Associations between body composition and lifestyle factors with bone mineral density according to time since menopause in women from Southern Brazil: a cross-sectional study

In the present study, weight, BMI, lean and fat mass and RMR were higher in postmenopausal women with less than 5 years since menopause with normal versus low bone mass. Interestingly, these variables did not differ significantly between women with normal and low bone mass and more than 5 years since menopause. This observation seems to support previous evidence showing that BMD is better correlated with percentage of body fat in pre- and perimenopausal than in postmenopausal women [22]. In addition, while it is known that total BMD is associated with higher BMI and fat mass, the profile of trabecular and cortical volumetric BMD (vBMD) varies according to BMI. Indeed, obese adults present higher trabecular vBMD but lower cortical vBMD [23]. Therefore, we hypothesize that the association of adiposity and BMD was more evident in recent postmenopausal women because they had more trabecular bone than those in later postmenopausal life (in whom trabecular bone is lost due to the high bone turnover occurring throughout the postmenopausal years). Further studies assessing volumetric bone density and microarchitecture by high-resolution peripheral quantitative computed tomography in postmenopausal populations are needed to confirm this hypothesis.

When the entire sample was analyzed, age, time since menopause, fat mass and RMR were associated with BMD in all three sites.

In fact, menopause is associated with a few years of rapid bone loss attributed to lower circulating levels of 17β-estradiol, related primarily to the decline in estrogen-mediated inhibition of bone resorption without a fully compensatory increase in bone formation [2]. For an interval of few years around the menopause, women lose 2 % of bone annually. Afterward, bone loss slows to about 1 to 1.5 % per year [24, 25]. Recker et al., [25] found that menopausal bone loss is a composite of loss caused by estrogen deprivation and age per se for the hip and total body, but is caused by estrogen deprivation alone for the spine. In the Study of Women’s Health Across the Nation (SWAN), women who transitioned through menopause experienced a significantly higher rate of bone loss than women who remained premenopausal, independent of age [26]. In turn, a recent study suggests that time since menopause may have a stronger predictive value for low BMD in the lumbar and hip areas than did serum FSH or estradiol levels [27]. Data from the present study reinforces that idea, showing that women with more than 5 years since menopause had higher prevalence of osteoporosis, as well as lower BMD in all sites when compared to those with less time since menopause. In addition, women who underwent menopause more than 5 years ago had a 3-fold increased odds ratio for low bone mass.

Regarding the association between BMD and BMI we found in our study, the odds ratio for low bone mass was five times for a BMI lower than 25 kg/m², being this cut-off the lowest tertile of our sample. In this sense, low weight or low BMI is a well-documented risk factor for future fracture [1]. Zhu and coworkers have recently reported in a Western Australian population that the associations of BMI with BMD measures were attenuated in those with high BMI [5], suggesting that low body weight should be considered as a risk factor for osteoporosis and related fracture, rather than obesity being a protective factor.

In the present study fat mass was associated with BMD in all sites and with reduced odds ratio for low bone mass. However, the influence of fat mass on BMD is a debatable issue and seems to be related to menopausal status [28]. In postmenopausal women, adipose tissue is the major sources of estrogen from aromatization [29]. Therefore, it has been suggested that subcutaneous adipose tissue have higher aromatase activity in comparison to visceral adipose tissue, and could exert a more beneficial effect than visceral fat in bone health after menopause. In this sense, body composition analysis by DXA does not allow to discriminate subcutaneous and visceral fat, which is a limitation of the present study. Further studies using other methodologies are needed in order to clarify this issue.

While in our study BMD measures in all three sites did not differ according to lean mass tertiles, lean mass was lower in participants with low bone mass versus normal bone mass and less than 5 years since menopause. Lima and coworkers showed that in older women, lean mass was significantly correlated with BMD independently of height and fat mass [28]. Some other cross sectional studies with postmenopausal women suggests that lean mass is not an independent correlate of BMD [30, 31]. In turn, in pre- and peri-menopausal women lean mass has been reported to be a main predictor of BMD [32, 33]. The stronger association between lean mass and BMD may be attributed to differences in determinants of lean mass, such as exercise, lifestyle factors, serum estrogen concentrations or a combination of these factors [32].

Concerning RMR, studies in different populations have also reported a strong relationship between BMD and RMR [34, 35]. We found that participants with low bone mass have lower RMR, in line with a previous research that have also shown that a lower lean mass in postmenopausal women is associated with a lower RMR [36]. Taken together these data suggest that interventions aiming to increase lean mass, which increases RMR, could represent a simple and useful strategy to prevent osteoporosis in women, especially in recent postmenopausal women, such as physical activity (PA) practice. In fact, intervention studies have reported positive effects or associations between PA, BMD and markers of bone metabolism in pre- and postmenopausal women [37, 38]. However, walking may not be enough as a stimulus to increase lean mass in postmenopausal women [39], and these women should be encouraged to participate in regular programs of moderate physical activity [40]. Indeed, in the present study, participants were mostly sedentary, as objectively estimated by a pedometer, and this could have influenced on the association between lean mass and BMD that was independent of habitual PA.

In the specific context of osteoporosis prevention and management, a discussion of nutrition appropriately focuses on vitamin D, and protein in addition to calcium. According to our data the mean calcium intake was 799 mg/day meaning 69 % of dietary reference intakes for American women (1200 mg/day). However, in a longitudinal and prospective cohort study, based on the Swedish MammographyCohort [39] only calcium intake lower than 700 mg/day increased risk of fractures and of osteoporosis, high levels of intake did not further decrease the rate of fracture [41]. In the same cohort although not reflected in the fracture rate, women with high vitamin D intake (>5.4 μg/day) tended to have a slightly higher BMD, but in the present study vitamin D (mean of intake 4 μg/day) did not influence the BMD. In a recently published reanalysis of randomized vitamin D supplementation trials, it was concluded that an intake of 20 μg/day is needed to prevent nonvertebral fractures in women and men aged 65 years or older [6]. Regarding calories intake, a previous study showed higher cortical BMD in elderly women (mean age of 75 years) eating a diet exceeding the RDA for macronutrients (44 kcal/kg of ideal body weight) [42]. Interestingly, we did not find any association between calories intake and BMD, probably because our participants were in early postmenopausal. Dietary protein is positively linked to the maintenance of bone and muscle health and some experts suggest that the current recommended protein intake (≈70 g/day) may be inadequate for optimum skeletal and muscle health [43]. Our postmenopausal women had an average protein intake of 77 g/day, which may not be sufficient for interfering with the risk for low bone mass, as shown by the neutral OR related to meat and eggs food intake.

In turn, when micronutrients intake was analyzed, only vitamin A appears to be less consumed among women with lower bone mass. Considering all sample, vitamin A intake lower than 700mcg a day, that is the recommended amount for dietary reference intakes [18], was related to a higher OR for low bone mass. Indeed, vitamin A, retinol, beta‐carotene, and its metabolites are involved in bone metabolism and Wattanapenpaiboon et al. have shown a positive correlation of lumbar BMD with β -carotene levels in postmenopausal women [44]. A recent meta-analysis, also reported an U‐shaped relationship between serum retinol levels and hip fracture risk [45].

One limitation of the present study is the cross-sectional design that does not allow conclusions regarding the direction of cause and effect. Other limitation is the relatively small sample size of 99 participants and a moderate enrollment rate (16 % excluded participants), which could affect the external validity. However, the results observed in our sample of Southern Brazilian postmenopausal women are consistent and in line to those reported in other populations. Another limitation is that although pedometers are increasingly used to estimate habitual physical activity, they are not sensitive to the intensity or the type of the activity performed, and therefore may not accurately depict the loading forces of the activities performed, which are important for bone maintenance and/or development [38].