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Life Course Dietary Patterns and Bone Health in Later Life in a British Birth Cohort Study
 
 
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ABSTRACT
 
Evidence for the contribution of individual foods and nutrients to bone health is weak. Few studies have considered hypothesis-based dietary patterns and bone health. We investigated whether a protein-calcium-potassium-rich (PrCaK-rich) dietary pattern over the adult life course, was positively associated with bone outcomes at 60 to 64 years of age. Diet diaries were collected at ages 36, 46, 53, and 60 to 64 years in 1263 participants (661 women) from the MRC National Survey of Health and Development. DXA and pQCT measurements were obtained at age 60 to 64 years, including size-adjusted bone mineral content (SA-BMC) and volumetric bone mineral density (vBMD). A food-based dietary pattern best explaining dietary calcium, potassium, and protein intakes (g/1000 kcal) was identified using reduced rank regression.Dietary pattern Z-scores were calculated for each individual, at each time point. Individual trajectories in dietary pattern Z-scores were modeled to summarize changes in Z-scores over the study period. Regression models examined associations between these trajectories and bone outcomes at age 60 to 64 years, adjusting for baseline dietary pattern Z-score and other confounders. A consistent PrCaK-rich dietary pattern was identified within the population, over time. Mean ± SD dietary pattern Z-scores at age 36 years and age 60 to 64 years were -0.32 ± 0.97 and 2.2 ± 1.5 (women) and -0.35 ± 0.98 and 1.7 ± 1.6 (men), respectively. Mean trajectory in dietary pattern Z-scores ± SD was 0.07 ± 0.02 units/year. Among women, a 0.02-SD unit/year higher trajectory in dietary pattern Z-score over time was associated with higher SA-BMC (spine 1.40% [95% CI, 0.30 to 2.51]; hip 1.35% [95% CI, 0.48 to 2.23]), and vBMD (radius 1.81% [95% CI, 0.13 to 3.50]) at age 60 to 64 years. No statistically significant associations were found in men. During adulthood, an increasing score for a dietary pattern rich in protein, calcium, and potassium was associated with greater SA-BMC at fracture-prone sites in women. This study emphasizes the importance of these nutrients, within the context of the whole diet, to bone health.
 
"The PrCaK-rich dietary pattern was consistently positively associated with intakes of lowfat milk, lowfat yogurt, fruit, and vegetables, which had the highest positive factor loadings in each year of the survey. Other foods consistently positively associated with this pattern included whole-meal bread, fish and fish dishes, coffee, and tea. Whereas sugar and preserves, white bread, animal-based fats, sweet cereal products, processed meats, alcohol, chocolate and confectionery, and savory snacks were consistently negatively associated with the PrCaK-rich dietary pattern."
 
Discussion
 
Using longitudinal dietary data from the oldest-British post-war birth cohort study, these data show that, in women, improving the nutrient quality of their diet by increasing their scores for a PrCaK-rich dietary pattern over adult life (without increasing caloric intake) was positively associated with higher SA-BMC and vBMD at age 60 to 64 years. Most notably, the associations were strongest at those sites most prone to osteoporotic fracture, the spine and the hip, and were robust to adjustment for a range of important confounders.
 
The dietary pattern was positively associated with greater intakes of lowfat milk, lowfat yogurt, fruits and vegetables, whole-meal bread, fish, and fish dishes, and lower intakes of sugar and preserves, white bread, animal-based fats, sweet cereal products, processed meats, alcohol, chocolate and confectionery, and savory snacks.Importantly, this PrCaK-rich dietary pattern was also associated with lower total energy intakes, greater densities of fiber, vitamins (folate, carotene, vitamin C, vitamin D), other minerals (magnesium, phosphorus, and iron), and lower densities of carbohydrate and total sugars. The pattern identified broadly agreed with previous observational studies in which "nutrient dense" patterns were positively associated with BMC, BMD, bone turnover markers, or fracture risk.[6, 7, 9, 10, 14, 19] In the majority of studies, "nutrient dense" denotes a pattern rich in fruits and vegetables, and whole grains, with low consumption of processed and sugary foods. The limitations of those studies were that the methodology used did not allow specific nutrient or food groups to be identified as contributing to bone health, and that they were conducted at one time point so the importance of changing diet could not be related to bone outcomes. As recently noted by Hannan and colleagues[2] in a commentary in the Journal of Bone and Mineral Research, studies such as the one presented here are needed to fill a gap in understanding of the relationship between diet and health outcomes by extending the analysis beyond single micronutrients or macronutrients to describe whole diet with respect to bone health.
 

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The findings from this study are in agreement with previous studies that showed positive associations between dietary patterns characterized by greater consumption of fruit, vegetables, and whole grains and BMD in females.[6, 9, 10, 13-18] In contrast, combinations of unhealthy foods, including fried food, savory pies, confectionery, soft drinks, red and processed meats, and biscuits (cookies), have been negatively associated with BMD/BMC.[6, 7, 13, 18] There are few studies that have prospective fracture data. Data from the Canadian Multicentre Osteoporosis Study (CAMOS) cohort showed that a healthy pattern was associated with lower risk of low-trauma fractures in postmenopausal women (hazard ratio 0.86; 95% CI, 0.76 to 0.9).[5] In two Swedish cohorts higher rates of hip fracture in women were associated with a fruit and vegetable intake of less than five portions per day; less than one serving per day was associated with a 50% increased risk of fracture (hazard ratio 1.49; 95% CI, 1.32 to 1.68).[19] The PrCaK-rich dietary pattern identified in the current study supports current guidelines produced for the prevention of osteoporosis.[49] More broadly, this pattern is similar to the dietary pattern described in the American Heart Association Diet and Lifestyle recommendations for reducing cardiovascular disease risk, which was also associated with reduced risk of fracture and increased BMD.[14] Translating any advice from studies to public health guidelines is much easier for the public to interpret if there is a consistent message across common health conditions.[20, 50]
 
At the population level, the tracking of scores for the PrCaK-rich dietary pattern was not strong. This is not surprising, because the results from the dietary pattern trajectories showed that Z-scores were not constant, but tended to increase over time. These increases between age 36 years and 60 to 64 years indicate improvements in diet quality that were concurrent with changes in the UK food supply (eg, increased availability of lowfat dairy, and other products)[35] and the emergence of public health messages regarding diets for the prevention of chronic disease; eg, reduce fat intakes, avoid solid animal fats, consume more fruits and vegetables.
 
In contrast to our observations in women, no associations were observed between the dietary pattern and bone outcomes in men. This may be because the men were at a different stage of skeletal aging than the women. This is supported by studies of bone during male aging that suggest skeletal aging in males occurs more slowly, and starts at around age 60 years when hormonal changes start to occur.[51] However, in the Swedish cohort study positive associations were reported between dietary patterns and reduced fracture risk in men,[19] and in the CAMOS study there was a positive trend toward significance.[5]Given these previous findings, and those in our cohort in women, it will be important to investigate whether these relationships emerge in men at an older age when age-related bone loss has progressed farther and to investigate alternative dietary patterns. Another contributing factor may be that men in our study showed smaller changes in mean Z-scores for the PrCaK-rich dietary pattern over time than women (Fig. 2).
 
By including pQCT as an outcome measure we were also able to explore whether there were associations between dietary patterns and other aspects of bone health at the peripheral skeleton; ie, bone size, distribution, and strength. A greater improvement in the dietary score was associated with smaller medullary area but not with total area or strength.
 
These data indicate that an increase in the consumption of protein, calcium, and potassium-rich foods during adulthood was associated with less endosteal resorption and thus reduced cortical thinning, which would be protective against bone fragility. These data support evidence from previous studies that have shown reduced hip fracture risk in those with better diets.[5, 19]
 
There are several strengths to this study. The availability of longitudinal dietary assessments from multiple time points collected over 28 years using the same methodology and contemporaneous food composition data provided a opportunity to examine dietary patterns over the life course. The use of longitudinal models exploited all available data rather than limiting the analysis to respondents who completed all follow-ups, thus minimizing the possibility of a selective sample. Detailed dietary data were collected in the form of un-weighed 5-day or 7-day food diaries that provided information on the both the range and combinations of foods in this cohort, enabling detailed dietary pattern analyses. Our chosen method of dietary pattern analysis, RRR, allowed us to develop a hypothesis based on previous studies in which micronutrients and macronutrients were related to bone health and to identify patterns in food consumption that best explained provision of these nutrients in this cohort. Our bone outcomes were available from DXA and pQCT measurements at multiple skeletal sites. Finally, the sample size was moderately large across time points, and because of the nature of the cohort data collection and the narrow age-range at each time point, which minimized confounding by age, we were able to adjust for multiple confounders and lifestyle factors across adulthood. The main limitation of this study was the age of the population who are at a relatively early stage of aging; also, at age 60 to 64 years rates of osteoporosis and osteopenia in the population were low. Continuing follow-up in this cohort into old-age will be important to ascertain whether this dietary pattern predicts reductions in age-related bone loss in individuals and fracture incidence by making both the exposure and outcome data longitudinal.
 
In conclusion, a nutrient-dense dietary pattern that is rich in protein, calcium, and potassium associated with lower energy intake during adulthood is associated with better bone health at fracture prone sites in women. Such a dietary pattern is characterized by greater intakes of lowfat milk and yogurts, whole-grain bread and breakfast cereals, fruits and vegetables, and lower intakes of sugars, sweets, processed foods, and animal fats. To increase scores for this PrCaK-rich dietary pattern while maintaining total energy intake and to achieve a net improvement in overall diet quality, intakes of foods positively associated with the pattern would need to increase and intakes of foods negatively associated with the pattern would need to decrease. The findings of this dietary pattern analysis support current public health dietary guidelines for the dietary prevention of osteoporosis.

 
 
 
 
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