J Bone Miner Metab (2009) 27:629–633 DOI 10.1007/s00774-009-0074-6
SHORT COMMUNICATION
Total body, lumbar spine and hip bone mineral density in overweight adolescent girls: decreased or increased? Rawad El Hage Æ Christophe Jacob Æ Elie Moussa Æ Claude-Laurent Benhamou Æ Christelle Jaffre´
Received: 10 December 2008 / Accepted: 29 January 2009 / Published online: 17 April 2009 Ó The Japanese Society for Bone and Mineral Research and Springer 2009
Abstract Despite the epidemic of overweight adolescents, the effect of being overweight on bone mineral density (BMD) during this period is poorly understood. However, recent studies have suggested that overweight adolescents have lower BMD compared to normal-weighted adolescents after adjusting for body weight. The aim of this study was to determine the influence of being overweight on bone status in a group of adolescent girls. This study included 22 overweight (BMI [25 kg/m2) adolescent girls (15.4 ± 2.4 years old) and 20 maturation-matched (15.2 ± 1.9 years old) controls (BMI \25 kg/m2). Bone mineral area, bone mineral content, BMD at the whole body (WB), lumbar spine (L2–L4), femoral neck (FN), total hip (TH) and body composition (lean mass and fat mass) were assessed by dual-energy X-ray absorptiometry (DXA). Calculation of the bone mineral apparent density (BMAD) was completed for the WB and for L2–L4. Expressed as crude values, DXA measurements of BMD at all bone sites (TB, L2–L4, TH and FN) were higher in R. El Hage C. Jacob E. Moussa Laboratoire de Physiologie et de Biome´canique de la Performance Motrice, Universite´ de Balamand, Al Koura, Lebanon R. El Hage C.-L. Benhamou C. Jaffre´ UMR-S658, CHR d’Orle´ans, CHR d’Orle´ans-Porte Madeleine, BP 2439, 45032 Orle´ans Cedex 1, France R. El Hage (&) Department of Physical Education, Faculty of Art and Social Science, University of Balamand, P.O. Box 100, Tripoli, Lebanon e-mail:
[email protected] R. El Hage Rue Principale, Immeuble Abdallah Jabbour, Pre`s Pharmacie Antelias, Antelias-Metn, Lebanon
overweight adolescent girls compared to controls. After adjusting for either body weight, lean mass or fat mass, these differences disappeared. Finally, BMAD of the L2– L4 remained higher in overweight girls compared to controls after adjusting for lean mass. We conclude that overweight adolescent girls do not have lower BMD when compared with controls, even when BMD values are adjusted for weight, lean mass or fat mass. Keywords Bone mass Menarche Body weight Lean mass Fat mass
Introduction During the last 2 decades, there has been an increase in the prevalence of overweight among adolescents in several industrialized and developing countries, turning overweight into a public health problem [1, 2]. In women, it is well established that being overweight is associated with higher bone mineral density (BMD) and decreased risk of fracture [3]. In contrast, recent studies conducted in children and adolescents showed that being overweight is not only linked to orthopedic disorders, such as slipped capital epiphyses of the femora, scoliosis and genu valga [1], but also to an increased risk for forearm fractures [4, 5]. However, in adolescents, other studies using dual-energy X-ray absorptiometry (DXA) to examine the effect of overweight on BMD in adolescents have yielded conflicting results [6–10]. These differences may be related to differing approaches for the assessment of two-dimensional projected DXA bone measures relative to age, bone size and body size. In addition, one can notice that not all of these studies have taken into account the level of physical activity and the daily calcium intake despite the fact that
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these factors are well known to influence bone mass. Nevertheless, it is also known that obese and overweight children and adolescents tend to be less active than leaner controls [1, 2, 8]. Finally, it is important to note that some authors have suggested that overweight and obese children and adolescents have decreased bone mass relative to body weight [6–8]. For Rocher et al. [8], the influence of overweight on BMD might be site-specific. Thus, the purpose of this study was to investigate the influence of overweight (BMI [25 kg/m2) on total body, lumbar spine and hip BMD of adolescent girls by comparison to control (BMI \25 kg/m2) girls in a cross-sectional study; these two groups were matched for physical activity and for daily calcium intake.
Subjects and methods Subjects and study design The study participants were recruited from four private schools in Beirut, Lebanon. Inclusion criteria were being post-menarcheal (at least 1 year of regular menstrual cycles), adolescent, sedentary (practicing less than 2 h of physical activity per week and not involved in impact sports) girls from 12 to 20 years of age with no diagnosis of comorbidities and no history of fracture. The girls were non-smokers and had no history of major orthopedic problems or other disorders known to affect bone metabolism. Moreover, girls participating in this study were not pregnant and had not taken hormonal contraceptives for the past 6 months [11]. In this study, the number of years since menarche was considered as a maturation index (MI). Girls were divided into a group of overweight (BMI [25 kg/m2; n = 22) and a group of control girls (BMI \25; n = 20). These two groups were matched for physical activity. An informed written consent was obtained from the children and their parents. This study was approved by the University of Balamand Ethics Committee [11]. 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 girls were weighed wearing only underclothes. BMI was calculated as body weight divided by height squared (kg/m). Body composition (lean mass, fat mass, body fat percentage) was measured by dualenergy DXA (Dexa Hologic QDR-4500W; Waltham,
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Mass.). In our laboratory, the in vivo coefficients of variation were 1.13 and 0.54% for fat and lean mass, respectively [11]. Bone mass measurements Bone mineral content (BMC, in g) and density (BMD, in g/ cm2) were determined for each individual. The DXA measurements were completed for the whole body (WB), at the lumbar spine (L2–L4), at the total hip (TH) and at the femoral neck (FN) using the instrument previously described. In our laboratory, the coefficients of variation were\1% for BMC and BMD [11]. Bone mineral apparent density (BMAD) (g/cm3), an estimate of volumetric bone density, was calculated as previously described [12]. For WB, the formula BMAD = BMC/[WB bone mineral area (BMA2)/body height] was used, and for L2–L4, the formula BMAD = BMC (L2–L4)/L2–L4 BMA3/2 [12]. The same certified technician performed all analyses using the same technique for all measurements. Daily calcium intake The estimation of the daily calcium intake was based on a frequency questionnaire [13]. 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 calcium-enriched 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 1,300 mg of calcium. Statistical analysis Basic data are presented as mean ± standard deviation (SD) (Tables 1, 2) or as mean ± standard error (SE) (Table 3). 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, Mann–Whitney U tests were used. Associations between anthropometrics and bone data were given as Pearson correlation coefficients. DXA values were compared after adjustment for total body weight, lean mass and fat mass using a one-way analysis of covariance (ANCOVA). The difference was considered statistically significant at P \ 0.05. Data were analyzed using NCSS (2001).
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Table 1 Clinical characteristics of the overweight and control adolescent girls Overweight (n = 22) Age (years)
15.4 ± 2.4
MI (years)
3.7 ± 3.0
Body weight (kg) Height (cm)
73.5 ± 10.9*** 160.3 ± 6.1
Controls (n = 20) 15.2 ± 1.9 2.8 ± 2.2 55.0 ± 10.8 159.9 ± 4.7
BMI (kg/m2)
28.5 ± 2.7***
21.5 ± 3.3
Fat mass (kg)
29.0 ± 5.7***
16.7 ± 5.8
Lean mass (kg)
42.4 ± 5.1***
36.9 ± 4.8
Fat mass (%)
39.3 ± 3.0***
29.0 ± 5.8
Daily calcium intake (mg/days)
748 ± 274
783 ± 285
Values are mean ± SD MI maturation index (years since menarche), BMI body mass index * P \ 0.05; ** P \ 0.01; *** P \ 0.001
Table 2 Crude bone mineral values in overweight and control adolescent girls
WBBMC (g) WBBMA (cm2) 2
Overweight (n = 22)
Controls (n = 20)
1,936 ± 310**
1,698 ± 207
1,869 ± 170**
1,735 ± 136
WBBMD (g/cm )
1.031 ± 0.091*
0.976 ± 0.070
WBBMAD (g/cm3)
0.088 ± 0.006
0.090 ± 0.006
LSBMD (g/cm2)
0.970 ± 0.125*
0.891 ± 0.108
LSBMAD (g/cm3)
0.148 ± 0.015**
0.133 ± 0.014
THBMD (g/cm2)
0.887 ± 0.103*
0.816 ± 0.083
0.844 ± 0.108**
0.756 ± 0.114
2
FNBMD (g/cm ) Values are mean ± SD
WB whole body, BMC bone mineral content, BMA bone mineral area, BMD bone mineral density, BMAD bone mineral apparent density, LS lumbar spine (L2–L4), TH total hip, FN femoral neck * P \ 0.05; ** P \ 0.01
Results Characteristics of the subjects Clinical characteristics of adolescent girls are displayed in Table 1. Age, MI, height and daily calcium intake were not different between the two groups. Overweight girls had a significantly higher total body weight, fat mass, lean mass and BMI compared to controls (P \ 0.001). Crude bone measurements Bone measurements expressed as crude values are presented in Table 2. Overweight girls had higher whole-body BMC (P \ 0.01), whole-body BMA (P \ 0.01), wholebody BMD (P \ 0.05), TH BMD (P \ 0.05), FN BMD (P \ 0.01), lumbar spine BMD (P \ 0.05) and lumbar spine BMAD (P \ 0.01) when compared to controls. Whole-body BMAD was not statistically different between overweight and control girls. Associations between anthropometrics and crude bone measurements Body weight, lean mass, fat mass and BMI were all positively correlated to whole-body BMC, whole-body BMA, whole-body BMD, LSBMD, LSBMAD, THBMD and FNBMD (P \ 0.01) (Table 3). Adjusted bone mineral values X-ray absorptiometry measurements adjusted for body weight, lean mass and fat mass are shown in Table 4. When measurements were adjusted for either BMI, body weight or fat mass, BMD (TB, L2–L4, TH and FN), BMC (WB) and BMAD (WB and L2–L4) were not different between the two groups. Finally, when measurements were adjusted for lean mass, BMD (TB, L2–L4, TH and FN) and
Table 3 Correlations (r) between anthropometrics and crude bone mineral values
Body weight (kg) 2
WBBMC (g)
WBBMA (cm2)
WBBMD (g/cm2)
WBBMAD (g/cm3)
LSBMD (g/cm2)
LSBMAD (g/cm3)
THBMD (g/cm2)
FNBMD (g/cm2)
0.76***
0.86***
0.49***
-0.24
0.58***
0.54***
0.56***
0.64***
BMI (kg/m )
0.64***
0.72***
0.46**
-0.23
0.53***
0.54***
0.51***
0.58***
Fat mass (kg)
0.69***
0.77***
0.45**
-0.20
0.54***
0.56***
0.53***
0.59***
Lean mass (kg)
0.77***
0.86***
0.49***
-0.24
0.55***
0.43**
0.56***
0.66***
WB whole body, BMC bone mineral content, BMA bone mineral area, BMD bone mineral density, BMAD bone mineral apparent density, LS lumbar spine (L2–L4), TH total hip, FN femoral neck, BMI body mass index ** P \ 0.01; *** P \ 0.001
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Table 4 Bone mineral values adjusted for body weight, lean mass and fat mass in overweight and control adolescent girls Adjusted for body weight
Adjusted for lean mass
Adjusted for fat mass
Overweight (n = 22)
Controls (n = 20)
Overweight (n = 22)
Controls (n = 20)
Overweight (n = 22)
Controls (n = 20)
WBBMC (g)
1,779 ± 39
1,870 ± 41
1,836 ± 40
1,807 ± 42
1,765 ± 44
1,885 ± 46
WBBMD (g/cm2)
1.004 ± 0.016
1.005 ± 0.017
1.013 ± 0.016
0.995 ± 0.017
1.002 ± 0.016
1.007 ± 0.017
WBBMAD (g/cm3) LSBMD (g/cm2)
0.089 ± 0.001 0.921 ± 0.021
0.089 ± 0.001 0.945 ± 0.022
0.089 ± 0.001 0.940 ± 0.022
0.089 ± 0.001 0.923 ± 0.023
0.089 ± 0.001 0.914 ± 0.022
0.089 ± 0.001 0.952 ± 0.023
LSBMAD (g/cm3)
0.144 ± 0.003
0.137 ± 0.003
0.146 ± 0.003*
0.134 ± 0.003
0.142 ± 0.002
0.138 ± 0.003
THBMD (g/cm )
0.850 ± 0.018
0.855 ± 0.018
0.862 ± 0.017
0.842 ± 0.018
0.846 ± 0.018
0.860 ± 0.019
FNBMD (g/cm2)
0.792 ± 0.019
0.813 ± 0.020
0.808 ± 0.019
0.794 ± 0.020
0.788 ± 0.020
0.817 ± 0.021
2
Values are mean ± SE WB whole body, BMC bone mineral content, BMD bone mineral density, BMAD bone mineral apparent density, LS lumbar spine (L2–L4), TH total hip, FN femoral neck * P \ 0.05; ** P \ 0.01
BMC (WB) were not different between the two groups; however, overweight girls had higher L2–L4 BMAD in comparison to controls (P \ 0.05).
Discussion The main findings of this study were that, after adjustment for either body weight, lean mass or fat mass, overweight girls did not have lower BMC or BMD at all bone sites (total body, lumbar spine, TH and FN) in comparison to controls. Hence, this study suggests that the skeleton of the overweight girls adapts to the increased body weight. Regarding the crude values measured by DXA, overweight girls had heavier, larger and denser bones than controls, which is in accordance with previous studies stating that body weight might improve bone mineralization in overweight children and adolescents by increasing the mechanical loading on weight-bearing bones [9, 10]. In addition, anthropometrical characteristics (weight, lean mass, fat mass and BMI) were positively correlated with BMD at all bone sites (total body, lumbar spine, TH and FN). This result is in line with those of two previous studies [9, 10]. However, after adjusting for either weight, lean mass or fat mass, there were no differences in BMD at all bone sites (total body, lumbar spine, TH and FN). The results of this study are in line with those reported by Petit et al. [14] who showed that the femur bone geometry is appropriately adapted to lean mass in overweight adolescents. Because BMD is dependent on bone thickness, there is a risk of an overestimated value in tall people and an underestimated value in short people. Katzman et al. [12] suggested an equation to minimize the contributions of bone dimensions. Therefore, we included in our study an
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estimation of BMAD, which is BMC normalized to a derived bone reference volume. Our study shows that overweight girls had higher L2–L4 BMAD even when adjusted for lean mass in comparison to controls. However, the whole-body BMAD was not different between the two groups, even after adjusting for weight or lean mass. Our results show that there is a site-specific effect of overweight on BMAD. The lumbar spine is an axial and a weight-bearing site, mainly composed of trabecular bone. Rico et al. [15] highlighted that trabecular and cortical bone do not have the same sensitivity to mechanical stress, which could be a consequence of different metabolic activities of bone tissue. Bone metabolic activity is known to be more active in trabecular than in cortical bone tissue [15]. Cortical and trabecular bones showed different adaptation patterns in response to a mechanical stress, as has been already documented in studies concerning young tennis players [16]. In response to mechanical loading, cortical bone mainly increased its size, and trabecular bone preferentially enhanced its density [16]. Also, our results are in contrast with those reported by Goulding et al. [6]; they were not surprising. In fact, overweight and obesity in adolescence are associated with higher lean mass for height [9, 10]. Therefore, overweight individuals should have greater bone strength because of the greater muscle forces required to move the increased body weight [10]. Besides, overweight and obesity are associated with increased circulating leptin, free insulin-like growth factor 1, insulin and free sex hormones; all these hormones are well known to stimulate bone formation [17]. One previous study concluded that obesity does not have a protective effect on BMD in prepubertal boys and girls [8]. This result is in contrast with those of our study. Hence, one can hypothesize that maturity (pre- or postpubertal) may influence differently the relation between
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obesity and BMD. Additionally, we have recently shown that the relation between fat mass and BMD is sex specific [18]. Lastly, it is important to note that endocrine factors (e.g., hormones), which control BMD, are affected by the growth spurt, the weight status (obese or normal) and the gender [9–11, 17]. In conclusion, this study suggests that there is no difference concerning BMD in overweight adolescent girls compared with controls when values are adjusted for either weight, lean mass or fat mass. Finally, DXA data provide only quantitative information and do not allow the assessment of qualitative factors contributing to bone fragility [19]. Therefore, further investigations on bone geometry and microarchitecture are necessary to better understand the effects of overweight on bone parameters.
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