Introduction. Methods

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1 (2000) 24, 627±632 ß 2000 Macmillan Publishers Ltd All rights reserved 0307±0565/00 $ Overweight and obese children have low bone mass and area for their weight A Goulding 1 *, RW Taylor 2, IE Jones 1, KA McAuley 1, PJ Manning 1 and SM Williams 3 1 Department of Medicine, Otago University, Dunedin, New Zealand; 2 Department of Human Nutrition, Otago University, Dunedin, New Zealand; 3 Department of Preventive and Social Medicine, Otago University, Dunedin, New Zealand OBJECTIVES: To determine whether girls and boys categorized from body mass index () values as overweight or obese for their age have lower bone mineral content () or lower bone area in relation to total body weight than children of normal adiposity. DESIGN: Cross-sectional study in a university bone research unit. SUBJECTS: Two hundred girls and 136 boys aged 3 ± 19 y recruited from the general population by advertisement. MEASUREMENTS: Total body (g) and bone area (cm 2 ) measured by dual energy X-ray absorptiometry (DXA) in relation to body weight (kg), lean tissue mass (kg) and fat mass (kg) in boys and girls of three different percentile groupings: normal weight ( < 85th percentile); overweight (85 to 94th percentile); obese ( 95th percentile). RESULTS: Obese children had higher, bone area, and fat mass for chronological age than those of normal body weight (P < 0.001). In spite of this the observed values for age-adjusted total body and bone area relative to body weight were each lower than predicted values, in both overweight and obese children (2.5 ± 10.1% less, P < 0.05) than in children of lower adiposity. CONCLUSION: In overweight and obese boys and girls there is a mismatch between body weight and bone development during growth: their bone mass and bone area are low for their body weight. (2000) 24, 627±632 Keywords: obesity; bone development; body composition; DXA; future health risks Introduction The increasing prevalence of obesity in childhood and adolescence observed in many countries is currently a major public health concern. This rising adiposity may be due in part to decreased physical activity. 1±3 Since physical activity is strongly osteogenic during growth 4,5 diminished participation in weight-bearing exercise by overweight children could affect bone development adversely. Although there is a general perception that overweight children are skeletally advanced, 6 we recently observed that a high proportion of children with distal forearm fractures were overweight. In spite of this, our fracture cases had lower bone mass and bone area density throughout their skeletons than fracture-free controls, and we suggested that a low bone mineral content relative to body weight might make overweight children vulnerable to fragility fractures. 7,8 Others report low bone density in the spine and radius of overweight children 9±11 and orthopaedic problems such as slipped capital epiphyses of the femora, 12 scoliosis and tibia varu 13 are recognized health risks of childhood obesity. *Correspondence: Dr A Goulding, Department of Medicine, University of Otago, PO Box 913, Dunedin, New Zealand. ailsa.goulding@stonebow.otago.ac.nz Received 20 September 1999; accepted 16 December 1999 The present study was undertaken to test the hypothesis that overweight and obese fracture-free children and adolescents have low bone mass or low bone area for their body weight. We chose to examine relationships of bone mineral content and bone area to total body weight in the whole body rather than at regional bone sites because these represent the whole skeleton and are therefore less subject to variability in site-speci c maturation rates. No previous studies appear to have systematically evaluated the relationships of total bone mass or bone area to total body weight in fracture-free children of these differing grades of adiposity Methods New Zealand girls (n ˆ 200) and boys (n ˆ 136) aged 3 ± 19 y were recruited from the general population by advertisement for studies of bone health, anthropometry and nutrition. All were of Caucasian ethnicity. The protocol was approved by the Ethics Committee of our hospital and informed written consent was obtained from each participant and a parent or guardian. No children taking medication affecting either body weight or bone growth were enrolled. No child had broken any bone at any stage of life.

2 628 Subjects came to the study centre where they answered a short health questionnaire. Parents=caregivers helped younger children answer the questions. Pubertal development (Tanner stage) was assessed as described previously 7 and was con rmed in the boys after a physical examination by an endocrinologist. No measurements of bone age were obtained. Children were weighed and measured without shoes in light clothing and bone and body composition was measured by dual energy X-ray absorptiometry (DXA). Height was measured with a Harpenden stadiometer and weight with an electronic scale. Body mass index () was determined as body weight divided by height squared (kg=m 2 ). To measure total body bone mass (total bone mineral content,, (g)), total bone area (cm 2 ) and body composition (lean mass (kg), fat mass (kg), and fat percentage) a rectilinear total body scan was performed on each child using the fast or medium mode as appropriate for body size, with a Lunar DPX-L scanner (Lunar Corporation, Wisconsin, USA). 7 Subjects were allocated to three groups according to their calculated centile values for age, using standard reference data used in our hospital. 14 Group 1 were controls ( < 85th centile), group 2 were overweight ( > 85th centile and < 95th centile) and group 3 were obese ( 95 centile). Sexes were grouped separately. Descriptive results are presented as means and standard deviations. Stagewise regression was used to analyse the data. 15 In the rst stage log-transformed and total body area were regressed on age and age 2 and total body weight, which had also been logtransformed. This provided equations from which the expected value of the dependent variable was calculated. The residual or the difference between the observed value and the predicted value was also calculated for each observation. In the second stage of the regression analysis the residuals were used as the dependent variables and regressed on two dummy variables so that comparisons could be made between those with a between 85 ± 94th centile and those with a 95th centile with those with < 85th centile, the reference group. The analysis was repeated using total body lean mass (Table 4) and then total body fat mass (Table 5) instead of weight. It was necessary to use age 2 in the model to account for decreasing rates of bone growth among the older children. As the data were log transformed before analysis, the comparison between the observed values, and those predicted from the regression analysis was determined from ratios with 95% con dence intervals. Results Table 1 shows the main characteristics of our study population. Of the girls, 165 subjects (82.5%) had Table 1 Characteristics of our two study populations Girls Boys (n ˆ 200) (n ˆ 136) Age (y) 9.7 (4.2) 11.0 (4.2) 3.1 ± ± 19.9 Weight (kg) 34.5 (15.2) 42.2 (19.6) 15 ± ± 98 Height (cm) 135 (20.6) 145 (24.3) 94 ± ± 191 (kg=m 2 ) 18.0 (3.4) 18.8 (3.3) 13 ± ± 29.4 Lean mass (kg) 24.2 (9.0) 32.3 (14.7) 11 ± ± 70.7 Fat mass (kg) 8.4 (6.6) 7.7 (6.3) 1.4 ± ± 36.4 (g) 1257 (672) 1657 (925) 402 ± ± 4425 % Fat 22.1 (8.3) 17.3 (8.4) 9.4 ± ± 45.7 Bone area (cm 2 ) 1318 (498) 1628 (643) 607 ± ± 3131 Values are means with standard deviations shown in parentheses. Ranges are listed below each variable. values placing them in group 1, 22 (11%) in group 2, and 13 (6.5%) in Group 3. Of the boys, 111 subjects (81.6%) had values placing them in group 1, 17 (12.5%) in group 2, and 8 (5.9%) in group 3. Thus the distribution of obese and overweight children in our study did not differ from that expected in a normal population. Pubertal status was appropriate for age in all subjects; all girls over 14 y had reached menarche and all boys over 14 y had Tanner Stage grades of 3 or more. In the girls, standard deviation scores for heightfor-age 16 (means (s.d.)) were similar in our three groups: group 1, 0.70 (1.13); group 2, 0.51 (1.24); group 3, 0.49 (1.67), showing that increasing adiposity was not associated with increased height. By contrast, obese boys (group 3) were signi cantly taller (P < 0.05) than control boys (group 1): standard deviation scores for height-for-age being: group 1, 0.70 (1.08); group 2, 1.17 (1.13); group 3, 1.59 (1.84). As expected, in both sexes the standard deviation scores for weight-for-age (girls 0.34 (0.89); 1.24 (0.81); and 3.12 (1.62), boys 0.70 (1.0); 2.53 (1.03); and 4.79 (2.15)) were signi cantly higher in both overweight and obese subjects vs those of group 1 (P < 0.001). Variables in relation to chronological age In obese girls, but not in overweight girls,, bone area and lean mass were each increased relative to chronological age (P < 0.005). In both sexes fat mass was increased relative to chronological age in both overweight and obese subjects (P < 0.001). In the boys, and bone area values for chronological age were increased in both overweight (P < 0.003) and in obese groups (P < 0.001) but lean mass relative to chronological age was increased only in the overweight boys (P < 0.005). Obese boys (group 3) and

3 boys of normal weight (group 1) had similar lean mass for chronological age. values was signi cantly less in overweight and obese groups for both girls and boys. 629 in relation to body weight in children of different adiposity (age-adjusted data) Figure 1 shows the relationship of bone mineral content to total body weight according to gender in the whole study sample. Table 2 shows both the observed and predicted from weight after adjusting for age and age-squared for the three groups. The ratio of the observed to predicted Bone area in relation to body weight in children of different adiposity In our age-adjusted data the relationship of area with was very close in the three groups in boys and girls with observed values ranging from 99.6 ± 101.6% of predicted values (data not shown). In the age-adjusted data, bone area relative to body weight followed a similar pattern as relative to body weight. area values for weight were lower than observed values in groups 2 and 3 in both sexes, suggesting inadequate enlargement of the bones to fully compensate for increased body weight in these groups (Table 3). in relation to lean tissue mass in children of differing adiposity After age-adjustment, the obese groups of both sexes, but not the overweight groups, had higher in relation to given lean tissue mass, suggesting adaptive increases in had occurred in children with high adiposity but not in those with moderate adiposity (Table 4). in relation to fat mass in children of differing adiposity In the age-adjusted data, only the boys (both overweight and obese subgroups) had higher observed than predicted values for in relation to fat mass than males of normal weight (Table 5). Table 3 weight a Total body bone area (cm 2 ) in relation to total body bone area bone area = Figure 1 Total body bone mineral content in relation to body weight in (a) girls (n ˆ 200) upper graph (log() ˆ *log(weight), SEE ˆ 0.13, R 2 ˆ 0.94) and (b) boys (n ˆ 136) lower graph (log() ˆ *log(weight), SEE ˆ 0.13, R 2 ˆ 0.95). Group 1 ˆ for age percentile < 85; Group 2 ˆ 85 ± 94; Group 3 ˆ 95. Girls 1 ( < 85) (85 ± 94) b 3 ( 95) b Boys 1 ( < 85) (85 ± 94) c 3 ( 95) b b Signi cantly different from group 1 (P < 0.001). c Signi cantly different from group 1 (P < 0.05). Table 2 Total body (g) in relation to total body weight a = Girls 1 ( < 85) (85 ± 94) b 3 ( 95) c Boys 1 ( < 85) (85 ± 94) d 3 ( 95) b b Signi cantly different from group 1 (P < 0.006). c Signi cantly different from group 1 (P < 0.001). d Signi cantly different from group 1 (P < 0.05). Table 4 Total body (g) in relation to total body lean tissue mass (kg) a = Girls 1 ( < 85) (85 ± 94) ( 95) b Boys 1 ( < 85) (85 ± 94) ( 95) c b Signi cantly different from group 1 (P < 0.05). c Signi cantly different from group 1 (P < 0.001).

4 630 Table 5 Discussion Total body (g) in relation to total fat mass (kg) a = Girls 1 ( < 85) (85 ± 94) ( 95) Boys 1 ( < 85) (85 ± 94) b 3 ( 95) b b Signi cantly different from group 1 (P < 0.05). Using a sample from the general population of fracture-free children, we demonstrate for the rst time that important discrepancies between bone area and bone mineral content relative to body weight occur in overweight and obese children during growth. Our overweight and obese children had lower bone area and bone mass for their body weight than subjects with body weights in the healthy range. We consider that this mismatch between high body weight and bone development during growth may place considerable strains on the bones and joints of overweight and obese children. We obtained some evidence of adaptative increases in relative to both lean mass and to fat mass in our youngsters with high adiposity, suggesting some skeletal compensations to elevate bone mass had taken place. Nevertheless, observed values relative to weight remained substantially lower than predicted values in all our overweight groups, these reductions averaging 8 ± 10% in our obese groups of children. All techniques used to estimate body composition have drawbacks, and concerns have been expressed regarding the ability of DXA scanners to discern and bone area with equal accuracy at all depths of overlying tissue. 17 ± 19 These problems are attributed to small variations in edge detection. However, given that has been shown to increase slightly when the amount of overlying tissue has been deliberately increased arti cially using lard, 17 and that generally decreases during weight loss 18,20 we are con dent that the observed values for our overweight and obese children are if anything slightly overestimated, rather than underestimated. Furthermore, the scanner we used is a pencil beam DXA and pencil beam scanners are superior to fanbeam DXA scanners for determining body composition. DXA scanners were originally designed to measure and they do this extremely accurately. The overweight children we measured have weights which lie well within the normal range for adults. Using the same brand of scanner (Lunar) as was used in the present study, Van Loan et al 19 showed that no signi cant changes occurred in either or bone area in fourteen overweight women who lost an average of 15.6 kg in fteen weeks. Our ndings that both and bone area are low relative to body weight in overweight children are perhaps surprising since there is good evidence that obese adolescents undergo early puberty and have advanced skeletal maturation (as shown by bone age) relative to chronological age, than leaner children. 21 However, previous investigators do not appear to have examined the quantitative relationships between bone mass or bone area to body weight in overweight=obese groups of children vs children of normal body weight. In support of our ndings that total body bone area and were low for body weight in groups 2 and 3, are earlier reports of decreased spinal density for body weight in obese children. 10,11 A recent preliminary report, based on measurements in 32 obese children, also found that increased levels of obesity in youth were associated with increased fat mass but not increased bone mineral content. 22 Our study was cross-sectional in design so we cannot say whether the mismatch in skeletal development for body weight which we observed represents a temporary lag between bone growth and bone mineral accrual relative to body weight, which will later be corrected by compensatory increased skeletal growth, or whether there will be a lasting de cit in bone mass for body weight into adult life. Prospective studies are needed to show whether the mismatches in and bone area relative to weight which we report are transient or lasting. Since overweight adults have higher bone mass than lighter individuals 23 it seems probable adaptation will occur over time. On the other hand inactive obese adults can have low bone density. 5 It may simply be that in childhood and adolescence the pace of gain in adipose tissue outstrips possible compensatory increases in bone size or mineral accrual. Alternatively, our overweight subjects may be insuf ciently active to optimize bone gain. Our results suggest that many overweight adolescents fail to adapt bone development adequately to cope with their excess weight. This may increase their likelihood of sustaining fractures when they fall as we have suggested elsewhere. 8 The weight=bone mass imbalance will place high strains on growing bones and joints and may induce lasting joint damage which could contribute to the pathogenesis of osteoarthritis in adult life. Obesity in youth is already an established risk factor for adult osteoarthritis. 24 We recognise that at present there is no consensus regarding the de nition of overweight or obesity in children. We chose to group subjects as overweight or obese by using the 85th and 95th centile values for age because is readily measured very accurately without the need for sophisticated technology. Furthermore, there is good agreement between and adiposity measured by DXA so that children above these centiles tend to be overfat. 25,26 These cutoffs have been employed to examine the prevalence of overweight in nationally representative cross-sectional surveys. 27 They have also been

5 recommended as useful in selecting youngsters for interventions to reduce adiposity. 28 Our study has some limitations. The participants were volunteers and so may not be a representative sample of the current pediatric population in New Zealand. However every fracture-free child aged 3 ± 19 y enrolled in Dunedin bone studies was included in our present analysis and since none were excluded on classi cation we had no bias for degree of adiposity. Reduced physical activity is considered an important contributor to the genesis of obesity and adversely in uences bone mineral accrual 29 whereas exercise has dual bene ts of augmenting and reducing body fat. Unfortunately we do not have any information on the physical activity of our subjects, the duration of their obesity or any information on hormone levels which undoubtedly in uence bone growth and mineral accrual. 30,31 The strengths of our study include the use of large samples of both genders, a wide age range, precise measurements of body composition supplied by DXA and the use of wellaccepted classi cations of overweight and obesity. Moreover, our predictions were based on regressions from the total samples of each gender, which provide conservative estimates of expected bone mineral content and area in groups of different adiposity. Conclusion In conclusion our study con rms the hypothesis that overweight and obese children have lower bone area and bone mass relative to body weight than their leaner peers. Further longitudinal investigations will be needed to de ne the reasons for this and to determine whether the decrease is transient or persistent. Because the mismatch between bone mass and body weight which we have documented during growth could increase the current and=or future vulnerability of these individuals to bone fractures and to later osteoarthritis, studies examining the in uence of childhood obesity upon development of fractures and arthritis and should also be undertaken. These topics have important public health implications. Acknowledgements This study was supported by the Health Research Council of New Zealand. We thank the participants and their parents for their willing co-operation. References 1 Prentice A, Jebb S. Obesity in Britain: gluttony or sloth? Br Med J 1995; 311: 437 ± Gortmaker S, Must A, Sobol A, Peterson K, Colditz G, Dietz W. Television viewing as a cause of increasing obesity among children in the US, 1986 ± 90. Arch Pediatr Adolesc Med 1996; 150: 356 ± Rossner S. Childhood obesity and adulthood consequences. 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