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J Appl Physiol 97: 1006-1012, 2004. First published May 7, 2004; doi:10.1152/japplphysiol.00068.2004
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Associations between physical activity and bone mass in black and white South African children at age 9 yr

J. A. McVeigh,1,2 S. A. Norris,1 N. Cameron,3 and J. M. Pettifor1

1Medical Research Council Mineral Metabolism Research Unit, Department of Paediatrics, University of Witwatersrand, and 2School of Physiology, University of Witwatersrand Medical School, Parktown, Gauteng 2193, South Africa; and 3Department of Human Biology, University of Loughborough, Leicestershire LE11 3TU, United Kingdom

Submitted 20 January 2004 ; accepted in final form 4 May 2004


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
We investigated differences in physical activity (PA) levels between black and white South African 9-yr-old children and their association with bone mineral content (BMC) and density (BMD) by using dual-energy X-ray absorptiometry. PA was analyzed in terms of a metabolic (METPA; weighted metabolic score of intensity, frequency, and duration) and a mechanical (MECHPA; sum of all ground reaction forces multiplied by duration) component. There were significant ethnic differences in patterns of activity. White children expended a significantly greater energy score (METPA of 21.7 ± 2.9) than black children (METPA of 9.5 ± 0.5) (P < 0.001). When children were divided into quartiles according to the amount and intensity of sport played, the most active white children (using METPA scores) had significantly higher whole body BMD and higher hip and spine BMC and BMD than less active children. White children in the highest MECHPA quartile also showed significantly higher whole body, hip, and spine BMC and BMD than those children in the lowest quartile. No association between exercise and bone mass of black children was found. In this population, PA has an osteogenic association with white children, but not black children, which may be explained by the lower levels of PA in the black children. Despite this, black children had significantly greater bone mass at the hip and spine (girls only) (P < 0.001) even after adjustment for body size. The role of exercise in increasing bone mass may become increasingly critical as a protective mechanism against osteoporosis in both ethnic groups, especially because the genetic benefit exhibited by black children to higher bone mass may be weakened with time, as environmental influences become stronger.

bone mass; South Africa; ethnicity

The need of exercise is a modern superstition, invented by people who ate too much and had nothing to think about. George Santayana (1863–1952)

GIVEN THAT ADULT CHRONIC DISEASES often have their origins in childhood, there is a critical need to better understand how physical activity (PA) and fitness levels in childhood and adolescence may shape health status in adulthood. Many studies have addressed loading activities and bone loss in adults and in elite athletes, and, although a number of studies have addressed the issues of exercise in children and its association with bone mineral accretion (3, 19, 25), the research is particularly sparse for those living in developing countries such as South Africa. We know very little about ethnic differences in these countries, particularly with regard to PA levels, bone mineral density (BMD), body composition, and obesity. Although the prevalence of obesity is higher in developed countries (24), it is nevertheless a serious emerging problem in developing countries (10) . Other chronic diseases of lifestyle, such as diabetes and hypertension, are also increasing, but little is known about the changing prevalence of osteoporosis and fragility fractures.

Evidence that PA is an effective strategy for the prevention of postmenopausal or age-related osteoporosis has been inferred from cross-sectional investigations of retired athletes, which showed increased bone mass in the athletes with a history of childhood weight-bearing PA (4). Studies have found a relationship between intensity of exercise and bone mass (16, 21). Further high levels of activity within the limits of normal lifestyle are also associated with increased BMD (9). This association has not been well explored or observed in prepubertal children and has not been observed in children living in developing countries such as South Africa. It is possible that the lower fracture rates reported in the elderly of developing countries may relate to higher PA levels during childhood and adulthood.

Bone adapts to loads applied to it; the crucial factors in optimizing this bone response are the age and degree of maturity of the subject during which the mechanical loading is initiated (6) and the magnitude of the load applied to the bone (13). Peak bone strain scores [mechanical PA (MECHPA)] have consequently been developed to "rate" the loading of different activities (13). It is during the growth period that mechanical loading is said to have the greatest influence on the skeleton (14, 15, 20).

There have been a number of studies that have confirmed that African Americans and South African blacks have greater BMD at the proximal femur and that African Americans have greater BMD at the lumbar spine as well as an increased cortical thickness than whites (2, 7). The age-adjusted hip fracture incidence is 50% lower in African American women than in Caucasian women (5), and what limited information there is suggests that South African blacks also have markedly lower hip fracture rates than South African white adults (32, 38). Very few of the factors influencing osteoporosis have been well studied between ethnic groups.

In this study, we assessed the association between PA [sedentary activity, sports participation, intensity of activity, commuting (actively and passively) to and from school] and skeletal mass in 386 healthy 9-yr-old black and white, male and female South African children. We hypothesized that 1) higher levels of PA [a greater metabolic equivalent PA (METPA) score] would be associated with higher bone mass; 2) the type of sport played influences bone mass (sports with a higher MECHPA score would have a greater osteogenic effect); and 3) ethnic groups would have different levels of PA, and, possibly, this could translate into different bone mass effects.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Subjects.   This is an observational study of a cohort of children recruited from the Birth to Twenty birth cohort, a longitudinal study of child health and development (11, 31, 41). All children born within a 6-wk period (April 23 to June 8, 1990) in the greater Johannesburg metropolitan area in South Africa were originally recruited. A random sample of children (n = 682), stratified by ethnic group (black and white), gender, and socioeconomic status, who were participating the Birth to Twenty cohort study were enrolled into a longitudinal study assessing factors influencing bone mass during childhood and adolescence (Bone Health Study) in 1999. Cross-checks were performed to ensure that there were no significant differences between the Birth to Twenty and Bone Health cohort for key demographic variables (residential area at birth, maternal age at birth, gravidity, gestational age, and birth weight). Complete data for this study were available for 386 children. Subjects were all healthy and aged 9 yr at the time of testing. Children who had asthma or were suffering from any disorder likely to affect bone metabolism were excluded from the study. The sample was composed of 44 white male, 158 black male, 38 white female, and 146 black female children. All subjects and their parents provided written, informed consent, and ethical approval was obtained from the University of the Witwatersrand Committee for Research on Human Subjects.

Questionnaire.   All subjects completed an interview with the caregiver present. We examined past medication, known diseases, and pubertal development [by Tanner hair development (39)]. Dietary calcium intakes were assessed by using a 24-h dietary recall questionnaire. Total PA was estimated by using a structured, detailed, retrospective interview taking into consideration all PA and inactivity over the previous 12 mo. The questionnaire was based on questionnaires validated in previous studies (12, 28) and modified appropriately for South African children. The intensity, frequency, and duration of all PA [at school, after school, at home, and commuting (actively and passively) to and from school] were taken into account. Intensities of activities were classified as multiples of one metabolic equivalent (the ratio of the associated metabolic rate for the specific activity to the resting metabolic rate). PA was scored in two ways as calculated from the questionnaire: 1) metabolic PA (METPA) score by weighting the intensity [multiples of basal metabolic rate (metabolic equivalents) and duration (h/wk)] (1) and 2) MECHPA score by weighting the peak bone strain [ground reaction forces as multiples of body mass and duration (h/wk)] (13). This score is based on the method developed by Groothausen et al. (13); however, we modified this by multiplying the ground reaction force by duration because the original measure did not include duration or frequency. Thus a sum score MECHPA was calculated as the sum of all MECHPA scores multiplied by duration (h/wk) per activity.

Bone measurements.   We measured whole body and site-specific bone mineral content (BMC) and BMD by using a Hologic QDR 4500A dual-energy X-ray absorptiometer (DXA) according to standard procedures. A spine phantom was scanned daily to determine the intrinsic coefficient of variation of the machine. During the course of the study, coefficients of variation for BMC and BMD were 0.48 and 0.35%, respectively. A trained DXA technician performed all scans, and intra-observer variation for our study was found to be below 1% for all skeletal sites. DXA scans were performed on the nondominant radius, left hip, lumbar spine (L1–L4), and whole body. The whole body scan obtained from the DXA enabled the assessment of whole body lean and fat tissue (g) and percent body fat.

Anthropometric measurements.   The height of each child, recorded to the nearest millimeter, was measured by using a stadiometer (Holtain, Crosswell, UK), and weight, recorded to the nearest 100 g, was measured by using a digital scale (Dismed, Haftway House, South Africa). Both devices were routinely checked every 3 mo throughout the study, and no adjustments were necessary to the calibrations of the equipment. Subjects were measured with light clothing and no shoes.

Data analysis.   Two kinds of relationships with bone mass, ethnicity, and PA were investigated. First, METPA and MECHPA scores were included as categorical variables (divided into quartiles) and analyzed separately for black and white children. Second, METPA and MECHPA scores were log transformed (data were negatively skewed) and correlated with bone mass variables separately for white and black children by using Pearson's correlation coefficients. All data are presented as means ± SD, unless otherwise noted. Data were analyzed by using SPSS version 11.0. An ANOVA was performed for all PA and bone and body composition measurements. An {alpha}-level of P < 0.05 was considered to be statistically significant. Bone mass differences within METPA and MECHPA quartiles and between the race groups were assessed by using a multivariate ANOVA. The Bonferroni multiple comparison test was used to assess group differences. {chi}2 Tests were used for categorical variables. DXA data are reported both with and without adjustment for height and weight.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Anthropometric and bone characteristics.   Included in the study were 82 white and 304 black 9-yr-old children, with approximately equal numbers of male and female children in each group. All children were prepubertal. Table 1 shows the results for unadjusted DXA and body composition data. White children had significantly lower hip BMD (P < 0.001) and significantly greater hip area (P = 0.002) than black children, and white female children had lower spine BMD than black female children (P = 0.005). White female and male children were significantly taller (P < 0.001) and had higher calcium intakes (P < 0.001) than their black peers. White male children were also heavier then black male children (P = 0.04) and had significantly greater lean tissue mass (P < 0.001). There were no significant differences between black and white children for body mass index (BMI). Table 2 shows the results for bone mass data adjusted for height and weight. After adjustment for height and weight, black children still had a significantly higher hip BMD than white children (P < 0.001), black male children had higher hip BMC than white male children (P = 0.038), and black female children had higher spine BMC (P = 0.005) and spine BMD (P = 0.004) than white female children.


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  		Table 1. Unadjusted DXA, height, weight, age, BMI, and calcium data

 

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  		Table 2. Cohort bone mass characteristics after adjusting for differences in height and weight

 
PA.   PA data are presented in Table 3. Over 90% of white males and females participated in physical education classes at school compared with only ~30% of their black peers. White female children spent a significantly greater time sleeping (P = 0.006) and playing sports, with a higher METPA score (P < 0.001) and MECHPA score (P = 0.034) than black female children. Black female children spent a greater time actively commuting to and from school (i.e., walking or riding) each day than white female children (P < 0.001). White male children also spent a significantly greater time sleeping (P = 0.019), expending a significantly greater METPA score (P < 0.001), and playing sports, which generated a higher MECHPA score (P < 0.001), than black male children. White and black children spent similar amounts of time participating in sedentary activities and commuting passively to and from school (i.e., via car, bus, taxi, or train).


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  		Table 3. Physical activity characteristics

 
Associations between bone characteristics and METPA.   Subjects were divided into quartiles [from Q1 (least active) to Q4 (most active)] on the basis of their METPA scores. There were no significant differences in anthropometric values (height, weight, BMI, percent fat, and fat and lean tissue), between METPA quartiles for white or black children. There were no significant differences between bone mass values and METPA quartiles in black children except for whole body BMD (P = 0.022). There were, however, significant relationships between METPA quartiles and bone mass values in white children at the hip (P = 0.013; P = 0.001) and spine (P = 0.019; P = 0.003) (BMC and BMD) and for whole body BMD (Fig. 1).



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  		Fig. 1. Bone mass across metabolic equivalent physical activity (METPA) quartiles for black ({bullet}) and white ({blacktriangleup}) children. A: whole body bone mineral density (WBBMD). B: hip bone mineral content (BMC). C: hip bone mineral density (BMD). D: spine BMC. E: spine BMD. Each symbol denotes a quartile, presented from left to right as lowest (Q1) to highest (Q4). Values are means ± SE. White children in Q4 had significantly higher bone mass than those in Q1 and Q2 (*P < 0.05).

 
Log METPA scores were significantly correlated with bone mass values at all sites except for the radius in white children (Table 4); however, in black children, the only significant relationship was between log METPA and WBBMD (r = 0.18, P = 0.002).


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  		Table 4. Correlations between log METPA and MECHPA values and bone mass measurements in black and white children

 
Associations between bone characteristics and MECHPA.   Subjects were divided into quartiles [from Q1 (very low loading) to Q4 (high loading)] on the basis of their MECHPA scores. These MECHPA quartiles were then compared with BMC and BMD at various sites. There were no significant differences in anthropometric values (height, weight, BMI, and fat and lean tissue) between MECHPA quartiles for white or black children. However, body fat percent was significantly (P = 0.025) lower in black children with MECHPA scores in Q4 (highest loading) compared with Q2 (low loading). There were no significant differences between bone mass values and MECHPA quartiles in black children. There were, however, significant differences in bone mass measures between MECHPA quartiles for white children at all sites except for the radius. For white children, the most active group (Q4) had significantly higher whole body (P = 0.016), hip (P = 0.001), and spine (P = 0.004) BMD and hip (P = 0.008) and spine (P = 0.024) BMC than the two least active groups (Q1 and Q2) (Fig. 2).



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  		Fig. 2. Bone mass across mechanical physical activity (MECHPA) quartiles for black ({bullet}) and white ({blacktriangleup}) children. A: WBBMC. B: hip BMC. C: hip bone BMD. D: spine BMC. E: spine BMD. Each symbol denotes a quartile, presented from left to right as lowest (Q1) to highest (Q4). Values are means ± SE. White children in Q4 had significantly higher bone mass than those in Q1 and Q2 (*P < 0.05).

 
Significant positive correlations between bone mass (BMC and BMD) and log MECHPA scores were found in white children at all sites except for the radius (Table 4). No correlations were found for any site in black children.


   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
To our knowledge, this is the first study undertaken in a population of normal prepubertal children in a developing country to investigate ethnic differences in the bone mass response to PA. We have found that whole body BMD and hip and spine BMC and BMD were significantly associated with increased levels of activity (i.e., a greater METPA score) and mechanical stress (MECHPA score) in white children. More active white children had a superior whole body BMD (up to 8% greater) and hip (up to 17% greater) mass and spine (up to 17%) mass than less active children, even before reaching adolescence and early adulthood, the period during which PA is assumed to be most influential on bone development (22, 37). These findings are in agreement with Janz et al. (18) and Slemenda et al. (36), who reported 4–7% greater bone mass in prepubertal children in the highest quartiles of weight-bearing PA. Significant positive correlations were found only for whole body BMD in black children. When BMC and BMD were plotted against activity quartiles for both METPA and MECHPA scores, an increase in both bone mass variables were seen for white children but not for black children. In this study, PA appeared to have an osteogenic association with bone mass in white children but not in black children. It appears that black children do not reach a high enough "threshold" of activity to induce an osteogenic association. This was evidenced by the black children's narrower range in activity scores. The highest activity and loading quartiles for black children had mean scores that were much lower than those of the white children's highest quartiles. Nevertheless, lower PA levels in this group of black children did not appear to negatively impact bone mass; black children as a whole still had a greater hip and spine (girls only) bone mass than the white children. The possibility of a genetic protection against low bone mass and fracture in blacks must be considered because calcium intakes and PA were lower in the black than in the white children. For blacks living in developing countries such as South Africa, as lifestyle and dietary patterns change with urbanization, fractures in the elderly may become more prevalent; thus PA may become increasingly more important as a means of protecting the skeleton in this population.

PA is an exogenous factor influencing bone health, and special attention should be given to its role in optimizing bone health. Studies performed in developed countries such as North America and Europe have shown that inactivity and activity patterns differ by ethnicity, with minority groups engaging in less PA (12). Hispanics and non-Hispanic blacks are less active than Caucasians, and African American children expend less energy than white children (8). Obesity and higher body weight are strongly associated with a sedentary lifestyle and lack of PA in the adult population of the European Union (26), and the latter are key components in the growing overweight and obesity problem in Western populations. Of the few studies that have been recently published from developing countries, similar findings have been reported from South Africa (23, 35) and Nigeria (24). Despite differences in PA between black and white prepubertal children in the present study, no differences in BMI were noted between the ethnic groups.

The association between activity and bone mass is greatest in the weight-bearing regions of the skeleton. In our study, significant positive correlations were found at all weight-bearing sites in white children. Pocock et al. (29) have suggested that a possible reason for the hip being the site most receptive to differing levels of PA is because differences in skeletal load are most pronounced at the hip, as a result of the greater increment of load at this than at other sites. It is known that low-force activities, such as a long-distance running, swimming, and cycling, increase muscle endurance but not bone mass. Maximal force activities such as weight lifting and sports involving violent acceleration of the body put greater loads on bones than low-force exercises (33). Several studies have indicated that bone mass is a function of muscle strength (9, 27, 34). The positive influence of body weight and muscle mass on bone is well documented (17).

Studies investigating the association of past and present PA with bone mass and muscle mass and strength have led to inconsistent results. Although a few studies have examined the intensity, frequency, and duration of exercise needed to produce a significant effect on body composition and bone mass (3, 19, 25), no studies have observed children in developing countries. Additionally, most of these studies have been conducted in female subjects only and very few of these have examined ethnic differences. Schoenau and Frost (33) suggested that bone strength adapts to isometric muscle forces and peak momentary forces. Our data substantiate this observation. White children playing sports with a high bone strain such as rugby and gymnastics showed greater BMC and BMD at the whole body and at the hip, with the greatest difference again being observed at the hip (up to 17% greater in the "high-strain" group than in the "low-strain" groups). This suggests corresponding kinds of exercises during growth could help to achieve greater bone strength and subsequently minimize fractures in later life.

Studies have raised the possibility that the sooner children become active, the greater their bone accrual, lean muscle mass, and possible greater peak bone mass. On the basis of the present evidence, it is clear that bones of growing children benefit most from moderate to high levels of exercise and activity. What is unclear at present is the duration of the effect of exercise on bone once it is stopped and what effect this prepubertal exercise will have on bone mass after the pubertal growth spurt. Additionally, it is not clear whether we would see the same benefits of exercise with regard to bone mass in black children if they were participating at higher activity levels, similar to those of their white peers. One of the aims of the Birth to Twenty study is to attempt to answer these questions as these children move through puberty and into adulthood. Very few data exist on PA, bone mass, and body composition in developing countries. What is known, however, is that rapid changes in diet, activity, and the prevalence of obesity are occurring in residents of these countries (30). These changes are associated with an increase in chronic diseases, which will need to be addressed.

This study reports cross-sectional data from black and white 9-yr-old South African children involved in a longitudinal study. Therefore, these results may not necessarily be extrapolated to other populations. It will be important to follow up longitudinally to examine whether the observations made here persist into adolescence. Although a number of approaches to assessing children's PA have been described, no specific method has been identified as the best option for all studies (40). Although we acknowledge that there are limitations to using activity recall questionnaires, in this large longitudinal cohort of children, recall questionnaires are the only practical way to assess PA.

Understanding PA's impact on bone mass is central to developing primary prevention strategies for osteoporosis. Programs promoting physical education and PA are also desperately needed, specifically in the South African context. The lack of black children participating in physical education lessons at school is cause for concern, as it contributes to the lack of PA in the black children. Although fracture rates are relatively low at the present time in elderly black subjects, obesity and associated hypertension and diabetes are major concerns. Thus development of a culture of exercise is seen as being important in attempting to address these problems.


   GRANTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
ACKNOWLEDGMENTS
 REFERENCES
 
This work was funded by the Medical Research Council (South Africa) and the Wellcome Trust (United Kingdom).


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
REFERENCES
 
The authors thank T. Sibiya, E. Tseou, and Dr. H. Thompson for valuable assistance with data collection and S. Mohamed for assistance with the DXA scanning.


   FOOTNOTES
 

Address for reprint requests and other correspondence: J. A. McVeigh, School of Physiology, Univ. of the Witwatersrand Medical School, 7 York Rd., Parktown, Gauteng 2193, South Africa (E-mail: mcveighja{at}physiology.wits.ac.za).

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 

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