Journal of Clinical Densitometry
Volume 9, Issue 1 , Pages 84-90, January 2006

Bone Mineral Density of Healthy Turkish Children and Adolescents

  • Damla Goksen

      Affiliations

    • Ege University Faculty of Medicine Department of Pediatric Endocrinology and Metabolism, Bornova/İzmir, Turkey
    • Corresponding Author InformationAddress correspondece to: Damla Goksen, Mithatpaşa cad No 1114/5, Güzelyalı/İzmir 35290 Turkey.
    • ,
  • Sukran Darcan

      Affiliations

    • Ege University Faculty of Medicine Department of Pediatric Endocrinology and Metabolism, Bornova/İzmir, Turkey
    • ,
  • Mahmut Coker

      Affiliations

    • Ege University Faculty of Medicine Department of Pediatric Endocrinology and Metabolism, Bornova/İzmir, Turkey
    • ,
  • Timur Kose

      Affiliations

    • Ege University Faculty of Computer Engineering, Bornova/İzmir, Turkey

Received 28 March 2005; received in revised form 21 June 2005 and 10 August 2005; accepted 10 August 2005.

Article Outline

Abstract 

The objective of this article is to gain reference values of lumbar and femoral neck bone mineral density (BMD) for healthy Turkish children. Three hundred forty-five children aged 2–18 years were examined. Weight and height development were normal for age according to national growth charts. Areal BMD (aBMD) was corrected using the model of Kroger et al (9). The results of the lumbar and femoral aBMD increased progressively from childhood to adulthood. Statistically significant correlation was found between lumbar and femoral neck aBMD and age and height (p<0.01). Lumbar volumetric (vBMD) data were similar between males and females. Femoral vBMD was only significantly different at the ages of 8 and 16 (p<0.05) in girls and boys and did not increase with age. A significant increase in aBMD L1–L4 values according to puberty was observed between all Tanner stages, except Tanner stages 3 and 4 (p>0.05). A significant difference was found between stages 1 and 2, and 2 and 3 in femoral neck aBMD (p<0.05). This data provides a tool for the investigation and follow-up of Turkish children at risk for low-bone mineralization.

Key Words: Areal bone mineral density (aBMD), volumetric bone mineral density (vBMD), children, adolescents

 

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Introduction 

During childhood and adolescence, bone mineral density (BMD) increases until peak bone mass is reached. Age, weight, height, pubertal status, nutrition, physical activity level, and ethnicity are the factors that influence peak bone mass and BMD 1, 2. Dual energy X-ray absorptiometry (DXA) is the method of choice to measure BMD allowing rapid assessment of low radiation dose with high precision and accuracy.

In physical terms, bone mass depends on the size and the density of skeletal bone. It is not possible to measure true bone density by DXA because it measures only the cross-sectional area of the scanned bone. True BMD is a function of the bone mineral content per volume of bone (3). Correction of lumbar BMD for bone volume by the use of mathematical formulations reduces the effect of bone size during growth (4). In some studies it has been shown that volumetric BMD (vBMD) remains dependent on age and bone size during growth, except prior to puberty when femoral neck vBMD is independent of age 5, 6, 7, 8, 9. Studies in healthy children using quantitative computed tomography (QCT) have shown that BMD of cortical bone is not influenced by age, anthropometric parameters, puberty, gender or race; however events during puberty are the major determinants of the increases in the cancellous bone density (10).

In order to assess children and adolescents who are at risk for low bone mass, normative data based on large samples are required (11). Several cross-sectional studies have presented normative data for children and adolescence, but these are limited with small sample size, they are specific to geographic areas, and they use different software programs 5, 11, 12, 13, 14, 15, 16, 17, 18, 19.

The objective of this study was to gain BMD reference values for the lumbar spine and femoral neck of healthy Caucasian Turkish children, and to evaluate the influence of age, nutrition, physical activity, weight, height, and pubertal status on these reference values. This normative BMD data provides information on children as young as 2 years of age that can be used as reference values for children and adolescents based on age and pubertal status using the Hologic QDR 4500A (Hologic, Bedford, MA) in the array mode, which will enable us to treat and follow-up these patients.

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Subjects and Methods 

A total of 345 Caucasian children aged 2–18 years were examined (i.e., 176 girls and 169 boys). The participants were recruited from the primary and secondary schools of İzmir, Turkey. The study protocol was approved by the ethics committee of the Ege University Medical Faculty. Written informed consent was obtained from individual participants if they were of legal adult age and from their parents if they were not.

Children treated with oral corticosteroids, anticonvulsants, or heparin, or who suffered from metabolic bone disease (i.e., those who had a bone age of more or less than 1 standard deviation (SD) from their chronological age, disease of the kidneys or liver, diabetes mellitus, and were small for their gestational age or were premature) were excluded from the study. Participants included in the study were between 10–90 percentile for height and weight according to Neyzi et al (20).

A questionnaire was administered to all subjects to determine calcium and vitamin D intake, physical activity, medical history, low birth weight, and age at onset of puberty. The questions were asked to participants or to one of the parents if the child was less than 12 years of age. A food frequency for the dietary intake of calcium (Ca) was obtained from each participant to estimate daily Ca intake (i.e., daily milk and milk product consumption of each child was asked, and Ca intake other than daily products, which is 250 mg/day for each child was added; Table 1) (21). Physical activity included physical classes and organized sports measured in min/wk in school-age children. In preschool-age children, organized sports were accepted as physical activity.

Table 1. Estimated Calcium Intake From Dairy Products
Milk8 oz300 mg
Yogurt8 oz300 mg
Cheese1 oz200 mg

Height was measured without shoes with a wall mounted Harpenden stadiometer (Holtain LTd., Crymych, UK). Weight was measured without shoes on a standard balance nearest to 0.1 kg. Pubertal development was evaluated according to the method of Tanner (22), and bone age according to Greulich and Pyle (23) by the same pediatric endocrinologist in every child.

The BMD (gr/cm2) of the lumbar spine and femoral neck was measured with dual energy X-ray absorptiometry (Hologic QDR 4500A Fan Beam X-ray Bone Densitometer, Hologic, Bedford, MA). During measurement of the lumbar spine, the child was supine and physiological lumbar lordosis was flattened by elevation of the knees. For femoral neck positioning, the manufacturer's standards were used. All measurements were performed and analyzed by the same person. This measurement was an areal density that varied with bone size. Bone volume was calculated based on the 2-dimensional DXA measurements on L1–L4 and the femoral neck. To calculate vBMD of the lumbar spine and femoral neck, the mathematical model of Kroger et al (9) was used, which assumed the lumbar body and femoral neck as having a cylindrical shape (9). The volume of the femoral neck is=Π×(radius of femoral neck)2×height of measured area in femoral neck =Π×(area of the femoral neck from the scan projection =2r×h)2/4 height of measured area in femoral neck. So vBMD is: BMD×(4/[Π×height/area]). The height of the femur neck can be obtained on the scans. Each lumbar vertebral body was approximated as a cylinder. The diameter and height of the four vertebral bodies were obtained from DXA scans. The bone volume of each vertebral body is calculated as π×(diameter/2)2×height, where the diameter of the vertebral column is area/height of the four vertebrae, which can be obtained on the scans (9).

The SPSS version 10.0 program (SPSS Inc., Chicago, IL, USA) was used for statistical analysis. The results are given as mean±SD. Two-way variance analyses were used for the statistical analysis of aBMD and vBMD related to gender and age. The results of the two-way variance analyses showed a significant difference between age and gender, but the interaction between age and gender factors were not statistically significant, indicating that the changes between age groups were similar between males and females. For this reason the variables were analyzed separately according to age groups with one-way variance analysis. Multiple regression analysis was performed with the backward elimination method to find the factors (i.e., puberty, height, and weight) influencing aBMD and vBMD.

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Results 

The aBMD of the lumbar spine (L1–L4) and femoral neck increased with age in boys and girls. Mean aBMD of the lumbar spine and femoral neck in boys and girls in age groups are given in Table 2.

Table 2. Increase of aBMD and vBMD L1–L4 According to Age in Males and Females
FemalesMales
aBMDvBMD aBMDvBMD
AgenMean±SDMean±SDnMean±SDMean±SD
2–2.99120.432±0.0610.195±0.03880.401±0.0460.170±0.040
3–3.99140.473±0.0720.209±0.046120.472±0.0620.198±0.041
4–4.99170.513±0.0550.224±0.029120.498±0.0510.204±0.027
5–5.99140.525±0.0750.217±0.031230.506±0.0650.205±0.037
6–6.99150.520±0.0530.209±0.026100.522±0.0530.197±0.032
7–7.99150.559±0.0550.224±0.03390.532±0.0840.192±0.037
8–8.99110.559±0.0520.217±0.02880.543±0.0710.187±0.027
9–9.9930.556±0.1020.192±0.053100.610±0.0500.225±0.026
10–10.9990.656±0.0740.223±0.014140.568±0.0730.206±0.033
11–11.9970.739±0.1260.251±0.02490.660±0.0470.230±0.028
12–12.99140.766±0.1020.239±0.023120.662±0.0510.219±0.014
13–13.99120.818±0.0980.260±0.032110.702±0.1140.206±0.032
14–14.9950.786±0.0520.240±0.015110.746±0.0960.229±0.026
15–15.9980.894±0.1410.273±0.042110.861±0.0710.248±0.021
16–16.99140.922±0.0670.279±0.02641.027±0.1200.275±0.031
17–1840.977±0.0830.298±0.01350.919±0.0910.247±0.023

Abbr: aBMD, areal bone mineral density; vBMD, volumetric bone mineral density; SD, standard deviation.

Males and females in the same age groups were compared with two sample Student's t-tests. Mean values of the lumbar aBMD were similar in males and females until the age of 10 years, and a significant difference between the two groups at the age of 10 years and at the ages of 12 through 14 years were found (p<0.01). In contrast, the femoral neck aBMD of the boys was greater than the girls, but was only statistically significant at ages 8 and 16 years (p<0.05). The Lumbar vBMD was similar in both groups until the age of 18 years (p>0.05). The increment was statistically significant between the ages of 11 and 13 years and 15 through 18 years in girls, and 13 through 18 years in boys (p<0.05). Femoral vBMD was only significantly different at the ages of 8 and 16 years (p<0.05) between girls and boys and did not increase with age (r=−0.04 and −0.16 in girls and boys, respectively). Mean vBMD of the lumbar spine and femoral neck in boys and girls are given in Table 3.

Table 3. Increase of Areal and Volumetric Femoral Neck BMD According to Age in Males and Females
Females Males
aBMDvBMD aBMDvBMD
AgenMean±SDMean±SDSnMean±SDMean±SDS
2–2.99110.460±0.0550.295±0.06070.455±0.0590.272±0.046
3–3.99110.503±0.0490.299±0.046110.554±0.1110.331±0.065
4–4.99170.511±0.0430.298±0.031120.563±0.0500.314±0.046
5–5.99140.532±0.0680.287±0.043230.547±0.0670.296±0.049
6–6.99150.558±0.0590.290±0.038100.576±0.0510.310±0.036
7–7.99150.571±0.0520.286±0.04490.651±0.0800.319±0.040
8–8.99110.578±0.0530.286±0.03480.647±0.0560.310±0.035
9–9.9930.637±0.0230.292±0.032100.722±0.0540.348±0.036
10–10.9990.628±0.0880.275±0.036140.672±0.0640.293±0.039
11–11.9970.655±0.1030.258±0.03090.702±0.0560.286±0.027
12–12.99140.723±0.1010.284±0.047120.732±0.0600.310±0.038
13–13.99120.673±0.0770.265±0.041110.793±0.1100.280±0.023
14–14.9950.714±0.0900.271±0.044110.785±0.0740.277±0.024
15–15.9980.806±0.1090.313±0.039110.830±0.1010.291±0.048
16–16.99140.756±0.0710.281±0.04040.913±0.1350.295±0.039
17–1840.851±0.0970.345±0.03550.841±0.0920.258±0.017

Abbr: BMD, bone mineral density; aBMD, areal bone mineral density; vBMD, volumetric bone mineral density; SD, standard deviation; SDS, Standard deviation score.

Because the variations according to age for males and females were not similar for lumbar aBMD, different regression models were performed for boys (i.e., predicted BMD, L1–L4=0.455+0.0018×age2, R2=% 81,6; p=0.00) and girls (i.e., predicted BMD, L1–L4=0.3157+[0.0562 ×age] – [0.054×age2]+[0.003×age3, R2=% 76,6; p=0.00]). Because the interaction was not significant between gender and age in areal femur neck BMD, one regression model was performed for both males and females (i.e., predicted femur neck=0.407+0.023×age, R2=% 67, 2; p=0.00).

Fig. 1, Fig. 2, Fig. 3, Fig. 4 show aBMD and vBMD of lumbar vertebrae and the femoral neck according to pubertal development. In both sexes, increase in aBMD L1–L4 values according to pubertal status were significant except aBMD did not differ between Tanner stage 3 and stage 4 (p>0.05). There was no difference in L1–L4 aBMD between males and females according to pubertal status. A significant difference was found between stages 1 and 2, and 2 and 3 in femoral neck aBMD (p<0.05). Lumbar and femoral vBMD did not change with pubertal status as indicated by Tanner in either the males or the females.

Lumbar and femoral aBMD and lumbar vBMD showed positive correlation with age, height, weight, and physical activity in both females and males. Femoral neck vBMD showed no correlation with age, height, and weight in females and showed a negative correlation with age, height, and weight in males. Correlation coefficients decreased in spine vBMD, and the significance disappeared in femoral neck vBMD (Table 4).

Table 4. Correlation Analyses Between Age, Weight, Height, Calcium Intake, Physical Activity, and Areal and Volumetric BMD in the Lumbar Area and Femoral Neck
Gender HeightWeightAgeCalcium intakePhysical activity
FemalesaBMD L1-4r0.8840.8980.897−0.0130.322
p0.0000.0000.0000.8610.000
vBMD L1–4r0.5800.5980.603−0.0370.191
p0.0000.0000.0000.6320.014
aBMD femoral neckr0.8240.8430.821−0.0430.400
p0.0000.0000.0000.5740.000
vBMD femoral neckr−0.095−0.046−0.054−0.0210.103
p0.2170.5540.4890.7840.192
MalesaBMD L1–4r0.8680.8730.8460.0720.376
p0.0000.0000.0000.3590.000
vBMD L1–4r0.4610.4690.4630.0300.209
p0.0000.0000.0000.7050.008
aBMD femoral neckr0.8500.8300.8160.1000.425
p0.0000.0000.0000.2010.000
vBMD femoral neckr−0.189−0.168−0.1950.029−0.061
p0.0160.0330.0130.7190.450

Abbr: BMD, bone mineral density; BMD, areal bone mineral density; vBMD, volumetric bone mineral density.

As age and growth variables are codependent for aBMD, the relationship among these was examined using multiple regression tests with the backward elimination method. With multiple regression analysis, we revealed that approximately 85% of the observed changes in lumbar aBMD were accounted for by puberty, age, and weight in girls (i.e., predicted L1–L4 aBMD=−0.021+0.0208×puberty+ 0.000341×age(3)+0.39×weight[log]). As much as 82% of variation was explained by age, weight, and height in boys (i.e., predicted L1–L4 aBMD=2.923–0.066×age+ 0.0011×age(3)+0.771×age[log] −1.87×height[log]+ 0.901×weight[log]). Forty percent of the changes in lumbar vBMD were accounted for by age and weight in girls (i.e., predicted L1–L4 vBMD=−0.05−0.007×age−0.005× weight+0.000026×age(3)+0.27×weight[log]), and by 28%–30% by age, weight, and height in males (i.e., predicted L1–L4 vBMD=1.94−0.02×age −0.004×weight+0.3 ×age[log]+−1.2×height[log]+0.53×weight[log]).

Median calcium (Ca) intake of the children according to age groups 2–3.99, 4–7.99, and 8–18 years were 975 (range, 250–2,250), 850 (range, 250–1,650), 850 (range, 250–1,850) mg/d, respectively.

There was a significant difference between boys and girls regarding duration of physical activity (91.7±198.7 vs 45.5±121.7 min/wk, respectively; p<0.05). There were no correlations between femoral vBMD and physical activity in either boys or girls, and no correlations between any of the outcome measures and Ca intake.

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Discussion 

The DXA of the lumbar vertebrae and femoral neck is useful in the measurement of BMD in children because of its accuracy, low radiation dose, short scan time, and ease of examination without sedation. Age, weight, height, pubertal status, nutrition, physical activity, genetics, and ethnicity are the factors that influence peak bone mass and BMD 1, 2.

In this study, lumbar BMD started to increase at the age of 2 but showed a steeper increase from the age of 10 years in girls and 14 years in boys. Lumbar aBMD showed a significant difference between girls and boys at ages 10 through 14 years. This suggests the rapid development of spinal bone mass in girls indicating earlier onset of puberty in girls than in boys. Kroger et al (9) showed the same increase after the age of 10 years in girls and 12 years in boys. Rubin et al (24) showed that the increase started at the age of 10 years until the age of 15 years in girls and from the age of 13 to 17 years in boys.

The increase in femoral neck aBMD in girls and boys was linear as in the study of Kroger et al (9). This could be due to the increased cortical bone in the femoral neck. The Femoral neck aBMD showed linear increase in both genders until the age of 11. After this age, similar to the studies of Faulkner et al (11) and Bonjour et al (17), the increase in males was dominant but not significant. A significant difference was found at the age of 8 and 16 years between boys and girls, respectively. Faulkner et al (11) found males to have a greater aBMD at the femoral neck at all ages.

Lumbar vBMD increased with age, and there was no significant difference between girls and boys. It has been shown that volumetric BMD reduced the effects of age on BMD, but it is still dependent on age. Kroger et al (9), Boot et al (25) and Lu et al (4) showed that lumbar vBMD was only slightly influenced by age, indicating a slow increase in bone density. Kroger et al (9), when using vBMD, found the difference was statistically significant between ages 16 through 18 years. Femoral neck vBMD was independent of age during childhood and adolescence. Similar results have been shown with quantitative computerized tomography (QCT) and DXA 4, 5, 25, 26, 27.

Although in our study, aBMD values were different between girls and boys according to age depending on earlier puberty in girls, there was no difference in Tanner stages between males and females, because each stage represents the same maturity. Spinal aBMD was significantly different in every Tanner stage in girls and boys, except Tanner stages 3 and 4. Lumbar vBMD did not change with pubertal status. Femoral neck aBMD was different between Tanner stages 1 and 2, and 2 and 3. There was no difference between Tanner stages in femoral neck vBMD. Boot et al (25) and Rio et al (26) revealed a positive association between Tanner stage and aBMD and vBMD of the lumbar spine. Although Southard et al (16) showed an increase in every pubertal stage, Boot et al (25), after adjusting for age, showed that spinal aBMD did not increase with puberty in boys but showed that puberty was a major determinant for aBMD.

Both lumbar aBMD and vBMD increased with age, but in spinal vBMD the regression line decreased and there was no correlation of age with vBMD of the femur neck in girls and a negative correlation in boys suggesting that BMD increases were due to increases of bone size. Although corrections with mathematical formulas are not ideal or anatomically perfect, they are simple and practical in clinical practice (9). The normalization of BMD values considering the size of bones is necessary if the child is to be followed-up through the growing years. In children with small bones, areal density can lead to inaccurate assumptions. We can state that the use of aBMD in growth-retarded children will have some restrictions in determining Z-scores. Correct interpretation of DXA is important for identifying growth-retarded children who may be at a real risk of osteoporosis as in renal insufficiency and other chronic diseases causing growth retardation. If a child develops normal puberty, but is short, vBMD can be used, but if the child has delayed puberty and is short than aBMD according to height groups can be used (28).

Both Bonjour et al (17) and Takahashi (3) showed an abrupt increase in BMD from 150 cm to adult height in men and in women from 140 cm, which suggested the importance of pubertal growth spurt on bone mineral accumulation. With multiple regression analyses Rubin et al (24) revealed that weight and puberty were the most effective parameters on spinal BMD (r2=0.80−0.74). In the same study 76% of the observed changes in radial (cortical) BMD were accounted for by the independent variables of weight, height, puberty, and age, with weight being the single strongest predictor. In our study with multiple regression analysis, spinal aBMD was accounted for by puberty, age, and weight in girls, and age, weight, and height in boys. Femoral aBMD was accounted for by age and weight in girls, and by weight and height in boys.

Femoral neck vBMD was influenced by weight in boys but not in girls. This can be due to greater physical activity in boys possibly creating more muscle mass in boys than girls. With more muscle, the forces on the bones may be greater. Both genders, when adjusted for age, femoral neck aBMD and spinal aBMD was fluenced by weight and vBMD was not influenced by weight. Weight influence was probably due to the weight bearing on bones. Lonzer et al (27) determined positive correlation between weight and BMD.

It is known that calcium intake during childhood is important for optimal mineralization of the skeleton. There was no correlation between calcium intake and spinal and femoral aBMD and vBMD. The relatively higher Ca intake in younger children and lower intake in adolescence may account for these results because the correlation vanished when age was held constant as in Kroger et al's (9) study. However, Ca intake was estimated from a questionnaire and not from a 3-day record. We believe that our data are not precluded by an effect of Ca intake on bone mass in children.

Slemenda et al (29) found that the total hours of weight bearing activity per week was positively correlated to BMD of the radius and hip in boys and girls ages 5 to 14 years. Other studies found a positive correlation between physical activity and lumbar spine BMD or femoral neck in children 9, 24. Boot et al (25), found positive correlation with BMD in boys only. In our study, physical activity had a positive association with femoral and lumbar aBMD and vBMD, suggesting that physical activity may be an important determinant of bone density. The effect of physical activity on vBMD may suggest that it increases not only bone size but also vBMD.

This cross-sectional study provides normative values for lumbar spine and femoral neck aBMD and vBMD of children and adolescents as young as 2 years of age for the Turkish population. The major determinant of BMD seems to be weight in girls and boys.

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PII: S1094-6950(06)00002-3

doi:10.1016/j.jocd.2005.08.001

Journal of Clinical Densitometry
Volume 9, Issue 1 , Pages 84-90, January 2006

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