Associations of Lifestyle Factors with Bone Mineral Density among Male University Students in Japan

To investigate associations of lifestyle factors with bone mineral density among young men in Japan, we measured bone mineral density of the second metacarpal bone in 143 male university students, aged 18-22 years, by the computed X-ray densitometry. The subjects completed a lifestyle questionnaire including a quantitative food frequency questionnaire. Their mean±standard deviation of bone mineral density was 2.61±0.23 mmAl. Body mass index (Spearman’s ρ=0.232, p=0.006), daily walking time (ρ=0.186, p=0.028), and milk consumption at junior (ρ=0.250, p=0.003) and senior (ρ=0.195, p=0.020) high school were significantly correlated with the bone mineral density. For nutritional variables, the bone mineral density was positively correlated with energy-adjusted intakes of calcium (Pearson’s r=0.302, p=0.0002), potassium (r=0.265, p=0.001), saturated fatty acids (r=0.211, p=0.011), and magnesium (r=0.173, p=0.039), and with those of milk and dairy products (r=0.228, p=0.006) and fruits (r=0.205, p=0.014), while being negatively associated with energy-adjusted noodle consumption (r=-0.185, p=0.027). The positive correlation of milk consumption at junior high school with the bone mineral density was not materially altered by adjustment for the body mass index, calcium intake, and walking time. Single-life students had lower bone mineral density compared with those lived with families (p=0.044). Bone mineral density could be increased by modifying dietary habits in young men.

smoking habits, and current and previous exercise time.Almost every junior high school student is provided with milk at school lunch in Japan, then, from overall milk consumption in junior high school days, milk supplied at school lunch was excluded.

Statistical analysis
Our study was conducted in two periods, namely, January (n=81) and December 2000 (n=62) and BMD level differed between the two groups of subjects, but overall associations of lifestyles with BMD were similar between the two groups (data not shown).Accordingly, we here presented the data as a whole.
Body mass index (BMI) was calculated as (body weight [kg]) /(height [m])2.The two-sample t test was used to test mean differences between two groups.The associations of lifestyle factors with BMD were examined by use of the Spearman's rank correlation coefficients ( p ), because the lifestyle variables could not easily be approximated to normal distribution.
Intakes of energy, nutrients, and food groups were estimated from the response to FFQ using a weighted food composition table.They were adjusted for energy intake by using the residuals from linear regression models."Energy and nutrient intakes and food group consumption were all natural-log transformed to improve their normality before the analyses.Pearson's correlation coefficients were computed between BMD and energy-adjusted intakes of nutrients or food groups.
Multiple linear regression models" were adopted for multivariate analyses.BMD was first regressed on energy-adjusted intakes of nutrients or food groups and on past milk consumption with adjustment for loge(BMI) and time of survey, that is, January or December 2000 (model 1).We further adjusted for energy-adjusted calcium intake (model 2).In the final model (model 3), the relationships between BMD and the dietary variables were examined, controlling for loge(BMI), energy-adjusted calcium intake, loge (daily walking time), and time of survey.
We considered BMI, calcium intake, and daily walking time in the final model, because they were significantly associated with present BMD.BMI and daily walking time were also loge-transformed to improve normality.All p values were two-sided, and the statistical analyses were undertaken using the StatVie(*) version 5 for Windows®.25
Table I   Excluding milk provided at school lunch.SD: standard deviation.between calcium intake and BMD in male university students.Calcium deficiency has been associated with lower bone mass in girls in their teens14.17and in middle-aged29 or older30 adults.The associations in young men,14.18however, have rarely been investigated in Japan.Our findings suggested that calcium intake during the young age would affect bone mass even in men.Young Japanese take much less calcium compared with Western people.
In the United States, the mean daily calcium intake was 1,101 mg in men aged 19-30 years,15 while only 540 mg in males aged 20-29 years in Japan.31Therefore, low calcium intake may be a risk factor of future osteoporosis and its related fractures, particularly in Japan.It may be worth noting, however, that osteoporosisrelated fractures are not so common in Japan as in US2 albeit the low calcium intake in Japanese.The determinants of BMD other than calcium intake should be considered to explain this apparent paradox.
We also showed significant positive associations between BMD and intakes of potassium and magnesium, but they turned to be insignificant when considering calcium intake.This might probably be explained by strong correlations among intakes of calcium, potassium, and magnesium due in part to the overlap in dietary sources of these nutrients.We found a strong correlation of energy-adjusted calcium intake with that of potassium (Pearson's r=0.842) or magnesium (r=0.613).In the present study, milk and dairy products were the largest dietary source of calcium (44.7%, estimated from the FFQ data), followed by pulses (11.3%), vegetables and fruits (8.7%), and fishes and shellfishes (4.4%).The second source, pulses, is rich in magnesium."The third source, vegetables and fruits, contains much potassium and magnesium.
SFA also had a positive correlation with BMD, but the correlation again disappeared after adjustment for calcium intake.This might largely be due to high calcium content in milk and dairy products that also contain considerable SFA.The Pearson correlation coefficient between energy-adjusted calcium and SFA intake was as high as 0.776 in our subjects.Intakes of bread and milk have a mutual association because of their well matching, which may explain the finding that the association of bread consumption with BMD was attenuated after controlling for calcium intake.
As for dietary history, our findings suggested that milk consumption in the growing period such as junior high school days increased BMD, independently of current calcium intake.Many studies' 9.17.18.33 have reported effects of milk drinking on BMD at young ages.Teegarden et al.17 found that higher milk consumption during adolescence was associated with a greater peak bone mass in young women, whereas current calcium intake could influence present BMD.In addition, milk intake at the younger age may consequently lead to more milk drinking in the later life.
The major sources of caffeine in children and teenagers are chocolate-containing foods, cola, coffee, and tea beverages.34 We attempted to assess the effect, if any, of caffeine consumption on BMD.Consumption of major caffeine sources during adolescence, however, was not correlated with BMD.Caffeine intake has been hypothesized to decrease BMD by increasing urinary calcium excretion in postmenopausal women.35 On the other hand, Lloyd et al. 34 and Conlisk et al.36 reported no apparent relationship between caffeine intake and BMD in younger women.Our results in younger men were consistent with their findings.
Single-life students had lower BMD than those with families.They consumed less milk and dairy products (mean consumption per day: 74 g vs. 221 g, p=0.001 by t test for energy-adjusted values) and fruits (83 g vs. 108 g, p=0.023), compared with those lived with families.For nutrients, single-life students took less calcium (271 mg vs. 500 mg, p<0.0001), potassium (1,638 mg vs. 2,221 mg, p<0.0001), magnesium (211 mg vs. 252 mg, p<0.0001), vitamin C (51 mg vs. 67 mg, p=0.001), and SFA (14.4 g vs. 18.9 g, p=0.003).Intakes of these foods or nutrients were positively associated with an increased BMD.In addition, they showed shorter walking time per day (mean: 66 min vs. 74 min, p=0.008 by t test for natural-log transformed values) compared with those with family members.Our results, therefore, suggested that the poor nutrition and short walking time led to the lower BMD in single-life students.Ikai et al.37 reported that poor nutrition with an imbalanced diet was more frequently appeared in boarding female university students.They tended to skip a meal more frequently and to take fewer meals per week at their lodgings, which seemed to be due to an irregular daily life and lonely meals.
There appeared a positive correlation between BMD in the metacarpal bone and BMI.This may not be explained by mechanical loading imposed on bone.The bone mass, however, is also hormonally regulated.Recent studies38.39have suggested that leptin stimulates osteoblastic differentiation and mineralization of bone matrix.Leptin is secreted by adipocytes, and its serum levels are strongly related to body fatness.38.39 Circulating leptin, therefore, may contribute to the association of BMI with BMD in the metacarpal bone.
The insulin-like growth factor-I (IGF-I) is another hormone that has extensively been studied in relation to bone resorption and formation.'It also enhances osteoblastic differentiation and may play a role in maintaining bone mass.Physical activity may elevate serum levels of IGF-I.41This might explain why BMD in the metacarpal bone positively correlated with walking time although walking does not directly give substantial mechanical stress to this bone.
One methodological limitation of this study is that our FFQ was validated only in a population largely different from that of this survey.21.22 Intakes of protein sources, vegetables, and several nutrients were much less in the present study than in the National Nutrition Survey,31 which may partly be ascribable to an underestimation by the FFQ.A validation study against dietary records or recalls is warranted in male university students.Another shortcoming of this FFQ is that we could not estimate intakes of phosphorus and vitamin K, which might have affected BMD.19.42.43The physical activity questionnaire was not validated in this study.An error in the recall might have attenuated the association between past exercise and BMD, whereas daily walking time at the time of survey could more easily be reported.
Ferrari et al.12 suggested that environmental and dietary factors interact with polymorphisms of vitamin D receptor gene in affecting peak bone mineral mass in young men.Further investigations involving genetic markers will also be warranted.
In conclusion, the present study disclosed associations of dietary factors with BMD in male university students who have rarely been examined in Japan.Nutritional intakes or dietary habits were found to be important to increase BMD also in young men as in young women.Bone mineral density could be elevated by modifying dietary habits and increasing calcium intake at the young age.Longitudinal studies will certainly be necessary to verify the findings of our cross-sectional study, because such prospective investigations have rarely been conducted in young men in Japan, in particular.

Table 2
summarizes mean daily intakes of nutrients and Pearson's correlation coefficients (r) between energy-adjusted nutrient intakes and BMD.The BMD was positively correlated with intakes of calcium (r=0.302,p=0.0002), potassium

Table 1 .
Means and medians of selected Lifestyle factors and Spearman's rank correlation coefficients ( p ) between bone mineral density and the variables (n=143).

Table 3 .
Mean daily consumption of food groups and Pearson's correlation coefficients (r) between energy-adjusted food group intakes and bone mineral density (n=143).

Table 4 .
Multiple linear regression analysis for associations between selected dietary factors and bone mineral density (mmAl, n=143).
Kanzawa M, Yano S, et al.Plasma leptin concentrations are associated with bone mineral density and the presence of ver-I in healthy younger and older men.J Clin Endocrinol Metab 1990;71:1468-73.42.Ilich JZ, Kerstetter JE.Nutrition in bone health revisited: a story beyond calcium.J Am Coll Nutr 2000;19:715-37.