This health check-up cohort found a significantly strong effect on the low BMD of some personal features, such as female, older age, low education level, ever and current smokers, low physical activity intensity, and low BMI. In addition, compared to that of previous cross-sectional studies, this longitudinal study confirmed that shorter sleep duration and poor sleep quality, low dairy consumption, vegetarian diet, high triglyceride levels, low uric acid levels, low walkability, and low solar radiation exposure were associated with low BMD.
A higher education level was positively correlated with preventing osteoporosis by having more opportunities to have adequate knowledge and a good attitude toward preventing osteoporosis [27].
In univariate logistic regression, ever and current smokers were shown to be less likely to have low BMD at baseline, possibly owing to the effect of sex and other unadjusted confounders. In the total sample and male subgroup, ever and current smokers were more likely to have low BMD in multivariable logistic regressions using the GEE approach. In the female subgroup, smoking status was not selected as an influencing variable to put into multivariable logistic regression. The effect of smoking on BMD differed between men and women. Among men, current and recent smokers showed a lower BMD than that of non-smokers in a cohort of older men and women with over 40 years of follow-up. However, among women who did not use estrogen, no significant association was found between smoking and BMD [28].
Regular physical activity promotes bone health during aging. Compared with light-intensity exercises such as strolling, Tai Chi, playing golf, and gardening, moderate-intensity exercises such as badminton, brisk walking, and dancing were significantly negatively correlated with osteoporosis. However, heavy or violent intensity exercises such as swimming and running were not significant in the present study. For males, among light-, moderate-, and heavy- or violent-intensity exercises, the latter is the most effective in preventing osteoporosis. Controlled trials suggest that moderate-to high-intensity exercise, especially combined resistance and impact training, provide a positive stimulus to lumbar spine BMD and that low-intensity exercise is relatively ineffective [29]. However, not only does intensity affect BMD, but exercise volume, duration, and frequency are also related to BMD [15]. According to the different types of exercise, the amount of BMD increase varies in different parts, such as the lumbar spine, femoral neck, and total hip [15].
It has been reported that too short or too long sleep duration, taking a daytime nap, and poor sleep quality increase the risk of osteoporosis [11 30]. A large-scale cross-sectional study revealed that women aged over 50 years with sleep duration < 5 h/day had a higher risk of osteoporosis (OR = 7.35; 95% CI 3.43–15.71), and participants with poor sleep quality had 5.57 (95% CI 1.60–19.41) odds of osteoporosis [31].
Vegetarians, especially vegans, have a lower BMD and a higher fracture risk than non-vegetarians [32]. In Taiwan, soy products, such as soy milk and tofu, are typical diets rich in proteins and isoflavones. Soy protein and isoflavones may play a role in the retardation of bone loss [33]. Increasing the knowledge of nutrients and elevating the quality of vegetarian and vegan diets can reduce the decline in BMD.
Dairy products are rich in protein, calcium, phosphorus, magnesium, and zinc, and are beneficial for bone production. Regardless of the type of dairy product, there was a positive association with the reduced risk of low BMD.
In our study, increasing BMI was inversely related to low BMD. This conclusion is similar to that of previous studies [34]. Two mechanisms have been proposed for this phenomenon. First, a higher BMI enhances bone strength to load heavier mechanical loading of total body weight in early adulthood [35]. Second, the production of adipose tissue, such as adipokines, estrogen, leptin, and interleukin-6, can regulate metabolic processes in bone tissue through different mechanisms [35].
An inverse relationship between the waist circumference and lumbar BMD among middle-aged men and premenopausal women is revealed in a four-wave of the National Health and Nutrition Examination Survey from 2011 to 2018 in United States [36]. Increasing fat mass has a negative correlation with bone mass when excluding the mechanical loading effect of body weight, and waistlines can play a role in the evaluation of abdominal fat accumulation [35].
Consistent with previous studies, an inverse relationship between triglycerides and BMD was observed [37]. A Mendelian randomization study reported a causal weak negative effect of triglycerides on BMD (effect size (standard error) = 0.013(0.005)) [37].
Uric acid plays a paradoxical role in osteoporosis. Uric acid acts as a pro-oxidant in the cell and an antioxidant, mainly in plasma [38]. Pro-oxidants are related to reduced BMD, and antioxidants exert protective effects against osteoporosis. A recent review concluded that normal or high uric acid levels are associated with decreased bone resorption and increased bone formation; however, hyperuricemia has the opposite effect [39].
In addition, we found that walkability was negatively correlated with low BMD. Promoting the convenience of walkability is a factor that prevents the acceleration of bone resorption. The attractiveness of open spaces and neighborhood-built environments, such as parks or playground equipment, is essential to individuals walk and elevate their physical activity behaviors. Sugiyama et al. pointed out that nearest neighborhood open spaces within a 1.6-km radius from residences are likely to encourage recreational walking [16]. The outdoor space of elementary schools is open for public use outside of school time in Taiwan. Many Taiwanese people, especially children and elders, like to exercise in parks or schools. The present study found that the number of schools and parks within a 1 km buffer of residence was associated with a reduced risk of osteoporosis.
Vitamin D is mainly acquired from sun exposure, and small quantities of vitamin D are absorbed from the diet [7]. Vitamin D is transferred to 1,25(OH)2D3 in the circulation, and 1,25(OH)2D3 can induce bone mineralization. Taiwan is located across the tropics and subtropics, between 20° N and 25° N. The effect of solar radiation on BMD was observed in the present study. Sunlight exposure depends on geographic location, time of day, season, climatic conditions, and air pollution. Leal et al. showed that vitamin D3 production in São Paulo (LAT 23° S) was 20.1% (95% CI 12.9–27.2) lower than that in Fortaleza (LAT 3° S) over a year in vitro experiment [7]. Farrar et al. indicated sun-exposure guidelines on vitamin D acquisition, which is noontime unshaded summer sunlight exposure of 30 min at 30°N three times per week with sufficient skin surface area exposed [40].
Menopause has an important impact on the endocrine, skeletal, cardiovascular, immune, and genitourinary systems [41]. After menopause, the bone-sparing effect of estrogen reduces bone resorption by inhibiting osteoclast activity. When estrogen deficiency increases, the release of bone-resorbing cytokines stimulates osteoclast activity [42]. Postmenopausal plasma estrogen is mainly produced and metabolized by adipose tissue. Increased plasma concentrations of estrogens are observed with greater body weight [41] and are related to abdominal fat deposition. The concentration of estrogen is also affected by solar radiation. Relevant to the present study, changes in uric acid, triglycerides, and sleep are related to changes in sex hormones, especially in the postmenopausal period. One pathway associated with uric acid regulation is conjugated estrogen, which increases renal clearance of plasma uric acid [43]. In general, plasma uric acid concentration is higher in men than in women, and postmenopausal women are lower than premenopausal women [43]. Loss of estradiol is associated with increased triglyceride levels, which was also observed in previous studies. However, other factors influence triglyceride levels, such as body weight [44]. Aging, endocrine, and psychological status affect sleep disturbances, including trouble falling asleep and frequent nocturnal awakenings during the menopausal transition [45]. However, some studies have suggested no direct correlation between sleep problems and hormonal changes during menopause [46]. In our study, appropriate sleep duration and good sleep quality were positively associated with low BMD, but only in postmenopausal women.
The strength of this study is its large sample size and repeated health check-up data with a comprehensive assessment. The longest follow-up period was nine years. One limitation of our study was that self-reported questionnaires may have led to recall bias, especially the amount and frequency of food consumption. Second, despite the large sample size, the prevalence of low BMD (10.66%) in the study population was relatively low. Because the study used Mei Jau health exam data, in which participants were healthier, people with osteoporosis or osteopenia may be less likely to attend health examination and more likely to seek medical resources. Third, the solar exposure of each participant was not quantified because of data limitations. Fourth, there may be some unmeasured factors that are potential confounders, such as estrogen level, mood symptoms, and objective sleep data. Fifth, the generalization of our findings to whole Taiwanese population is also limited because the studied cohort might have had a higher socioeconomic status than the general population [47]. In the future, we will explore the relationship between sleep status and BMD during the peri- and postmenopausal periods after adjusting for psychological factors and hormone levels.