J Bone Miner Metab (2013) 31:304–314 DOI 10.1007/s00774-012-0401-1
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 Ó The 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 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. 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:
[email protected] Y. Xu Department of Clinical Medicine, Medical College, Jinan University, Guangzhou 510630, China
123
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 posteroanterior (PA) spine and total body less head (TBLH) as recommended by the International Society of Clinical Densitometry (ISCD) [4]. For BMD reporting, Z scores, rather than T scores should be used for this population. However, Z scores 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 normative databases from different geographies have been published [7]. To date, there has been no complete study covering children and adolescents in the Chinese
J Bone Miner Metab (2013) 31:304–314
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 subjects 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 adolescents 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 fracture. 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, standard-array mode). DXA measured parameters included BMD, BMC, and BA. The TBLH variables were determined 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
305
spine phantom according to the manufacturer’s instructions. All DXA measurements were performed by a welltrained technologist throughout the study. Statistical analysis Descriptive statistics were used to analyze baseline characteristics and measurements. Paired-sample t tests were performed to compare the BMD of the TB and the TBLH for each gender and age group. Two sample t tests were used to find possible differences in various parameters between boys and girls of the same age group. Pearson’s correlation coefficients (r) were calculated to assess correlations among different variables. The heightfor-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 representing 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 ¼ Mð1 þ LSZÞ1=L where Z is the Z score corresponding to a given percentile. The percentile curves were constructed using the lmsChartMaker program (ver. 2.3; Medical Research Council, UK). All the tests were 2-tailed, and a p value of\0.05 was considered statistically significant.
Results Table 1 summarizes the baseline characteristics of the participating subjects. Bone measurements (i.e., BMD, BMC, and BA) of the subjects are shown in Tables 2 and 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 5 and 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 7 and 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
123
123
66 85
36
66
68
91
70
55
28
41
34
41
39
38
19
5 6
7
8
9
10
11
12
13
14
15
16
17
18
19
19.4 (0.3)
18.2 (0.2)
17.5 (0.3)
16.6 (0.3)
15.4 (0.2)
14.5 (0.3)
13.4 (0.3)
12.4 (0.3)
11.3 (0.3)
10.5 (0.3)
9.4 (0.3)
8.6 (0.3)
7.3 (0.3)
5.4 (0.3) 6.3 (0.3)
Age (years)
Boys
57.0 (6.3)c c
169.5 (4.2)c c
60.1 (8.8)
56.2 (7.0)c
168.4 (5.0)c
172.1 (6.1)
55.4 (6.3)c
168.3 (5.4)c
49.4 (7.6) 52.1 (6.4)a
c
39.5 (4.2)
a
166.4 (6.7)c
165.7 (8.1)
153.5 (9.1)
33.7 (7.3) 35.3 (8.2)
30.8 (6.3)
27.3 (6.3)
145.6 (8.2)a
a
16.3 (2.5)
20.2 (2.3)
19.8 (2.3)
19.8 (2.1)
19.6 (1.9)
18.8 (2.1)
17.9 (1.9)
16.7 (2.3)
16.5 (2.6)
25.8 (3.8)
a
p \ 0.05,
b
c
46.9 (4.0)
9.6 (5.4)
b
6.6 (4.5)c
7.0 (3.0)c
6.2 (3.2)c
6.8 (3.3)c
5.3 (2.8)
41
55
72
38
31
43
26
c
5.6 (3.7)b
61 41
6.5 (4.7)
5.9 (4.0)
71
51
62
41
63 68
n
p \ 0.01, c p \ 0.001 compared with girls of the same age group (unpaired-sample t tests)
c
46.5 (4.3)c
45.5 (5.3)c
45.3 (4.8)c
42.7 (4.9)c
41.2 (6.6)
32.4 (6.1)
27.6 (4.7)
5.5 (3.6)
4.6 (4.3)
21.7 (2.4)
15.6 (2.8)a 23.7 (3.1)b
3.1 (1.9)b
16.1 (2.1)c
3.1 (2.0)
2.4 (1.5) 2.5 (1.6)a
20.5 (1.9)b
15.6 (1.6)c 16.9 (2.1)c
FM (kg)
15.5 (1.7)
15.6 (1.4)a
23.5 (3.8)a 25.5 (3.7)
14.6 (1.9) 14.8 (1.7)a
19.0 (2.9)a 20.6 (3.5)a
LM (kg)
18.4 (2.1)c
BMI (kg/m )
Weight (kg)
143.0 (6.9)
137.8 (7.6)
131.9 (5.2)
127.9 (0.6)
122.3 (6.3)
113.8 (4.9) 117.5 (5.5)
Height (cm)
2
BMI body mass index, SD standard deviation, LM lean mass, FM fat mass
n
Age
Table 1 Baseline characteristics of the participating subjects by gender and age group [mean (SD)]
19.6 (0.3)
18.3 (0.3)
17.5 (0.3)
16.6 (0.3)
15.3 (0.3)
14.4 (0.3)
13.5 (0.3)
12.4 (0.3)
11.4 (0.3)
10.4 (0.3)
9.5 (0.3)
8.5 (0.3)
7.4 (0.2)
5.4 (0.3) 6.4 (0.3)
Age (years)
Girls
159.5 (7.2)
157.5 (5.3)
157.1 (6.2)
157.1 (5.8)
159.4 (5.8)
158.7 (6.0)
155.8 (7.5)
149.5 (6.2)
145.7 (7.6)
138.6 (6.9)
131.4 (6.0)
128.5 (6.6)
121.1 (7.5)
112.9 (5.6) 117.1 (4.5)
Height (cm)
50.2 (7.7)
48.4 (6.6)
48.5 (7.2)
49.4 (6.6)
47.7 (7.5)
47.0 (7.6)
41.7 (7.1)
36.2 (6.2)
34.4 (6.9)
28.9 (4.7)
25.9 (3.7)
25.4 (5.6)
21.6 (3.0)
17.9 (2.7) 19.9 (3.1)
Weight (kg)
19.7 (2.3)
19.5 (2.0)
19.6 (2.4)
20.0 (2.4)
18.7 (2.3)
18.6 (2.3)
17.1 (1.9)
16.1 (2.0)
16.1 (2.3)
14.9 (1.9)
15.0 (1.4)
15.3 (2.4)
14.8 (1.7)
14.0 (1.7) 14.5 (1.6)
BMI (kg/m2)
32.9 (3.8)
32.2 (4.9)
32.0 (3.5)
32.1 (3.4)
32.5 (4.2)
32.7 (4.3)
31.4 (3.9)
27.6 (3.5)
25.5 (3.6)
22.2 (3.0)
19.8 (2.3)
19.2 (2.2)
16.7 (1.6)
14.3 (1.7) 15.5 (1.6)
LM (kg)
14.2 (5.5)
12.9 (3.4)
13.4 (3.8)
14.0 (4.5)
13.2 (5.4)
11.4 (4.7)
8.7 (3.9)
7.3 (3.4)
6.6 (3.2)
4.9 (2.1)
4.4 (1.8)
3.3 (1.6)
3.3 (1.7)
2.5 (1.1) 3.1 (1.6)
FM (kg)
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J Bone Miner Metab (2013) 31:304–314
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Table 2 BMD, BMC, and BA of total body by gender and age group [mean (SD)] Age
n
Boys
n 2
BMD (g/cm )
2
BMC (g)
Girls BMD (g/cm2)
BA (cm )
BMC (g)
BA (cm2)
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 12
70 55
0.869 (0.057) 0.864 (0.053)
1199.16 (215.10) 1224.16 (244.02)a
1373.00 (181.18) 1409.07 (211.92)
61 41
0.872 (0.056) 0.889 (0.070)
1215.02 (219.09) 1333.02 (250.38)
1387.19 (188.15) 1490.35 (185.55)
13
28
0.896 (0.058)
1415.66 (257.94)
1571.98 (211.91)
14
41
0.975 (0.098)
1921.20 (437.81)
15
34
1.004 (0.084)
2032.87 (367.44)
26
0.925 (0.077)
1538.22 (282.12)
1653.78 (206.47)
1948.6 (277.59)a
43
1.008 (0.087)
1862.99 (354.58)
1835.50 (216.77)
2011.48 (216.24)a
31
1.025 (0.072)
1943.84 (312.03)
1888.67 (202.24)
c
2146.10 (185.26)c
38
1.048 (0.080)
1964.39 (295.05)
1867.08 (177.74)
16
41
1.070 (0.074)
2307.24 (327.72)
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)
c
c
55
1.059 (0.083)
2010.35 (320.38)
1888.98 (176.19)
2264.10 (219.77)c
41
1.055 (0.082)
2042.86 (354.43)
1927.26 (233.91)
b
18
38
1.114 (0.112)
19
19
1.122 (0.048)b
2473.95 (418.15)
2546.93 (327.44)c
2207.39 (167.34)
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 t tests)
Table 3 BMD, BMC, and BA of TBLH by gender and age group [mean (SD)] Age
n
Boys
n 2
BMD (g/cm )
BMC (g)
2
Girls BMD (g/cm2)
BA (cm )
BMC (g)
BA (cm2)
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 12
70 55
0.750 (0.058) 0.760 (0.063)
864.05 (193.87) 907.18 (232.59)a
1141.11 (175.07) 1180.36 (208.68)a
61 41
0.769 (0.058) 0.786 (0.069)
904.99 (202.66) 1006.07 (222.30)
1166.57 (182.80) 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)
a
15
34
0.933 (0.081)
1661.59 (324.31)
1766.77 (209.97)
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 t tests)
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.
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J Bone Miner Metab (2013) 31:304–314
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 Table 4 Pearson’s r values for the correlations between total body BMD and TBLH BMD by age group Age
Boys
Girls
n
r
p
n
r
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 11
91 70
0.867 0.860
\0.001 \0.001
71 61
0.869 0.858
\0.001 \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
n number of subjects
using height and weight growth charts. In addition, Z score 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 subjects were enrolled only from the southern part of China. No previous reports have shown BMD and BMC differences between southern and northern Chinese children and adolescents. A wider range of subjects covering broader geographic regions may be required. In this study, participants 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 5 Percentile distribution of BMD (g/cm2) for total body and subcranial skeleton by age group in boys Age
n
Subcranial skeletona
Total body 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
123
63
68
41
62
51
91
61
41
26
43
31 38
72
55
41
5
6
7
8
9
10
11
12
13
14
15 16
17
18
19
0.862
0.909
0.895
0.887 0.895
0.810
0.747
0.765
0.753
0.719
0.705
0.713
0.711
0.672
0.651
Min
Total body
0.877
0.921
0.918
0.887 0.902
0.828
0.747
0.768
0.774
0.743
0.705
0.726
0.718
0.692
0.695
3rd
0.981
1.004
0.992
0.968 0.993
0.956
0.890
0.833
0.832
0.793
0.783
0.770
0.766
0.750
0.730
25th
a
Total body with the head ROI removed from analysis
BMD bone mineral density, ROI region of interest
n
Age
1.073
1.049
1.045
1.009 1.035
1.007
0.920
0.891
0.870
0.823
0.824
0.819
0.793
0.779
0.756
50th
1.105
1.110
1.086
1.064 1.111
1.081
0.979
0.952
0.914
0.868
0.850
0.844
0.823
0.799
0.788
75th
1.228
1.265
1.220
1.194 1.235
1.152
1.087
1.042
0.999
0.937
0.944
0.894
0.899
0.862
0.849
97th
1.237
1.286
1.267
1.194 1.243
1.155
1.087
1.044
1.033
0.955
0.961
0.916
0.909
0.876
0.855
Max
0.754
0.736
0.796
0.768 0.799
0.736
0.681
0.648
0.661
0.578
0.562
0.587
0.578
0.560
0.514
Min
0.764
0.753
1.157
0.768 0.804
0.747
0.681
0.655
0.664
0.612
0.573
0.592
0.581
0.560
0.524
3rd
Subcranial skeletona
Table 6 Percentile distribution of BMD (g/cm2) for total body and subcranial skeleton by age group in girls
0.865
0.863
0.797
0.861 0.862
0.852
0.787
0.731
0.730
0.673
0.650
0.632
0.612
0.587
0.567
25th
0.925
0.919
0.870
0.902 0.904
0.892
0.832
0.783
0.765
0.711
0.685
0.670
0.637
0.607
0.590
50th
0.967
0.968
0.911
0.941 0.975
0.966
0.862
0.839
0.806
0.744
0.719
0.708
0.664
0.643
0.624
75th
1.085
1.136
0.959
1.108 1.117
1.025
1.001
0.942
0.929
0.822
0.791
0.762
0.725
0.707
0.672
97th
1.092
1.200
1.064
1.108 1.134
1.027
1.001
0.951
0.943
0.862
0.792
0.766
0.734
0.737
0.675
Max
J Bone Miner Metab (2013) 31:304–314 309
123
123
66 85
36
66
68
71
70
55
35
41
34
41
39
38
19
5 6
7
8
9
10
11
12
13
14
15
16
17
18
19
2033.21
1631.19
1647.22
1378.28
1443.55
1000.62
1072.00
819.42
752.52
641.63
624.38
596.03
556.77
390.49 443.32
2033.21
1653.64
1670.42
1468.85
1443.97
1022.47
1073.49
881.09
819.93
740.67
694.97
637.91
557.39
455.07 522.83
2276.61
2239.40
2096.24
2108.64
1751.77
1672.58
1190.37
1056.06
1052.59
925.84
801.28
800.57
657.47
559.74 600.91
a
Total body with the head ROI removed from analysis
2547.49
2388.02
2402.46
2290.92
1997.66
1865.65
1403.07
1169.97
1147.11
1059.79
924.81
863.07
748.80
617.47 684.15
50th
2856.23
2774.76
2573.19
2566.13
2342.07
2191.50
1744.58
1388.73
1303.74
1186.60
1060.47
943.87
831.65
711.22 782.90
75th
3003.69
3279.74
2957.00
2895.22
2794.42
2896.75
2139.07
1829.54
1676.17
1429.05
1226.10
1137.69
1137.59
812.33 9334.56
97th
3003.69
3301.48
2700.00
2903.18
2801.06
2928.52
2152.99
1887.11
1725.72
1494.27
1237.82
1282.26
1143.33
830.61 1076.47
Max
1598.53
1395.81
1263.62
1051.31
1128.27
739.94
708.12
533.59
513.84
395.70
378.64
372.64
301.18
194.66 222.64
1598.53
1398.16
1290.05
1122.31
1128.42
741.38
713.65
602.92
541.67
470.32
432.94
382.77
303.78
243.22 270.42
3rd
Min
25th
Min
3rd
Subcranial skeletona
Total body
BMC bone mineral content, ROI region of interest
n
Age
Table 7 Percentile distribution of BMC (g) for total body and subcranial skeleton by age group in boys
1821.30
1813.57
1728.11
1674.43
1432.90
1354.14
915.13
742.99
712.70
630.80
530.36
485.39
401.58
312.12 340.09
25th
2080.37
1920.39
1923.02
1857.67
1638.48
1556.06
1083.23
839.80
808.35
736.41
624.02
558.20
453.68
366.71 406.74
50th
2325.11
2270.07
2070.15
2080.34
1915.92
1800.62
1367.49
1035.52
944.49
834.15
712.10
624.87
535.70
416.90 475.90
75th
2488.60
2690.80
2500.53
2425.85
2380.50
2445.37
1804.77
1475.46
1318.42
1092.91
905.17
798.68
791.75
504.88 629.05
97th
2488.60
2691.36
2502.00
2449.46
2387.56
2493.67
1819.59
1541.80
1352.17
1187.05
949.64
904.15
796.68
529.93 675.03
Max
310 J Bone Miner Metab (2013) 31:304–314
63 68
41
62
51
91
61
49
39
43
31
38
72
55
41
5 6
7
8
9
10
11
12
13
14
15
16
17
18
19
1345.41
1457.1
1342.27
1389.60
1489.48
1302.65
960.21
844.99
716.74
606.38
525.98
591.67
552.59
378.14 480.36
1384.74
1523.75
1510.5
1420.00
1489.48
1323.16
1020.8
904.35
772.7
712.59
620.09
600.44
558.52
428.64 488.98
1789.13
1779.48
1781.31
1707.65
1717.81
1610.53
1453.62
1169.7
1092.11
867.82
802.98
747.46
656.45
538.41 588.89
a
Total body with the head ROI removed from analysis
2024.54
1929.71
1913.47
1953.01
1977.66
1784.41
1623.02
1320.06
1192.46
992.73
905.97
847.97
715.11
587.28 643.94
50th
2446.10
2164.15
2121.09
2183.58
2110.77
2115.07
1912.13
1533.49
1338.70
1132.22
1003.43
957.77
813.25
678.30 732.39
75th
2859.37
2936.21
2721.95
2639.2
3004.67
2613.13
2338.67
2060.16
1872.90
1416.06
1263.25
1229.49
1091.78
774.79 901.33
97th
2897.73
2960.63
2778.32
2664.90
3004.67
2655.66
2347.25
2118.49
2003.92
1559.05
1296.00
1303.57
1119.02
782.37 1048.19
Max
954.77
1008.49
1060.97
1053.53
1107.92
1013.02
728.57
570.51
480.81
380.22
328.53
370.04
324.61
204.80 247.30
993.79
1063.28
1117.79
1068.37
1107.92
1031.23
770.60
620.13
546.74
470.45
380.83
383.48
330.11
221.13 263.06
3rd
Min
25th
Min
3rd
Subcranial skeletona
Total body
BMC bone mineral content, ROI region of interest
n
Age
Table 8 Percentile distribution of BMC (g) for total body and subcranial skeleton by age group in girls
1360.21
1349.45
1356.98
1304.67
1316.53
1261.97
1104.53
857.77
757.87
584.49
529.70
479.77
402.72
300.45 343.41
25th
1540.62
1519.65
1462.61
1486.24
1504.26
1369.17
1289.97
997.01
907.98
705.24
609.60
542.69
444.82
343.7 384.01
50th
1745.73
1678.03
1624.84
1688.10
1674.59
1664.67
1432.61
1225.78
1007.35
806.81
708.04
642.70
531.55
404.54 457.65
75th
2324.81
2425.76
2212.90
2135.52
2520.31
2135.4
1870.92
1659.96
1534.7
1086.55
895.92
867.85
716.65
508.95 626.96
97th
2363.14
2463.78
2260.74
2161.79
2520.31
2169.57
1874.82
1691.83
1592.18
1219.38
902.90
986.04
740.45
528.19 705.38
Max
J Bone Miner Metab (2013) 31:304–314 311
123
312
J Bone Miner Metab (2013) 31:304–314
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
compared to children from India [19]. It is generally accepted that different normal reference curves for different ethnic background are necessary for the accurate representation 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 difference 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 concerning 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 differences until age 16 for TB BMD and age 14 for BMC. Maynard et al. [28] reported that significant sex difference
123
were found at 15–18 years in TB BMC and 16–18 years in TB BMD in White children. In general, the normal reference 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/cm2) rather than a volumetric bone density. BMD
J Bone Miner Metab (2013) 31:304–314
313
Fig. 2 Bone mineral content (BMC) percentile curves adjusted for bone area (BA). Solid lines from the upper one represent the 97th, 75th, 50th, 25th, and 3rd percentiles
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-forBA, 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 different 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 reference 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 gratitude 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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