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Bone Mineral Content and Density in Overweight and Control Adolescent Boys
Journal of Clinical Densitometry: Assessment of Skeletal Health, vol. 14, no. 2, 122e128, 2011 Ó Copyright 2011 by The International Society for Clinical Densitometry 1094-6950/14:122e128/$36.00 DOI: 10.1016/j.jocd.2011.01.003
Original Article
Bone Mineral Content and Density in Overweight and Control Adolescent Boys Rawad El Hage,*,1 Zaher El Hage,1 Christophe Jacob,1 Elie Moussa,1 Denis Theunynck,2 and Rafic Baddoura3 1
Laboratory of Physiology and Biomechanics of Motor Performance, Division of Physical Education, University of Balamand, Al Koura, Lebanon; 2Laboratory of RELACS, Department of Physical Education, University of Littoral C^ ote d’opale, Dunkerque, France; and 3Department of Rheumatology, H^otel-Dieu Hospital, St Joseph University, Beirut, Lebanon
Abstract The aim of this study was to compare bone mineral content (BMC) and areal bone mineral density (aBMD) in overweight and control adolescent boys. This study included 27 overweight (body mass index [BMI] O 25 kg/m2) adolescent (17.1 2.1 yr old) boys and 29 maturation-matched (16.7 2.0 yr old) controls (BMI ! 25 kg/m2). Bone mineral area (BMA), BMC, and aBMD were assessed by dual-energy X-ray absorptiometry (DXA) at the whole body (WB), lumbar spine (L2eL4), total hip (TH), femoral neck (FN), and left forearm (ultra distal [UD], mid Radius, 1/3 Radius, and total Radius). Body composition (lean mass, fat mass, and fat mass percentage) was assessed also by DXA. The expressions WB BMC/height, WB aBMD/height, and WB BMAD were used to adjust for WB bone size. WB BMC, WB BMC/height, WB BMA, L2eL4 aBMD, TH aBMD, FN aBMD, and UD aBMD were higher in overweight boys compared with controls ( p ! 0.05). However, WB BMAD was lower in overweight boys compared with controls ( p ! 0.05). After adjustment for weight, lean mass, or BMI, using a one-way analysis of covariance, there were no differences between the 2 groups (overweight and controls) regarding bone characteristics (BMC, BMA, aBMD, BMC/height, aBMD/height, and BMAD of the WB and aBMD of the lumbar spine; the TH; the FN; and the forearm). In conclusion, this study shows that after adjusting for weight, lean mass, or BMI, there are no differences between overweight and control adolescent boys regarding aBMD values. Key Words: Body composition; bone strength; Lebanon; obesity; pediatrics.
drops in physical activity) and hereditary factors (1e8). Recently, birth weight, breast-feeding duration, and daily calcium intake (DCI) were linked to obesity in children and adolescents (4e8). For example, a high birth weight has been suggested to program an increased risk of adult obesity, whereas breast-feeding and high calcium diets may protect against childhood and adult obesity (4e8). Several previous studies have shown that overweight and obese adolescents have a higher risk of fracture when compared with controls (9e11). Thus, it is very important to understand the effect of being overweight or obese on the growing skeleton. To date, several studies aimed at exploring the effect of obesity and overweight on bone mineral content (BMC), areal bone
Introduction The prevalence of overweight and obesity in children and adolescents is increasing worldwide and especially in the middle-east (1e3). Obesity and overweight can result from several factors (1e8). In general, it is about the interaction of environmental factors (turbid by the food behavior and/or Received 12/05/10; Revised 01/19/11; Accepted 01/20/11. *Address correspondence to: Rawad El Hage, PhD, Division of Physical Education, Faculty of Arts and Social Sciences, University of Balamand, P.O. Box 100, Tripoli, Lebanon. E-mail: [email protected]
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BMD in Overweight Boys mineral density (aBMD), and bone strength indices in adolescents (9e19). However, these studies have given conflicting results. It is argued that obese and overweight adolescents have higher, equivalent, or lower aBMD and BMC when compared with controls (9e19). This may be explained partially by the following factors. Firstly, the relation between fat mass and aBMD in adolescence is influenced by sex (20e22). In reality, fat mass is more strongly related to the aBMD in girls than boys (20). Secondly, body weight is strongly related to the aBMD of the weight-bearing bones and to a lesser extent to the aBMD of the noneweight-bearing bones (18,19). Finally, the question of adjusting BMC and aBMD values for weight, lean mass, or body mass index (BMI) to judge the effects of overweight and obesity on these parameters remains open (11e14,18). Therefore, the aim of this study was to compare whole body (WB), total hip (TH), lumbar spine, and forearm aBMD in overweight and control adolescent boys. We hypothesized that overweight boys should have higher aBMD at the weight-bearing sites when compared with controls because being overweight is associated with higher lean mass for height (13,17).
Material and Methods Subjects and Study Design The study participants (n 5 60) were recruited from 5 private schools in Beirut, Lebanon. Inclusion criteria were being adolescent (Tanner stage between 3 and 5) boys from 14 to 20 yr of age with no diagnosis of comorbidities and no history of fracture. The boys were nonsmokers and had no history of major orthopedic problems or other disorders known to affect bone metabolism. Boys were divided into a group of overweight (BMI O 25 kg/m2; n 5 27) and a group of control boys (BMI ! 25 kg/m2; n 5 29). These 2 groups were matched for pubertal status. This study did not include extremely lean (BMI ! 16 kg/m2) boys or extremely obese (BMI O 40 kg/m2) boys. Four boys were excluded from this study because they were extremely obese or extremely lean. An informed written consent was obtained from the children and their parents. This study was approved by the University of Balamand Ethics Committee.
Anthropometric Measurements Height (cm) was measured in the upright position to the nearest 1 mm with a Seca standard stadiometer. Body weight (kg) was measured on a Taurus mechanic scale with a precision of 100 g. The boys were weighed wearing only underclothes. BMI was calculated as body weight divided by height squared (kg/m2). Body composition (lean mass, fat mass, and fat mass percentage) was assessed by dual-energy X-ray absorptiometry (DXA) (DXA Hologic QDR-4500W; Waltham, MA). In our laboratory, the in vivo coefficients of variation were !1% for fat and lean mass. A single operator performed and analyzed all DXA scans to standardize the analyses. Daily quality control scans were performed with the manufacturer’s phantom. Journal of Clinical Densitometry: Assessment of Skeletal Health
123 Bone Measurements BMC (g), bone mineral area (BMA, in cm2), and aBMD (g/cm2) were determined for each individual. The DXA measurements were completed for the WB at the lumbar spine (L2eL4), at the TH, at the femoral neck (FN), at the ultra distal (UD) Radius, at the 1/3 Radius, at the mid Radius, and at the total Radius using the instrument previously described. The Hologic APEX software, version 2 (1986e2007, Hologic Inc., Bedford, MA) was used to analyze the DXA scans on the Hologic machine. In our laboratory, the coefficients of variation were !1% for BMC and aBMD. Bone mineral apparent density (BMAD) (g/cm3), an estimate of volumetric bone density, was calculated as previously described (23). For WB, the formula BMAD 5 BMC/[WB (BMA2)/body height] was used. The expressions BMC/height and aBMD/height were used to adjust for whole-body bone size (14,24). The same certified technician performed all bone measurements using the same machine.
Pubertal Status Assessment Tanner pubertal status was determined by self-evaluation, a method of recognized validity and reliability (25). Children were provided with line drawings of the 5 Tanner stages and were instructed by a research assistant to choose the drawing that best represented their current stage of development. Children completed the form in a private setting away from the other children.
Birth Weight and Breast-Feeding Birth weights (kg) were obtained from the obstetric records. The duration (mo) of breast-feeding was recorded by the mothers. No distinction was made between exclusive and partial breast-feeding.
Daily Calcium Intake The estimation of the DCI was based on a frequency questionnaire (26). Selection of items was based on the food composition diet, frequency of use, and relative importance of food items as a calcium source. The total number of foods was 30 items. The questionnaire included the following food items: milk and dairy products, including calciumenriched items such as yoghurt, cheese, and chocolate. Items such as eggs, meat, fish, cereals, bread, vegetables, and fruits were also included. Adequacy of calcium in the subjects was assessed using the adequate intake guidelines of 1300 mg of calcium.
Physical Activity Exercise frequency was assessed from a questionnaire inquiring about the number of hours spent on sports per week (organized sports plus leisure-time activity). This questionnaire included questions on physical education classes, formal and informal activities, activities done at school, activities done out of school in sports clubs or gyms, and activities done at home. Volume 14, 2011
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Statistical Analysis Basic data are presented as mean standard deviation (Tables 1 and 2) or as mean standard error (Table 3). Chisquared tests were used to test the Tanner stage distribution between the 2 groups. Comparisons between the overweight and the control group were made after checking for Gaussian distribution. If Gaussian distribution was found, parametric unpaired t-tests were used. In other cases, ManneWhitney U-tests were used. Associations between clinical characteristics and bone data were given as Pearson correlation coefficients (for normally distributed variables) or Spearman correlation coefficients (for nonnormally distributed variables). Multiple linear regression analysis models were used to test the relationship between aBMD with age, lean mass, and height; and between WB BMC with age, height, lean mass, and fat mass; and r2 were reported. Bone data were compared after adjustment for total body weight, height, lean mass, BMI, fat mass, age, and Tanner stage using a one-way analysis of covariance. The difference was considered statistically significant at p ! 0.05. Data were analyzed using Number Cruncher Statistical System (2001).
Results Clinical Characteristics of the Subjects Clinical characteristics of the adolescent boys are displayed in Table 1. Tanner stage distributions did not differ between overweight and control boys. Age, mean Tanner
Table 1 Clinical Characteristics of Overweight and Control Adolescent Boys Parameter
Overweight (n 5 27)
Controls (n 5 29)
Age (yr) 17.1 2.1 16.7 2.0 Tanner (Nd3/4/5) 5/10/12 6/13/10 Tanner (%d3/4/5) 19/37/44 21/45/34 Birth weight (kg) 3.62 0.42 3.36 0.47 Breast-feeding (mo) 7.7 6.2 9.9 8.0 Weight (kg) 91.9 14.6*** 64.2 7.8 Height (cm) 174.0 5.7 173.2 5.6 BMI (kg/m2) 30.3 4.2*** 21.4 2.1 Lean mass (kg) 64.6 6.9*** 52.3 15.4 Lean mass/height (kg/cm) 0.352 0.033*** 0.292 0.031 Fat mass (kg) 24.7 8.1*** 9.6 3.0 Fat mass (%) 26.9 6.3*** 15.1 3.4 DCI (mg/d) 1,131 465 945 225 PA (h/wk) 3.5 2.5 4.2 2.4 Note: In italic: ManneWhitney U-tests were used; in normal font: parametric unpaired t-tests were used. Abbr: BMI, body mass index; DCI, daily calcium intake; PA, physical activity. ***p ! 0.001. Journal of Clinical Densitometry: Assessment of Skeletal Health
Table 2 Bone Characteristics of Overweight and Control Adolescent Boys Overweight (n 5 27)
Controls (n 5 29)
WB BMC (g) 2472 323* 2200 398 WB BMA (cm2) 2218 149*** 2044 179 WB aBMD (g/cm2) 1.11 0.08 1.07 0.12 WB BMC/height 14.2 1.6** 12.7 2.2 (g/cm) WB aBMD/height 0.0064 0.0004 0.0061 0.0006 (g/cm3) 0.087 0.005* 0.091 0.006 WB BMAD (g/cm3) L2eL4 aBMD (g/cm2) 0.993 0.119* 0.914 0.125 TH aBMD (g/cm2) 1.053 0.136** 0.949 0.140 FN aBMD (g/cm2) 0.978 0.140* 0.880 0.145 UD Radius aBMD 0.442 0.049* 0.410 0.060 (g/cm2) 0.698 0.060 0.679 0.072 1/3 Radius aBMD (g/cm2) 0.583 0.062 0.553 0.075 Mid Radius aBMD (g/cm2) 0.577 0.056 0.547 0.070 Total Radius aBMD (g/cm2) Note: In italic: ManneWhitney U tests were used; in normal font: parametric unpaired t-tests were used. Abbr: WB, whole body; BMC, bone mineral content; BMA, bone mineral area; aBMD, areal bone mineral density; BMAD, bone mineral apparent density; TH, total hip; FN, femoral neck; UD, ultra distal. *p ! 0.05; **p ! 0.01; ***p ! 0.001.
stage, birth weight, breast-feeding duration, height, physical activity (h/wk), and DCI were not different between overweight and control boys. However, body weight, lean mass, fat mass, fat mass percentage, and BMI were higher in overweight boys when compared with controls ( p ! 0.001).
Crude Bone Measurements in Overweight and Control Boys WB BMC, WB BMA, and WB BMC/height were higher ( p ! 0.05) in overweight boys when compared with controls. L2eL4, TH, FN, and UD Radius aBMD were higher in overweight boys compared with controls ( p ! 0.05). Finally, WB BMAD was higher in control boys when compared with overweight boys ( p ! 0.05) (Table 2).
Correlations Between Clinical Characteristics and Bone Data Age and Tanner stage were positively related to WB BMC, WB BMA, L2eL4 aBMD, UD aBMD, mid Radius aBMD, 1/3 Radius aBMD, and total Radius aBMD ( p ! 0.05). Weight, BMI, lean mass, and the ratio lean mass/height were positively related to WB BMC, WB BMC/height, WB Volume 14, 2011
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Table 3 Bone Data Adjusted for Body Weight, Lean Mass, and BMI in Overweight and Control Adolescent Boys Adjusted for body weight Overweight (n 5 27)
Controls (n 5 29)
Adjusted for lean mass Overweight (n 5 27)
Controls (n 5 29)
Adjusted for BMI Overweight (n 5 27)
Controls (n 5 29)
WB BMC (g) 2252 59 2450 63 2264 46 2437 49 2308 67 2386 71 WB BMA (cm2) 2101 24 2176 26 2114 17 2162 19 2136 30 2137 32 WB aBMD (g/cm2) 1.06 0.01 1.12 0.02 1.06 001 1.12 0.01 1.07 0.02 1.11 0.02 WB BMC/height 13.1 0.3 13.9 0.3 13.2 0.2 13.8 0.2 13.2 0.3 13.7 0.3 (g/cm) WB aBMD/height 0.0062 0.0001 0.0063 0.0001 0.0062 0.0001 0.0063 0.0001 0.0061 0.0001 0.0064 0.0001 (g/cm3) 0.091 0.001 0.086 0.001 0.092 0.001 0.087 0.001 0.090 0.001 WB BMAD (g/cm3) 0.086 0.001 L2eL4 aBMD 0.990 0.024 1.007 0.024 0.983 0.025 1.014 0.024 0.992 0.025 1.005 0.024 (g/cm2) 0.923 0.021 0.978 0.020 0.945 0.021 0.952 0.022 0.934 0.022 0.968 0.021 TH aBMD (g/cm2) FN aBMD (g/cm2) 0.903 0.025 0.949 0.024 0.936 0.025 0.911 0.026 0.907 0.025 0.944 0.024 UD Radius aBMD 0.422 0.010 0.428 0.009 0.428 0.010 0.425 0.010 0.423 0.010 0.427 0.010 (g/cm2) 0.688 0.012 0.706 0.017 0.676 0.012 0.700 0.112 0.675 0.012 0.699 0.012 1/3 Radius aBMD (g/cm2) 0.551 0.012 0.581 0.012 0.560 0.013 0.574 0.013 0.556 0.012 0.576 0.012 Mid Radius aBMD (g/cm2) 0.573 0.011 0.556 0.012 0.567 0.012 0.547 0.011 0.573 0.011 Total Radius aBMD 0.547 0.011 (g/cm2) Note: Values are means standard error. Abbr: WB, whole body; BMC, bone mineral content; aBMD, areal bone mineral density; BMAD, bone mineral apparent density; TH, total hip; FN, femoral neck; UD, ultra distal.
BMA, WB aBMD, WB aBMD/height, L2eL2 aBMD, TH aBMD, FN aBMD, UD Radius aBMD, mid Radius aBMD, and total Radius aBMD ( p ! 0.05). Fat mass was positively related to WB BMC (r 5 0.44; p ! 0.01), WB aBMD (r 5 0.28; p ! 0.05), WB BMC/height (r 5 0.43; p ! 0.01), WB BMA (r 5 0.58; p ! 0.001), TH aBMD (r 5 0.30; p ! 0.01), and negatively associated with WB BMAD (r 5 0.37; p ! 0.05). Birth weight was only related to WB BMAD (r 5 0.52; p ! 0.01). Breast-feeding duration (mo) and DCI (mg/d) were not significantly correlated to bone data. Finally, physical activity (h/wk) was only correlated to FN aBMD (r 5 0.26; p ! 0.05) (Table 4).
Multiple Linear Regression Analysis Models Fat mass was not significantly related to WB BMC after adjusting for age, height, and lean mass. Moreover, age and lean mass explained 45% of the lumbar spine aBMD variance and 47% of total Radius aBMD variance.
Adjusted Bone Data in Overweight Boys and Controls Bone characteristics adjusted for weight, lean mass, and BMI are shown in Table 3. After adjusting for weight, lean mass, BMI, or fat mass, WB BMC, WB BMA, WB BMC/height, Journal of Clinical Densitometry: Assessment of Skeletal Health
WB aBMD/height, WB BMAD, and aBMD (WB, L2eL4, TH, FN, UD Radius, 1/3 Radius, mid Radius, and total Radius) were not different between the 2 groups (overweight and controls). After adjusting for height, age, or Tanner stage, overweight boys had higher WB BMC, WB BMA, WB BMC/height, L2eL4 aBMD, TH aBMD, FN aBMD, and UD Radius aBMD values when compared with controls ( p ! 0.05).
Discussion The main findings of this study were that WB BMC, WB BMC/height, L2eL4 aBMD, TH aBMD, and UD aBMD were higher in overweight boys compared with controls and that after adjustment for weight, lean mass, fat mass, or BMI, there were no differences in BMC or aBMD between the 2 groups. Upto our knowledge, it’s the first study that compared BMD of several bone sites in overweight and control adolescent boys from Lebanon. Concerning the morphological characteristics, the ratio lean mass/height was higher in overweight boys compared with controls. This result is in accordance with those of several previous studies (13,14,17). In reality, being overweight is usually associated with increased lean mass, fat mass, and bone mass (12e14). Volume 14, 2011
0.65*** 0.64*** 0.40** 0.31* 0.35** 0.48*** 0.47*** 0.17 0.06 Note: In italic: Spearman coefficient of correlation; in normal font: Pearson coefficient of correlation. Abbr: WB, whole body; aBMD, areal bone mineral density; TH, total hip; FN, femoral neck; UD, ultra distal. *p ! 0.05; **p ! 0.01; ***p ! 0.001.
0.63*** 0.63*** 0.36** 0.38** 0.29* 0.46*** 0.43** 0.11 0.00 0.57*** 0.50*** 0.41** 0.17 0.42** 0.45** 0.46** 0.28 0.22 0.16 0.14 0.50*** 0.26 0.46*** 0.53*** 0.53*** 0.33* 0.26 0.30* 0.20 0.50*** 0.22 0.46*** 0.51*** 0.52*** 0.30* 0.20 0.50*** 0.43*** 0.47*** 0.36** 0.45*** 0.55*** 0.53*** 0.28 0.18 0.42** 0.23 0.29* 0.07 0.32* 0.39** 0.41** 0.21 0.11 Age (yr) Tanner (mean) Weight (kg) Height (cm) BMI (kg/m2) Lean mass (kg) Lean mass/height (kg/cm) Fat mass (kg) Fat mass (%)
0.46*** 0.27 0.39** 0.32* 0.34* 0.58*** 0.56*** 0.28* 0.15
Mid Radius aBMD (g/cm2) 1/3 Radius aBMD (g/cm2) UD Radius aBMD (g/cm2) FN aBMD (g/cm2) TH aBMD (g/cm2) L2eL4 aBMD (g/cm2) WB aBMD/ height (g/cm3) WB aBMD (g/cm2)
Table 4 Correlations Between Clinical Characteristics and Bone Mineral Density Values
0.65*** 0.64*** 0.40** 0.31* 0.35** 0.50*** 0.48*** 0.17 0.07
El Hage et al. Total Radius aBMD (g/cm2)
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Birth weight was not different between the 2 groups. Low birth weight has been found to be associated with a higher BMI in adults (5). The effect of birth weight on BMI may not be detected when the study population is too small. Breast-feeding duration was not different between the 2 groups. Several studies in Western societies have reported the protective effects of breast-feeding against childhood obesity (5e7). However, in our study, no clear association between breast-feeding duration and BMI was found. We suggest that genetic or environmental factors other than breast-feeding have a greater effect on BMI at this age. In our study, overweight boys had higher WB BMC, WB BMA, and WB BMC/height when compared with controls. Overweight and obesity during adolescence augment bone mass and dimensions (13). In addition, aBMD of the weight-bearing bones (lumbar spine, TH, and FN) was higher in overweight boys compared with controls, whereas aBMD of the WB, the 1/3 Radius, the mid Radius, and the Total Radius was not significantly different between the 2 groups. Thus, this study reinforces the hypothesis, which states that obesity and overweight have a site-specific effect on aBMD (18,19,27). In reality, the influence of obesity and overweight on weight-bearing bones is the result of load, this effect being comparable to the influence of physical activity (28). Overall, this study suggests a positive effect of overweight and obesity on aBMD of the weight-bearing bones in adolescent boys. Overweight and obesity may influence bone mass by another mechanism (29). Free sex hormones, insulin, insulin-like growth-factor-I, leptin, amylin, and preptin concentrations increase with obesity; these hormones can stimulate the osteoblastic activity and decrease the osteoclastic activity and may positively influence the aBMD of the weight-bearing and the noneweight-bearing bones (29). Wetzsteon et al. (30) showed in a longitudinal study (16 mo) conducted on overweight children that change in bone strength was positively related to change in lean mass and muscle cross sectional area but not to fat mass. In our study, lean mass was a stronger positive determinant of BMC, BMA, and aBMD than fat mass. Moreover, fat mass was not positively associated to WB BMC after adjusting for age, height, and lean mass. These results suggest that fat mass is not an independent determinant of BMC in boys. In actual fact, aBMD adapts primarily to dynamic (lean mass) rather than static loads (fat mass) (17). Interestingly, the relation between fat mass and bone mass in adolescents is highly influenced by sex (20e22,31). In truth, we have previously reported that fat mass is a positive determinant of lumbar spine aBMD and WB BMC in adolescent girls but not in adolescent boys (20). Age, Tanner stage, weight, lean mass, and BMI were positively related to BMC, BMA, and aBMD values. These results are in accordance with those of several previous studies conducted on adolescents (12e14,28). Fat mass was negatively associated with WB BMAD. This result is in line with that reported by Rocher et al. (18). In fact, the BMA/height and BMA2/height ratios were higher in overweight boys compared with controls in this study. Volume 14, 2011
BMD in Overweight Boys After adjustment for weight, lean mass, BMI, or fat mass, there were no differences in bone data between overweight and control boys. Thus, BMC and aBMD of the overweight boys adapt to the increased weight and lean mass. Furthermore, after adjustment for age or Tanner stage, overweight boys displayed higher WB BMC, WB BMA, WB BMC/ height, L2eL4 aBMD, TH aBMD, FN aBMD, and UD Radius aBMD values when compared with controls. Therefore, this study suggests that being overweight is associated with higher BMC and aBMD for age in adolescent boys. Physical activity (h/wk) was positively related to FN aBMD but not to lumbar spine aBMD. In fact, the genetic effect appears to be greater in the lumbar spine compared with the FN (32). It is possible that physical activity exerts a greater effect on the cortical component of the bony structure of the femur (32,33). Birth weight was not significantly related to BMC or aBMD and was negatively related to WB BMAD. This result is in contrast with that of our previous study conducted on adolescent girls in whom we showed that birth weight was positively associated with WB BMC, WB BMC/height, and WB aBMD (34). Accordingly, the relation between birth weight and BMC or aBMD in adolescents may be influenced by sex. Breast-feeding duration was not related to bone data in this group of adolescent boys. Further, large studies are necessary to better understand the relation between breastfeeding duration and bone mass in adolescents. In this study, mean DCI was below the daily requirements for this age group (1300 mg) (35). These results are in line with those of several reports, which measured DCI in Lebanese adolescents (14,36e38). In addition, DCI was not significantly related to bone data. These results are in agreement with those of several cross-sectional studies conducted on adolescents (14,20,21). The lack of correlation between DCI and bone data may be because of the cross-sectional nature of this study. The present study has several strengths. First, it is one of the few studies that explored the effects of being overweight on BMC and aBMD of several bone sites in pubertal boys. Secondly, this study aimed at studying the effects of being overweight on BMC and aBMD of weight-bearing and noneweight-bearing bones. Lastly, this study was conducted on Lebanese adolescents; it is well known that Lebanese adolescents have mean aBMD values, which are lower than Western normative values (38). We acknowledge several limitations of the study. Firstly, the cross-sectional nature of the study is a limitation because it cannot evaluate the confounding variables. Secondly, the small number of subjects and the matching method is a limitation. Thirdly, there are well-known difficulties in assessing diet, sexual maturation, and physical activity using self-reported questionnaires (39,40). For instance, Tanner self-assessment does not provide a high degree of accuracy of sexual maturation in obese children (39). Moreover, food-frequency questionnaires provide limited list of foods and do not allow specific ingredients to be entered for analysis (40). Fourthly, aBMD measured with DXA is a surrogate for bone strength but not Journal of Clinical Densitometry: Assessment of Skeletal Health
127 a measurement of it (41). In fact, bone strength is not only determined by the amount of bone mineral, but also by its partial distribution with respect to the loading forces that may be encountered (41). Therefore, further investigations on bone geometry and microarchitecture are necessary to better understand the effects of being overweight on the growing skeleton. Finally, according to Bolotin and Siev€anen (42), DXAmeasured in vivo BMD inaccuracies are patient specific, because the magnitude of the BMD value extracted from a given DXA measurement depends on the exact specifications of the bone marrow composition, the detailed composition of the extraosseous soft tissue, and the true (not measured) value of BMD (i.e., proportional to the average thickness of bone material along all X-ray paths traversing the given bone site) actually pertaining within the specific scan region of interest (ROI) of each given patient. Moreover, for any given extraosseous soft-tissue composition in the scan ROI, the more yellow the bone marrow the more DXA underestimates true BMD. Furthermore, for any given bone marrow composition, the smaller the proportion of fat in the extraosseous lean tissue the more the DXA-measured BMD underestimates the true value (42). In conclusion, this study suggests a positive effect of BMI on crude bone mineral density of the weight-bearing bones (lumbar spine, hip, and FN) in adolescent boys. However, after adjustment for weight, lean mass, or BMI, there are no differences between overweight and control adolescent boys regarding aBMD of the WB, the lumbar spine, the hip, and the forearm.
Acknowledgments This study was supported by a grant from the research council of the University of Balamand, Lebanon.
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128 9. Goulding A, Jones IE, Taylor RW, et al. 2001 Bone mineral density and body composition in boys with distal forearm fractures: a dual-energy x-ray absorptiometry study. J Pediatr 139: 509e515. 10. Skaggs DL, Loro ML, Pitukcheewanont P, et al. 2001 Increased body weight and decreased radial cross-sectional dimensions in girls with forearm fractures. J Bone Miner Res 16:1337e1342. 11. Goulding A, Taylor RW, Jones IE, et al. 2000 Overweight and obese children have low bone mass and area for their weight. Int J Obes Relat Metab Disord 24:627e632. 12. Ellis KJ, Shypailo RJ, Wong WW, Abrams SA. 2003 Bone mineral mass in overweight and obese children: diminished or enhanced? Acta Diabetol 40(Suppl 1):S274eS277. 13. Leonard MB, Shults J, Wilson BA, et al. 2004 Obesity during childhood and adolescence augments bone mass and bone dimensions. Am J Clin Nutr 80:514e523. 14. El Hage R, Moussa E, Jacob C. 2010 Bone mineral content and density in obese, overweight, and normal-weighted sedentary adolescent girls. J Adolesc Health 47:591e595. 15. Janicka A, Wren TA, Sanchez MM, et al. 2007 Fat mass is not beneficial to bone in adolescents and young adults. J Clin Endocrinol Metab 92:143e147. 16. Pollock NK, Laing EM, Baile CA, et al. 2007 Is adiposity advantageous for bone strength? A peripheral quantitative computed tomography study in late adolescent females. Am J Clin Nutr 86:1530e1538. 17. Petit MA, Beck TJ, Shults J, et al. 2005 Proximal femur bone geometry is appropriately adapted to lean mass in overweight children and adolescents. Bone 36:568e576. 18. Rocher E, Chappard C, Jaffre C, et al. 2008 Bone mineral density in prepubertal obese and control children: relation to body weight, lean mass, and fat mass. J Bone Miner Metab 26:73e78. 19. Ducher G, Bass S, Naughton GA, et al. 2009 Overweight children have a greater proportion of fat mass relative to muscle mass in the upper limbs than in the lower limbs: implications for bone strength at the distal forearm. Am J Clin Nutr 90: 1104e1111. 20. El Hage R, Courteix D, Benhamou CL, et al. 2009 Relative importance of lean and fat mass on bone mineral density in a group of adolescent girls and boys. Eur J Appl Physiol 105:759e764. 21. Arabi A, Tamim H, Nabulsi M, et al. 2004 Sex differences in the effect of body-composition variables on bone mass in healthy children and adolescents. Am J Clin Nutr 80:1428e1435. 22. Ackerman A, Thornton JC, Wang J, et al. 2006 Sex difference in the effect of puberty on the relationship between fat mass and bone mass in 926 healthy subjects, 6 to 18 years old. Obesity (Silver Spring) 14:819e825. 23. Katzman D, Bachrach L, Carter D, Marcus R. 1991 Clinical and anthropometric correlates of bone mineral acquisition in healthy adolescent girls. J Clin Endocrinol Metab 73:1332e1339. 24. Reid IR, Lindsay DP, Margaret CE. 1992 Fat mass is an important determinant of whole body bone density in premenopausal women but not in men. J Clin Endocrinol Metab 75:779e782. 25. Duke PM, Litt IF, Gross RT. 1980 Adolescents’ self assessment of sexual maturation. Pediatrics 66:918e920.
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El Hage et al. 26. Fardellone P, Sebert JL, Bouraga M, et al. 1991 Evaluation of the calcium content of diet by frequential self-questionnaire. Rev Rhum Mal Osteoartic 58:99e103. 27. Farr JN, Chen Z, Lisse JR, et al. 2010 Relationship of total body fat mass to weight-bearing bone volumetric density, geometry, and strength in young girls. Bone 46:977e984. 28. Boot AM, De Ridder MA, Pols HA, et al. 1997 Bone mineral density in children and adolescents: relation to puberty, calcium intake, and physical activity. J Clin Endocrinol Metab 82:57e62. 29. Reid IR. 2008 Relationships between fat and bone. Osteoporos Int 19:595e606. 30. Wetzsteon RJ, Petit MA, Macdonald HM, et al. 2008 Bone structure and volumetric BMD in overweight children: a longitudinal study. J Bone Miner Res 23:1946e1953. 31. Sayers A, Tobias JH. 2010 Fat mass exerts a greater effect on cortical bone mass in girls than boys. J Clin Endocrinol Metab 95:699e706. 32. Bonjour JP, Chevalley T, Rizzoli R, Ferrari S. 2007 Geneenvironment interactions in the skeletal response to nutrition and exercise during growth. Med Sport Sci 51:64e80. 33. Vicente-Rodriguez G, Jimenez-Ramirez J, Ara I, et al. 2003 Enhanced bone mass and physical fitness in prepubescent footballers. Bone 33:853e859. 34. El Hage R, Moussa E, Hammoud A, et al. 2010 Birth weight is an independent determinant of whole body bone mineral content and bone mineral density in a group of Lebanese adolescent girls. J Bone Miner Metab 28:360e363. 35. , DRI. 1997 Dietary reference intakes for calcium, phosphorus, magnesium, vitamin D, and fluoride. Institute of Medicine, Washington, DC. 36. El Hage R, Jacob C, Moussa E, et al. 2010 Daily calcium intake and body mass index in a group of Lebanese adolescents. J Med Liban 57:253e257. 37. Salamoun MM, Kizirian AS, Tannous RI, et al. 2005 Low calcium and vitamin D in healthy children and adolescents and their correlates. Eur J Clin Nutr 59:177e184. 38. Arabi A, Nabulsi M, Maalouf J, et al. 2004 Bone mineral density by age, gender, pubertal stages, and socioeconomic status in healthy Lebanese children and adolescents. Bone 35: 1169e1179. 39. Raman A, Lustig RH, Fitch M, Fleming SE. 2009 Accuracy of self-assessed Tanner staging against hormonal assessment of sexual maturation in overweight African-American children. J Pediatr Endocrinol Metab 22:609e622. 40. Schaefer EJ, Augustin JL, Schaefer MM, et al. 2000 Lack of efficacy of a food-frequency questionnaire in assessing dietary macronutrient intakes in subjects consuming diets of known composition. Am J Clin Nutr 71:746e751. 41. Ammann P, Rizzoli R. 2003 Bone strength and its determinants. Osteoporos Int 14(Suppl 3):S13eS18. 42. Bolotin HH, Siev€anen H. 2001 Inaccuracies inherent in dual-energy x-ray absorptiometry in vivo bone mineral density can seriously mislead diagnostic/prognostic interpretations of patient-specific bone fragility. J Bone Miner Res 16:799e805.
Volume 14, 2011
Original Article
Bone Mineral Content and Density in Overweight and Control Adolescent Boys Rawad El Hage,*,1 Zaher El Hage,1 Christophe Jacob,1 Elie Moussa,1 Denis Theunynck,2 and Rafic Baddoura3 1
Laboratory of Physiology and Biomechanics of Motor Performance, Division of Physical Education, University of Balamand, Al Koura, Lebanon; 2Laboratory of RELACS, Department of Physical Education, University of Littoral C^ ote d’opale, Dunkerque, France; and 3Department of Rheumatology, H^otel-Dieu Hospital, St Joseph University, Beirut, Lebanon
Abstract The aim of this study was to compare bone mineral content (BMC) and areal bone mineral density (aBMD) in overweight and control adolescent boys. This study included 27 overweight (body mass index [BMI] O 25 kg/m2) adolescent (17.1 2.1 yr old) boys and 29 maturation-matched (16.7 2.0 yr old) controls (BMI ! 25 kg/m2). Bone mineral area (BMA), BMC, and aBMD were assessed by dual-energy X-ray absorptiometry (DXA) at the whole body (WB), lumbar spine (L2eL4), total hip (TH), femoral neck (FN), and left forearm (ultra distal [UD], mid Radius, 1/3 Radius, and total Radius). Body composition (lean mass, fat mass, and fat mass percentage) was assessed also by DXA. The expressions WB BMC/height, WB aBMD/height, and WB BMAD were used to adjust for WB bone size. WB BMC, WB BMC/height, WB BMA, L2eL4 aBMD, TH aBMD, FN aBMD, and UD aBMD were higher in overweight boys compared with controls ( p ! 0.05). However, WB BMAD was lower in overweight boys compared with controls ( p ! 0.05). After adjustment for weight, lean mass, or BMI, using a one-way analysis of covariance, there were no differences between the 2 groups (overweight and controls) regarding bone characteristics (BMC, BMA, aBMD, BMC/height, aBMD/height, and BMAD of the WB and aBMD of the lumbar spine; the TH; the FN; and the forearm). In conclusion, this study shows that after adjusting for weight, lean mass, or BMI, there are no differences between overweight and control adolescent boys regarding aBMD values. Key Words: Body composition; bone strength; Lebanon; obesity; pediatrics.
drops in physical activity) and hereditary factors (1e8). Recently, birth weight, breast-feeding duration, and daily calcium intake (DCI) were linked to obesity in children and adolescents (4e8). For example, a high birth weight has been suggested to program an increased risk of adult obesity, whereas breast-feeding and high calcium diets may protect against childhood and adult obesity (4e8). Several previous studies have shown that overweight and obese adolescents have a higher risk of fracture when compared with controls (9e11). Thus, it is very important to understand the effect of being overweight or obese on the growing skeleton. To date, several studies aimed at exploring the effect of obesity and overweight on bone mineral content (BMC), areal bone
Introduction The prevalence of overweight and obesity in children and adolescents is increasing worldwide and especially in the middle-east (1e3). Obesity and overweight can result from several factors (1e8). In general, it is about the interaction of environmental factors (turbid by the food behavior and/or Received 12/05/10; Revised 01/19/11; Accepted 01/20/11. *Address correspondence to: Rawad El Hage, PhD, Division of Physical Education, Faculty of Arts and Social Sciences, University of Balamand, P.O. Box 100, Tripoli, Lebanon. E-mail: [email protected]
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BMD in Overweight Boys mineral density (aBMD), and bone strength indices in adolescents (9e19). However, these studies have given conflicting results. It is argued that obese and overweight adolescents have higher, equivalent, or lower aBMD and BMC when compared with controls (9e19). This may be explained partially by the following factors. Firstly, the relation between fat mass and aBMD in adolescence is influenced by sex (20e22). In reality, fat mass is more strongly related to the aBMD in girls than boys (20). Secondly, body weight is strongly related to the aBMD of the weight-bearing bones and to a lesser extent to the aBMD of the noneweight-bearing bones (18,19). Finally, the question of adjusting BMC and aBMD values for weight, lean mass, or body mass index (BMI) to judge the effects of overweight and obesity on these parameters remains open (11e14,18). Therefore, the aim of this study was to compare whole body (WB), total hip (TH), lumbar spine, and forearm aBMD in overweight and control adolescent boys. We hypothesized that overweight boys should have higher aBMD at the weight-bearing sites when compared with controls because being overweight is associated with higher lean mass for height (13,17).
Material and Methods Subjects and Study Design The study participants (n 5 60) were recruited from 5 private schools in Beirut, Lebanon. Inclusion criteria were being adolescent (Tanner stage between 3 and 5) boys from 14 to 20 yr of age with no diagnosis of comorbidities and no history of fracture. The boys were nonsmokers and had no history of major orthopedic problems or other disorders known to affect bone metabolism. Boys were divided into a group of overweight (BMI O 25 kg/m2; n 5 27) and a group of control boys (BMI ! 25 kg/m2; n 5 29). These 2 groups were matched for pubertal status. This study did not include extremely lean (BMI ! 16 kg/m2) boys or extremely obese (BMI O 40 kg/m2) boys. Four boys were excluded from this study because they were extremely obese or extremely lean. An informed written consent was obtained from the children and their parents. This study was approved by the University of Balamand Ethics Committee.
Anthropometric Measurements Height (cm) was measured in the upright position to the nearest 1 mm with a Seca standard stadiometer. Body weight (kg) was measured on a Taurus mechanic scale with a precision of 100 g. The boys were weighed wearing only underclothes. BMI was calculated as body weight divided by height squared (kg/m2). Body composition (lean mass, fat mass, and fat mass percentage) was assessed by dual-energy X-ray absorptiometry (DXA) (DXA Hologic QDR-4500W; Waltham, MA). In our laboratory, the in vivo coefficients of variation were !1% for fat and lean mass. A single operator performed and analyzed all DXA scans to standardize the analyses. Daily quality control scans were performed with the manufacturer’s phantom. Journal of Clinical Densitometry: Assessment of Skeletal Health
123 Bone Measurements BMC (g), bone mineral area (BMA, in cm2), and aBMD (g/cm2) were determined for each individual. The DXA measurements were completed for the WB at the lumbar spine (L2eL4), at the TH, at the femoral neck (FN), at the ultra distal (UD) Radius, at the 1/3 Radius, at the mid Radius, and at the total Radius using the instrument previously described. The Hologic APEX software, version 2 (1986e2007, Hologic Inc., Bedford, MA) was used to analyze the DXA scans on the Hologic machine. In our laboratory, the coefficients of variation were !1% for BMC and aBMD. Bone mineral apparent density (BMAD) (g/cm3), an estimate of volumetric bone density, was calculated as previously described (23). For WB, the formula BMAD 5 BMC/[WB (BMA2)/body height] was used. The expressions BMC/height and aBMD/height were used to adjust for whole-body bone size (14,24). The same certified technician performed all bone measurements using the same machine.
Pubertal Status Assessment Tanner pubertal status was determined by self-evaluation, a method of recognized validity and reliability (25). Children were provided with line drawings of the 5 Tanner stages and were instructed by a research assistant to choose the drawing that best represented their current stage of development. Children completed the form in a private setting away from the other children.
Birth Weight and Breast-Feeding Birth weights (kg) were obtained from the obstetric records. The duration (mo) of breast-feeding was recorded by the mothers. No distinction was made between exclusive and partial breast-feeding.
Daily Calcium Intake The estimation of the DCI was based on a frequency questionnaire (26). Selection of items was based on the food composition diet, frequency of use, and relative importance of food items as a calcium source. The total number of foods was 30 items. The questionnaire included the following food items: milk and dairy products, including calciumenriched items such as yoghurt, cheese, and chocolate. Items such as eggs, meat, fish, cereals, bread, vegetables, and fruits were also included. Adequacy of calcium in the subjects was assessed using the adequate intake guidelines of 1300 mg of calcium.
Physical Activity Exercise frequency was assessed from a questionnaire inquiring about the number of hours spent on sports per week (organized sports plus leisure-time activity). This questionnaire included questions on physical education classes, formal and informal activities, activities done at school, activities done out of school in sports clubs or gyms, and activities done at home. Volume 14, 2011
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Statistical Analysis Basic data are presented as mean standard deviation (Tables 1 and 2) or as mean standard error (Table 3). Chisquared tests were used to test the Tanner stage distribution between the 2 groups. Comparisons between the overweight and the control group were made after checking for Gaussian distribution. If Gaussian distribution was found, parametric unpaired t-tests were used. In other cases, ManneWhitney U-tests were used. Associations between clinical characteristics and bone data were given as Pearson correlation coefficients (for normally distributed variables) or Spearman correlation coefficients (for nonnormally distributed variables). Multiple linear regression analysis models were used to test the relationship between aBMD with age, lean mass, and height; and between WB BMC with age, height, lean mass, and fat mass; and r2 were reported. Bone data were compared after adjustment for total body weight, height, lean mass, BMI, fat mass, age, and Tanner stage using a one-way analysis of covariance. The difference was considered statistically significant at p ! 0.05. Data were analyzed using Number Cruncher Statistical System (2001).
Results Clinical Characteristics of the Subjects Clinical characteristics of the adolescent boys are displayed in Table 1. Tanner stage distributions did not differ between overweight and control boys. Age, mean Tanner
Table 1 Clinical Characteristics of Overweight and Control Adolescent Boys Parameter
Overweight (n 5 27)
Controls (n 5 29)
Age (yr) 17.1 2.1 16.7 2.0 Tanner (Nd3/4/5) 5/10/12 6/13/10 Tanner (%d3/4/5) 19/37/44 21/45/34 Birth weight (kg) 3.62 0.42 3.36 0.47 Breast-feeding (mo) 7.7 6.2 9.9 8.0 Weight (kg) 91.9 14.6*** 64.2 7.8 Height (cm) 174.0 5.7 173.2 5.6 BMI (kg/m2) 30.3 4.2*** 21.4 2.1 Lean mass (kg) 64.6 6.9*** 52.3 15.4 Lean mass/height (kg/cm) 0.352 0.033*** 0.292 0.031 Fat mass (kg) 24.7 8.1*** 9.6 3.0 Fat mass (%) 26.9 6.3*** 15.1 3.4 DCI (mg/d) 1,131 465 945 225 PA (h/wk) 3.5 2.5 4.2 2.4 Note: In italic: ManneWhitney U-tests were used; in normal font: parametric unpaired t-tests were used. Abbr: BMI, body mass index; DCI, daily calcium intake; PA, physical activity. ***p ! 0.001. Journal of Clinical Densitometry: Assessment of Skeletal Health
Table 2 Bone Characteristics of Overweight and Control Adolescent Boys Overweight (n 5 27)
Controls (n 5 29)
WB BMC (g) 2472 323* 2200 398 WB BMA (cm2) 2218 149*** 2044 179 WB aBMD (g/cm2) 1.11 0.08 1.07 0.12 WB BMC/height 14.2 1.6** 12.7 2.2 (g/cm) WB aBMD/height 0.0064 0.0004 0.0061 0.0006 (g/cm3) 0.087 0.005* 0.091 0.006 WB BMAD (g/cm3) L2eL4 aBMD (g/cm2) 0.993 0.119* 0.914 0.125 TH aBMD (g/cm2) 1.053 0.136** 0.949 0.140 FN aBMD (g/cm2) 0.978 0.140* 0.880 0.145 UD Radius aBMD 0.442 0.049* 0.410 0.060 (g/cm2) 0.698 0.060 0.679 0.072 1/3 Radius aBMD (g/cm2) 0.583 0.062 0.553 0.075 Mid Radius aBMD (g/cm2) 0.577 0.056 0.547 0.070 Total Radius aBMD (g/cm2) Note: In italic: ManneWhitney U tests were used; in normal font: parametric unpaired t-tests were used. Abbr: WB, whole body; BMC, bone mineral content; BMA, bone mineral area; aBMD, areal bone mineral density; BMAD, bone mineral apparent density; TH, total hip; FN, femoral neck; UD, ultra distal. *p ! 0.05; **p ! 0.01; ***p ! 0.001.
stage, birth weight, breast-feeding duration, height, physical activity (h/wk), and DCI were not different between overweight and control boys. However, body weight, lean mass, fat mass, fat mass percentage, and BMI were higher in overweight boys when compared with controls ( p ! 0.001).
Crude Bone Measurements in Overweight and Control Boys WB BMC, WB BMA, and WB BMC/height were higher ( p ! 0.05) in overweight boys when compared with controls. L2eL4, TH, FN, and UD Radius aBMD were higher in overweight boys compared with controls ( p ! 0.05). Finally, WB BMAD was higher in control boys when compared with overweight boys ( p ! 0.05) (Table 2).
Correlations Between Clinical Characteristics and Bone Data Age and Tanner stage were positively related to WB BMC, WB BMA, L2eL4 aBMD, UD aBMD, mid Radius aBMD, 1/3 Radius aBMD, and total Radius aBMD ( p ! 0.05). Weight, BMI, lean mass, and the ratio lean mass/height were positively related to WB BMC, WB BMC/height, WB Volume 14, 2011
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Table 3 Bone Data Adjusted for Body Weight, Lean Mass, and BMI in Overweight and Control Adolescent Boys Adjusted for body weight Overweight (n 5 27)
Controls (n 5 29)
Adjusted for lean mass Overweight (n 5 27)
Controls (n 5 29)
Adjusted for BMI Overweight (n 5 27)
Controls (n 5 29)
WB BMC (g) 2252 59 2450 63 2264 46 2437 49 2308 67 2386 71 WB BMA (cm2) 2101 24 2176 26 2114 17 2162 19 2136 30 2137 32 WB aBMD (g/cm2) 1.06 0.01 1.12 0.02 1.06 001 1.12 0.01 1.07 0.02 1.11 0.02 WB BMC/height 13.1 0.3 13.9 0.3 13.2 0.2 13.8 0.2 13.2 0.3 13.7 0.3 (g/cm) WB aBMD/height 0.0062 0.0001 0.0063 0.0001 0.0062 0.0001 0.0063 0.0001 0.0061 0.0001 0.0064 0.0001 (g/cm3) 0.091 0.001 0.086 0.001 0.092 0.001 0.087 0.001 0.090 0.001 WB BMAD (g/cm3) 0.086 0.001 L2eL4 aBMD 0.990 0.024 1.007 0.024 0.983 0.025 1.014 0.024 0.992 0.025 1.005 0.024 (g/cm2) 0.923 0.021 0.978 0.020 0.945 0.021 0.952 0.022 0.934 0.022 0.968 0.021 TH aBMD (g/cm2) FN aBMD (g/cm2) 0.903 0.025 0.949 0.024 0.936 0.025 0.911 0.026 0.907 0.025 0.944 0.024 UD Radius aBMD 0.422 0.010 0.428 0.009 0.428 0.010 0.425 0.010 0.423 0.010 0.427 0.010 (g/cm2) 0.688 0.012 0.706 0.017 0.676 0.012 0.700 0.112 0.675 0.012 0.699 0.012 1/3 Radius aBMD (g/cm2) 0.551 0.012 0.581 0.012 0.560 0.013 0.574 0.013 0.556 0.012 0.576 0.012 Mid Radius aBMD (g/cm2) 0.573 0.011 0.556 0.012 0.567 0.012 0.547 0.011 0.573 0.011 Total Radius aBMD 0.547 0.011 (g/cm2) Note: Values are means standard error. Abbr: WB, whole body; BMC, bone mineral content; aBMD, areal bone mineral density; BMAD, bone mineral apparent density; TH, total hip; FN, femoral neck; UD, ultra distal.
BMA, WB aBMD, WB aBMD/height, L2eL2 aBMD, TH aBMD, FN aBMD, UD Radius aBMD, mid Radius aBMD, and total Radius aBMD ( p ! 0.05). Fat mass was positively related to WB BMC (r 5 0.44; p ! 0.01), WB aBMD (r 5 0.28; p ! 0.05), WB BMC/height (r 5 0.43; p ! 0.01), WB BMA (r 5 0.58; p ! 0.001), TH aBMD (r 5 0.30; p ! 0.01), and negatively associated with WB BMAD (r 5 0.37; p ! 0.05). Birth weight was only related to WB BMAD (r 5 0.52; p ! 0.01). Breast-feeding duration (mo) and DCI (mg/d) were not significantly correlated to bone data. Finally, physical activity (h/wk) was only correlated to FN aBMD (r 5 0.26; p ! 0.05) (Table 4).
Multiple Linear Regression Analysis Models Fat mass was not significantly related to WB BMC after adjusting for age, height, and lean mass. Moreover, age and lean mass explained 45% of the lumbar spine aBMD variance and 47% of total Radius aBMD variance.
Adjusted Bone Data in Overweight Boys and Controls Bone characteristics adjusted for weight, lean mass, and BMI are shown in Table 3. After adjusting for weight, lean mass, BMI, or fat mass, WB BMC, WB BMA, WB BMC/height, Journal of Clinical Densitometry: Assessment of Skeletal Health
WB aBMD/height, WB BMAD, and aBMD (WB, L2eL4, TH, FN, UD Radius, 1/3 Radius, mid Radius, and total Radius) were not different between the 2 groups (overweight and controls). After adjusting for height, age, or Tanner stage, overweight boys had higher WB BMC, WB BMA, WB BMC/height, L2eL4 aBMD, TH aBMD, FN aBMD, and UD Radius aBMD values when compared with controls ( p ! 0.05).
Discussion The main findings of this study were that WB BMC, WB BMC/height, L2eL4 aBMD, TH aBMD, and UD aBMD were higher in overweight boys compared with controls and that after adjustment for weight, lean mass, fat mass, or BMI, there were no differences in BMC or aBMD between the 2 groups. Upto our knowledge, it’s the first study that compared BMD of several bone sites in overweight and control adolescent boys from Lebanon. Concerning the morphological characteristics, the ratio lean mass/height was higher in overweight boys compared with controls. This result is in accordance with those of several previous studies (13,14,17). In reality, being overweight is usually associated with increased lean mass, fat mass, and bone mass (12e14). Volume 14, 2011
0.65*** 0.64*** 0.40** 0.31* 0.35** 0.48*** 0.47*** 0.17 0.06 Note: In italic: Spearman coefficient of correlation; in normal font: Pearson coefficient of correlation. Abbr: WB, whole body; aBMD, areal bone mineral density; TH, total hip; FN, femoral neck; UD, ultra distal. *p ! 0.05; **p ! 0.01; ***p ! 0.001.
0.63*** 0.63*** 0.36** 0.38** 0.29* 0.46*** 0.43** 0.11 0.00 0.57*** 0.50*** 0.41** 0.17 0.42** 0.45** 0.46** 0.28 0.22 0.16 0.14 0.50*** 0.26 0.46*** 0.53*** 0.53*** 0.33* 0.26 0.30* 0.20 0.50*** 0.22 0.46*** 0.51*** 0.52*** 0.30* 0.20 0.50*** 0.43*** 0.47*** 0.36** 0.45*** 0.55*** 0.53*** 0.28 0.18 0.42** 0.23 0.29* 0.07 0.32* 0.39** 0.41** 0.21 0.11 Age (yr) Tanner (mean) Weight (kg) Height (cm) BMI (kg/m2) Lean mass (kg) Lean mass/height (kg/cm) Fat mass (kg) Fat mass (%)
0.46*** 0.27 0.39** 0.32* 0.34* 0.58*** 0.56*** 0.28* 0.15
Mid Radius aBMD (g/cm2) 1/3 Radius aBMD (g/cm2) UD Radius aBMD (g/cm2) FN aBMD (g/cm2) TH aBMD (g/cm2) L2eL4 aBMD (g/cm2) WB aBMD/ height (g/cm3) WB aBMD (g/cm2)
Table 4 Correlations Between Clinical Characteristics and Bone Mineral Density Values
0.65*** 0.64*** 0.40** 0.31* 0.35** 0.50*** 0.48*** 0.17 0.07
El Hage et al. Total Radius aBMD (g/cm2)
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Birth weight was not different between the 2 groups. Low birth weight has been found to be associated with a higher BMI in adults (5). The effect of birth weight on BMI may not be detected when the study population is too small. Breast-feeding duration was not different between the 2 groups. Several studies in Western societies have reported the protective effects of breast-feeding against childhood obesity (5e7). However, in our study, no clear association between breast-feeding duration and BMI was found. We suggest that genetic or environmental factors other than breast-feeding have a greater effect on BMI at this age. In our study, overweight boys had higher WB BMC, WB BMA, and WB BMC/height when compared with controls. Overweight and obesity during adolescence augment bone mass and dimensions (13). In addition, aBMD of the weight-bearing bones (lumbar spine, TH, and FN) was higher in overweight boys compared with controls, whereas aBMD of the WB, the 1/3 Radius, the mid Radius, and the Total Radius was not significantly different between the 2 groups. Thus, this study reinforces the hypothesis, which states that obesity and overweight have a site-specific effect on aBMD (18,19,27). In reality, the influence of obesity and overweight on weight-bearing bones is the result of load, this effect being comparable to the influence of physical activity (28). Overall, this study suggests a positive effect of overweight and obesity on aBMD of the weight-bearing bones in adolescent boys. Overweight and obesity may influence bone mass by another mechanism (29). Free sex hormones, insulin, insulin-like growth-factor-I, leptin, amylin, and preptin concentrations increase with obesity; these hormones can stimulate the osteoblastic activity and decrease the osteoclastic activity and may positively influence the aBMD of the weight-bearing and the noneweight-bearing bones (29). Wetzsteon et al. (30) showed in a longitudinal study (16 mo) conducted on overweight children that change in bone strength was positively related to change in lean mass and muscle cross sectional area but not to fat mass. In our study, lean mass was a stronger positive determinant of BMC, BMA, and aBMD than fat mass. Moreover, fat mass was not positively associated to WB BMC after adjusting for age, height, and lean mass. These results suggest that fat mass is not an independent determinant of BMC in boys. In actual fact, aBMD adapts primarily to dynamic (lean mass) rather than static loads (fat mass) (17). Interestingly, the relation between fat mass and bone mass in adolescents is highly influenced by sex (20e22,31). In truth, we have previously reported that fat mass is a positive determinant of lumbar spine aBMD and WB BMC in adolescent girls but not in adolescent boys (20). Age, Tanner stage, weight, lean mass, and BMI were positively related to BMC, BMA, and aBMD values. These results are in accordance with those of several previous studies conducted on adolescents (12e14,28). Fat mass was negatively associated with WB BMAD. This result is in line with that reported by Rocher et al. (18). In fact, the BMA/height and BMA2/height ratios were higher in overweight boys compared with controls in this study. Volume 14, 2011
BMD in Overweight Boys After adjustment for weight, lean mass, BMI, or fat mass, there were no differences in bone data between overweight and control boys. Thus, BMC and aBMD of the overweight boys adapt to the increased weight and lean mass. Furthermore, after adjustment for age or Tanner stage, overweight boys displayed higher WB BMC, WB BMA, WB BMC/ height, L2eL4 aBMD, TH aBMD, FN aBMD, and UD Radius aBMD values when compared with controls. Therefore, this study suggests that being overweight is associated with higher BMC and aBMD for age in adolescent boys. Physical activity (h/wk) was positively related to FN aBMD but not to lumbar spine aBMD. In fact, the genetic effect appears to be greater in the lumbar spine compared with the FN (32). It is possible that physical activity exerts a greater effect on the cortical component of the bony structure of the femur (32,33). Birth weight was not significantly related to BMC or aBMD and was negatively related to WB BMAD. This result is in contrast with that of our previous study conducted on adolescent girls in whom we showed that birth weight was positively associated with WB BMC, WB BMC/height, and WB aBMD (34). Accordingly, the relation between birth weight and BMC or aBMD in adolescents may be influenced by sex. Breast-feeding duration was not related to bone data in this group of adolescent boys. Further, large studies are necessary to better understand the relation between breastfeeding duration and bone mass in adolescents. In this study, mean DCI was below the daily requirements for this age group (1300 mg) (35). These results are in line with those of several reports, which measured DCI in Lebanese adolescents (14,36e38). In addition, DCI was not significantly related to bone data. These results are in agreement with those of several cross-sectional studies conducted on adolescents (14,20,21). The lack of correlation between DCI and bone data may be because of the cross-sectional nature of this study. The present study has several strengths. First, it is one of the few studies that explored the effects of being overweight on BMC and aBMD of several bone sites in pubertal boys. Secondly, this study aimed at studying the effects of being overweight on BMC and aBMD of weight-bearing and noneweight-bearing bones. Lastly, this study was conducted on Lebanese adolescents; it is well known that Lebanese adolescents have mean aBMD values, which are lower than Western normative values (38). We acknowledge several limitations of the study. Firstly, the cross-sectional nature of the study is a limitation because it cannot evaluate the confounding variables. Secondly, the small number of subjects and the matching method is a limitation. Thirdly, there are well-known difficulties in assessing diet, sexual maturation, and physical activity using self-reported questionnaires (39,40). For instance, Tanner self-assessment does not provide a high degree of accuracy of sexual maturation in obese children (39). Moreover, food-frequency questionnaires provide limited list of foods and do not allow specific ingredients to be entered for analysis (40). Fourthly, aBMD measured with DXA is a surrogate for bone strength but not Journal of Clinical Densitometry: Assessment of Skeletal Health
127 a measurement of it (41). In fact, bone strength is not only determined by the amount of bone mineral, but also by its partial distribution with respect to the loading forces that may be encountered (41). Therefore, further investigations on bone geometry and microarchitecture are necessary to better understand the effects of being overweight on the growing skeleton. Finally, according to Bolotin and Siev€anen (42), DXAmeasured in vivo BMD inaccuracies are patient specific, because the magnitude of the BMD value extracted from a given DXA measurement depends on the exact specifications of the bone marrow composition, the detailed composition of the extraosseous soft tissue, and the true (not measured) value of BMD (i.e., proportional to the average thickness of bone material along all X-ray paths traversing the given bone site) actually pertaining within the specific scan region of interest (ROI) of each given patient. Moreover, for any given extraosseous soft-tissue composition in the scan ROI, the more yellow the bone marrow the more DXA underestimates true BMD. Furthermore, for any given bone marrow composition, the smaller the proportion of fat in the extraosseous lean tissue the more the DXA-measured BMD underestimates the true value (42). In conclusion, this study suggests a positive effect of BMI on crude bone mineral density of the weight-bearing bones (lumbar spine, hip, and FN) in adolescent boys. However, after adjustment for weight, lean mass, or BMI, there are no differences between overweight and control adolescent boys regarding aBMD of the WB, the lumbar spine, the hip, and the forearm.
Acknowledgments This study was supported by a grant from the research council of the University of Balamand, Lebanon.
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