The authors have no conflict of interest
Physical Activity and Calcium Consumption Are Important Determinants of Lower Limb Bone Mass in Older Women†
Version of Record online: 3 AUG 2004
Copyright © 2004 ASBMR
Journal of Bone and Mineral Research
Volume 19, Issue 10, pages 1634–1639, October 2004
How to Cite
Devine, A., Dhaliwal, S. S., Dick, I. M., Bollerslev, J. and Prince, R. L. (2004), Physical Activity and Calcium Consumption Are Important Determinants of Lower Limb Bone Mass in Older Women. J Bone Miner Res, 19: 1634–1639. doi: 10.1359/JBMR.040804
- Issue online: 2 DEC 2009
- Version of Record online: 3 AUG 2004
- Manuscript Accepted: 11 MAY 2004
- Manuscript Revised: 2 APR 2004
- Manuscript Received: 18 DEC 2003
- elderly cohort;
- physical activity
A population-based study of 1363 older women showed that the 24% who achieved high physical activity and dietary calcium intakes had a 5.1% higher hip BMD than those who did not, supporting the concept that lifestyle factors play an important role in the maintenance of lower extremity bone mass in older women.
Introduction: Although there is general agreement that increased dietary calcium consumption and exercise can slow bone loss in older women, the amount required to have this effect in an older population remains uncertain. This study was devised to examine the effects of calcium consumption (CC) and physical activity (PA) (lifestyle management) on bone mass in an older female population.
Materials and Methods: Using a cross-sectional study design, a population-based sample of older women (mean age, 75 ± 3 years) had hip and heel bone mass measured using DXA (Hologic 4500A; n = 1076) and quantitative ultrasound (QUS, Lunar Achilles; n = 1363), respectively. CC and PA were measured by a validated habitual food frequency and activity questionnaire, respectively. Dose-response effects of PA and CC on bone mass were examined using ANOVA.
Results and Conclusions: Division of the PA and CC into tertiles best described the dose-response effects. After adjustment for CC, age, weight, alcohol consumption, and cigarette smoking, high PA compared with medium or low PA was associated with higher hip BMD and heel QUS (total hip BMD, 3.1%; p < 0.001; QUS stiffness, 2.7%; p = 0.002). After adjustment for PA and covariates, high or medium CC compared with low CC was associated with higher total hip BMD (1.8%; p = 0.027), with no effect at the QUS heel site. PA and CC were dichotomized at the cut-points for effects on BMD. The combination of high PA and CC, achieved by 24% of the population, was associated with a total hip BMD that was 5.1% higher (34% of SD) than those individuals in the low PA and CC group. Stiffness was 3.6% (23% of SD) higher in the high PA and CC group than in the low PA and CC group. If the whole population undertook and achieved a high PA and high CC lifestyle, the population risk of hip fractures may be expected to be reduced by about 17% in this age group as a result of beneficial effects on the musculoskeletal system.
Low bone mass is recognized as a major risk factor for osteoporotic fractures.(1) Physical activity (PA) has been reported to have beneficial effects on the skeleton by contributing significantly to attainment of peak bone mass(2), (3) and maintenance of bone mass later in adulthood.(4) Moreover, resistance training has beneficial and site-specific effects(5) that improve BMD as well as muscle strength. Although physical inactivity results in bone loss,(6) the amount of PA required for maintenance of BMD in the older population remains uncertain. A recent meta-analysis of 18 randomized controlled exercise trials showed that aerobics, weight-bearing exercise, and resistance training were effective in minimizing bone loss.(7) The exercise programs reported varied, but generally, subjects undertook the exercise at least three times per week for ≥20 minutes. The weighted mean improvement in BMD for combined aerobics and resistance exercise compared with control was 1.79% at the spine and 0.68% at the hip. Brisk walking for at least 30 minutes three times per week at moderate to high intensity was found to improve BMD at the spine and hip site by 1.31% and 0.92%, respectively.
There is a general consensus from clinical trial data that dietary calcium supplementation slows bone loss in older women.(8–13) In women at least 10 years past menopause, calcium supplementation of 1000 mg/day for 4 years completely prevented bone loss at the hip and lower limb, whereas cessation of the supplementation after 2 years was associated with a resumption of bone loss.(9) In postmenopausal women, calcium consumption (CC) requirements increase along with renal excretion rates.(14)
We have shown in a prospective study that combined weight-bearing exercise and supplemental calcium in younger postmenopausal women prevents bone loss at the hip.(8) This study showed that the addition of an exercise regimen was necessary to observe a beneficial effect of calcium supplementation on femoral neck BMD. This supports the conclusion reached by Specker from a meta-analysis of studies, the majority being women subjects 30–72 years of age, that examined the effects of calcium and PA on BMD. This study found that calcium and exercise may have an interactive effect on bone mass.(15) However, the magnitude of the effects of habitual CC and PA separately and together on bone mass in older populations remains uncertain. The aim of this study was to examine the dose effects of CC and PA on bone mass as measured by hip DXA and heel quantitative ultrasound (QUS) in an epidemiological study of a population of older women to determine whether evidence for the additive or multiplicative effects of the two lifestyle factors could be found.
MATERIALS AND METHODS
Fourteen hundred ninety-seven women were recruited using a population-based approach in which a random selection of women over the age of 70 and on the Western Australian electoral roll received a letter inviting them to join the study. Over 98% of women of this age are on the electoral roll, and 18% of women approached responded. Subjects were excluded if they were receiving bone active agents including calcium supplements (25%) or if they had significant current illness (0.8%). Although the subjects entering the study were weighted in favor of those in higher socio-economic categories,(16) they did not differ from the whole population in health resource use.(17) All subjects were enrolled in a 5-year trial of the effects of calcium on fracture outcome in which the treated group received 1.2 g of calcium carbonate daily and the placebo group received a matched placebo. Smoking history and average daily alcohol consumption information was obtained from each subject. A subject was considered to have a history of smoking if she smoked at least one cigarette per day for a period of at least 3 months. Alcohol consumption data were dichotomized into two groups: ≤20 or >20 g/day, which is the limit recommended by the Australian National Health and Medical Research Council as being associated with low risk of chronic harm.(18) Weight and height were measured, and body mass index (BMI) was calculated. Informed consent was obtained, and the Human Rights Committee of the University of Western Australia approved the study.
The women filled in a questionnaire that included the following questions. “Do you participate in any sports recreation or regular physical activity?” “Please list any sports recreation or regular physical activity, including walking, that you undertook in the last three months.” Those who answered “yes” to the first question were asked to list up to four activities and the duration (in hours per week) that they engaged in each activity. Women who answered “no” to the activity question were classified as being sedentary and scored zero for activity. Activity levels in the active women were calculated in kilocalories per day for each woman, taking into account her body weight and using published energy costs of listed activities.(19), (20) Where data for specific activities were unavailable, the energy cost of a similar activity was used; for example, for lawn bowls, the value of light walking was used. It was assumed that walking for exercise would be performed at the lower end of the range given the age of these women.(16) We have previously used such an approach to calculation of PA in younger women.(16)
At the commencement of the study, each subject completed a self-administered semiquantitative food frequency questionnaire developed by the Anti Cancer Council of Victoria (ACCV),(21–23) from which the daily consumption of calcium was derived.
At baseline, QUS of the calcaneus of the left foot was measured twice in all subjects using a Lunar Achilles Ultrasound machine (Lunar, Madison, WI, USA). The manufacturer's quality assurance methods were used. The averaged measurement of the speed of sound (SOS), broadband ultrasound attenuation (BUA), and stiffness was used in this analysis. The CVs for SOS and BUA determined on the subjects in this study in our laboratory were 0.43% and 1.59%, respectively. At 12 months, BMD was measured at the hip on a Hologic Acclaim QDR 4500A fan beam densitometer in 1076 subjects. The CV at the hip was 1.2%.(24)
All statistical procedures were performed using SPSS for Windows version 11.5 (SPSS, Chicago, IL, USA). The homogeneity of variance and normality assumptions were checked by visual inspection of residuals from ANOVA models and using Kolmogorov-Smirnov goodness-of-fit test, respectively. The BMD and QUS data were analyzed using ANOVA to assess the additive and multiplicative effects of CC and PA. Hip BMD was measured at 12 months after randomization to calcium or placebo; therefore, this treatment was included in the analysis as a covariate. Age, weight, cigarette smoking, and alcohol consumption were also included as covariates in all analyses. All statistical tests were two-tailed. Probability values <5% were considered significant.
The baseline characteristics of the population are described in Table 1.
Of the 1497 women (70–85 years) that reported on activity, 1125 (75%) reported that they participated in sports recreation or regular PA, whereas 374 (25%) reported they did not. Classification of BMD and QUS values into tertiles of PA best described the dose-response effect of PA on bone at both skeletal sites (Table 2). After adjustment for calcium consumption, age, BMI, alcohol consumption, and smoking history, subjects who were classified into the top tertile of PA had significantly greater BMD at the total hip, trochanter, femoral neck, and intertrochanter sites compared with those in the lowest two tertiles. Similar findings were evident for the QUS data SOS, BUA, and stiffness.
The average daily dietary consumption of calcium was 964 ± 350 mg/day. Intakes ranged from 204 to 2359 mg daily. Almost 61% of the subjects had CCs below 1000 mg/day. The women were divided into tertiles of CC, and BMD was compared using ANOVA (Table 3). Subjects who were classified into the two highest tertiles had significantly greater BMD at the trochanter site compared with those in the lowest tertile, after adjustment for PA, age, BMI, alcohol consumption, and smoking history. No association was seen at other hip sites or with QUS data. Therefore, at the trochanter, an additive effect of PA and CC was shown. No additional benefit of CC, after adjustment for PA, on heel QUS measurements was observed.
The additive effects of PA and CC on total hip and femoral neck BMD are shown in Fig. 1. The SOS data at the heel site are also shown, although there was no significant effect of CC at this site. Having shown a dose-response effect in this population, we dichotomized the CC and PA data at the cut-points suggested by the tertile analysis to better illustrate the size of the treatment effect attainable by older females (Table 4; Fig. 2). The cut-points were 792 mg calcium/day and 169 kcal/day. This analytical approach showed the additive effects of high PA and CC at the hip sites. In addition to an additive effect of CC and PA, the analysis of the dichotomized data suggested an multiplicative effect of CC and PA at the hip, which achieved statistical significance at the femoral neck (Table 4; Fig. 2). The combination of high PA and CC, achieved by 24% of the population, was associated with greater DXA BMD at all the hip sites. The effect size was quite substantial, varying between 4.4% and 6.4% higher bone mass in subjects undertaking both high PA and CC compared with low PA and CC. The heel QUS data for SOS, BUA, and stiffness showed an effect of high PA compared with low PA, with some benefit from high CC, varying from 0.3% for SOS to 3.6% for stiffness, for high PA and CC compared with low PA and CC.
The role of increased PA and CC in maintenance of bone mass in age-related and postmenopausal osteoporosis has been increasingly recognized as playing a potentially useful role in fracture prevention.(13) In this epidemiological study, we examined the separate and combined effects of these lifestyle factors in a large population of older individuals living in the community. Our results extend other studies by examining the dose-response effects of these two modifiable lifestyle factors (CC and PA) achieved by a substantial proportion of the population. In addition, we have studied the way in which they may have additive or multiplicative effects on bone mass.
In this study, a 3.1% greater hip BMD, a 2.3% greater femoral neck BMD, and a 2.7% greater heel QUS stiffness is reported in subjects with high PA compared with those with low PA. In this regard, it is consistent with other epidemiological studies showing similar beneficial effects of exercise. Although the tertile analysis did not show a plateau effect, thereby excluding a beneficial effect of even higher PA, it reflected levels of activity achievable by a substantial proportion of this age group. The definition of the PA threshold for an effect on bone determined in this study is consistent with findings from previous randomized controlled trials of weight-bearing exercise effects on bone mass.(8), (25) These studies suggest a minimum activity level equaling 4 h/week in older women to be beneficial to bone. A previous study of the effect of brisk walking for >240 minutes/week showed an increase in calcaneal BUA, especially in subjects who took up brisk walking compared with those who maintained walking or ceased this activity.(25) An epidemiological study of 16,862 men and women in Taiwan reported that exercise was one of several lifestyle determinants of QUS stiffness in both genders.(26)
Beneficial effects of CC >792 mg/day on DXA bone mass at the hip but not at the heel site as measured by QUS were shown in this study. This threshold for CC is somewhat below the current recommended dietary intake (RDI) of 1000 mg/day(27) for Australian postmenopausal women; however, the RDI calculation includes a safety margin. Previous intervention studies that have shown a positive effect of calcium supplementation on BMD have compared supplemented intakes to control intakes <800 mg/day.(8–12)
This study also emphasizes the beneficial additive effect of high PA and CC on maintaining BMD at the hip, an important skeletal site at risk of fracture in the elderly. The high PA/CC group had a DXA total hip BMD 5.1% higher than the low PA/CC group. The PA and CC effects was additive at the total hip and trochanter sites and were multiplicative at the femoral neck. A meta-analysis of 17 exercise trials concluded that a high calcium intake is required for exercise to be beneficial in maintaining bone mass, suggesting that calcium and exercise do not act independently of each other.(15) Our study does not entirely support this conclusion, because we have shown additive effects of PA and CC at some hip sites, indicating that calcium and exercise are acting independently of each other at maintaining bone mass at these sites. However, we did observe a multiplicative effect of PA and CC at the femoral neck, suggesting that PA is only effective at maintaining bone mass at this site if there is adequate CC. In a previous randomized controlled trial, we showed that calcium was only effective in preserving BMD at the femoral neck if subjects were also undertaking an exercise program,(8) suggesting that exercise effects at this site are particularly sensitive to the availability of adequate calcium. At the heel site, the tertile analysis showed an effect of high PA on QUS. Although not statistically significant, high CC improved the effect of PA on QUS measurements in the dichotomized analysis. The explanation for a relative lack of effect of CC on QUS measurements at the heel is uncertain, but other epidemiological studies have not shown an effect of high CC either.(28)
These data suggest that public health messages advising a CC of >800 mg/day and 4 h of walking or more per week could be expected to increase hip BMD by 3–5%, which would be expected to reduce hip fractures by about 10–17% based on the widely accepted concept that an SD (15%) increase in bone mass should reduce hip fractures by 50% on a population basis.(29) In addition, the well-documented evidence for a beneficial effect of exercise on improvements in balance and reduction in falls would be expected to reduce fracture rates.(30) As a result of these data, a health promotion campaign to increase the PA and CC of the lowest 76% of the older female population to values achieved by the highest 24% of the population may be a cost-effective public health approach to fracture prevention. Moderate-intensity weight-bearing exercise, such as brisk walking and low-impact aerobic exercise, for 240 minutes/week is recommended.
This study was supported by the Healthway Health Promotion Foundation of Western Australia and the Australasian Menopause Society.
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