulkner et al. [24] found no gender differ-
ences until age 16 for TB BMD and age 14 for BMC.
Maynard et al. [28] reported that significant sex difference
were found at 15–18 years in TB BMC and 16–18 years in
TB BMD in White children. In general, the normal refer-
ence database for pediatric DXA should be gender-specific.
The influence of head in TB BMD and BMC needs to be
taken into consideration when assessing bone density in
growing children. There is growing evidence that TBLH
measurements should be the standard when assessing TB
bone. Various studies have already published a pediatric
BMC and BMD normative database excluding the head
region [23,27,29,30]. Willing et al. [29] revealed that the
BMC of the head comprised a greater percentage of whole
body BMC in small children compared to taller children.
Taylor et al. [30] showed that in normal children aged
2–9 years, TBLH BMD was better predicted by age than
TB BMD and that head BMD accounted for most of the
variance in TB BMD and age accounted for \50 % of the
variance in the head BMD. The results of our study further
verified the contribution of the head region in TB BMD and
BMC. TBLH BMD may be a better parameter than TB
BMD in terms of explaining the real skeletal status for
children and adolescents.
DXA measurements are 2-dimensional and BMD is an
areal (g/cm
2
) rather than a volumetric bone density. BMD
Fig. 1 Height percentile curves
adjusted for age and bone area
(BA) percentile curves adjusted
for height. Solid lines from the
upper one represent the 97th,
75th, 50th, 25th, and 3rd
percentiles
312 J Bone Miner Metab (2013) 31:304–314
123

is affected by the subject’s size, and tends to underestimate
bone density in small subjects and overestimate in larger
subjects [31]. Various approaches could correct the size
effects. Molgaard recommended a 3-step method to adjust
height-for-age, bone area (BA)-for-height, and BMC-for-
BA, to discriminate 3 possible clinical situations in which a
low bone mass may occur as ‘short’ bones, ‘narrow’ bones,
and ‘light’ bones [32]. In our study, we adopted the method
of Molgaard et al. to develop percentile curves for bone
size and BMC for use in addition to normative DXA data.
Our study might have some limitations related to study
design. First of all, it was a cross-sectional study and
longitudinal data need to be obtained. Secondly, other
limitations should be pointed out concerning DXA. DXA
devices from different manufacturers might not give
identical results, due to differences in scan modes, software
version [33], and the calibration methods adopted by dif-
ferent DXA manufacturers [34,35]. Our reference data is
limited only to results derived from the Lunar Prodigy
DXA densitometer. In addition, attention should be paid
when using provided normative values due to the potential
differences in genetic, nutrition, and physical activities
between the population being assessed and the population
used to establish such normative values.
This study describes complete DXA TB normal refer-
ence data for Chinese children and adolescents aged
5–19 years. The results of this study may be used to
establish a normal reference database and can be used in
assessment of children and adolescents with bone disorders
in China.
Acknowledgments The authors would like to express their grati-
tude to all participating children and their parents. We are grateful to
Dr Qi Zhou, GE Healthcare Shanghai and Dr Jing Xiang, First
Hospital of Jiaxing for their useful comments and suggestions. We
also thank the staff members of the Department of Nuclear Medicine,
First Affiliated Hospital of Jinan University for excellent technical
support.
Conflict of interest None of the authors have any personal or
financial conflicts of interest.
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