“Ossa sanus in corpore sano” A sound bone in a sound body: the importance of nutrition, physical activity, and nonpharmacologicalmanagement in osteoporosis






Alba GÓMEZ-CABELLO,a,b PhD
Ignacio ARA,b,c PhD
Germán VICENTE-RODRÍGUEZb,d PhD
José Antonio CASAJÚS,b,e MD, PhD
José Antonio CASAJÚS,b,e PhD
a Centro Universitario de la Defensa,
Zaragoza, SPAIN
b GENUD “Growth, Exercise, Nutrition and Development” Research Group
University of Zaragoza, SPAIN
c GENUD Toledo Research Group
University of Castilla-La Mancha
Toledo, SPAIN
d Department of Sport and Exercise
Science, Aberystwyth University
Ceredigion, UNITED KINGDOM
e Faculty of Health and Sport Science (FCSD), Department of Physiatry and Nursing, University of Zaragoza
SPAIN

“Ossa sanus in corpore sano” A sound bone in a sound body: the importance of nutrition, physical activity, and nonpharmacological management in osteoporosis


by A. Gómez-Cabello, I. Ara, A. González-Agüero, J. A. Casajús and G. Vicente-Rodríguez, Spain



This review summarizes and updates the knowledge regarding the importance of nutrition and physical activity on bone mass and fracture risk. Adequate nutrition is of great importance to guarantee optimal development and maintenance of bone structures. Use of calcium and vitamin D in combination is effective in preventing osteoporosis as it helps to reduce the bone loss that occurs during the ageing process. Moreover, proteins can also impact skeletal mass and the risk of fractures, and other nutrients such as vitamins C and K or antioxidants are also associated with increased bone mass, though more research is needed to fully understand these associations. In addition to appropriate nutrition, physical activity and specific training programs represent another key factor in the prevention and/or treatment of osteoporosis. Bone mass seems to benefit from present and past physical activity. Sport practice at the time of bone development increases bone density, and more recent sport training contributes to the preservation of bone-related variables. Therefore, those who are more active throughout life have a higher bone mass, and subsequently a reduced risk of osteoporosis later in life. Moreover, physical activity appears to be a powerful stimulus to prevent the risk of osteoporotic fractures, especially at the hip. Finally, specific training programs are useful to mitigate the decline in bone mass during senescence, especially in postmenopausal women.

Medicographia. 2014;36:170-175 (see French abstract on page 175)



One of the major demographic changes occurring in developed societies is a significant ageing of the population. Currently, people over 65 represent up to 20% of the total population in several countries, a proportion that is expected to rise in the coming decades due to increased life expectancy.1

In older people, age-related bone loss in both sexes is usually in the range of 0.5% to 1.0% per year, with an apparent increased rate of bone loss at the femoral neck with increasing age, especially in women. For this reason, the risk of fracture is higher in women and increases with age. Therefore, as people are living longer, osteoporosis and fracture risk are expected to increase. Osteoporosis is commonly referred to as a “silent disease” as there are no symptoms until the first fracture occurs. The adverse outcomes of osteoporosis do not manifest themselves until later in life, when the incidence of fractures increases. Osteoporotic fractures— defined as those fractures associated with low-energy trauma occurring at sites associated with low bone mineral density (BMD)2—constitute a global and growing problem, especially in postmenopausal women. The frequency of these fractures increases by 1% to 3% per year in many areas worldwide,3 which has a deep impact on the quality of life4 and mortality5 of individuals. In the case of hip fracture, most deaths occur in the first 3 to 6 months following the event, 20% to 30% of which are causally related to the fracture event itself.6 In Europe in 2005 all osteoporotic fractures in men and women collectively accounted for 3.7 million fractures, representing a direct cost of €36 billion.2 Moreover, health economists estimate that osteoporosis-related costs will double by 2050 in Europe. This means an increase of up to €80 billion in 2050.7

Low BMD is a major risk factor for all types of fracture; however, other factors such as age over 75 years, self-reported health, low body mass, weight loss, height, history of fractures, years since menopause, parental hip fracture, calcium intake, and physical inactivity may also contribute to the development of this disease.8-10 These risk factors for low BMD, osteoporosis, and osteoporotic fractures include both unchangeable and modifiable factors. In fact, it is widely known nowadays that diet and physical activity are two important modifiable lifestyle factors that can prevent—or at least slow down—the rate of bone loss. Therefore, the aim of this review is to summarize and update the knowledge regarding the importance of nutrition, physical activity, and nonpharmacological management on bone mass and fracture risk in older adults and elderly people as a starting point for developing future interventions to maintain a higher quality of life in people throughout the ageing process.

Nutrients, bone mass, and fracture risk
Adequate nutrition plays an important role in the development and maintenance of bone structures resistant to usual mechanical stresses. Many nutrients play a role in optimizing bone mass. In addition to calcium and vitamin D, other nutrients such as proteins, vitamin C, vitamin K, or other antioxidants can also impact skeletal mass and the risk of fractures.

Calcium and vitamin D
Calcium and vitamin D are the most commonly studied nutrients in relation to bone mass and the risk of fractures. A review has shown that interventions including food rich in either calcium, vitamin D, or a combination of both improve serum bone markers and BMD and reduce falls.11

Clearly, both calcium and vitamin D contribute to healthy bone maintenance during ageing, although their relative contribution is still unclear. While most studies found that vitamin D supplementation improves BMD and serum markers of bone health; it seems that vitamin D given alone at doses of 10 to 20 μg per day is not effective in preventing fractures if it is not accompanied by adequate calcium intake. By contrast, calcium and vitamin D given together seem to reduce hip fractures, total fractures, and probably vertebral fractures, irrespective of sex, age, or previous fractures.12 It therefore appears that while vitamin D supplementation combined with coadministration of calcium reduces the rate of falls in older people, vitamin D alone might not be effective in preventing hip fracture, vertebral fractures, or any new fracture. For that reason, it seems that an increase in dietary calcium is necessary to guarantee the effectiveness of vitamin D supplementation on the rate of falls and fractures.

The effect of combined calcium and vitamin D was specifically evaluated by Tang et al13 in a meta-analysis that showed that calcium and vitamin D treatment was associated with a 12% risk reduction in all types of fractures and a reduced rate of bone loss of 0.5% at the hip and 1.29% at the spine. Moreover, it was found that the fracture risk reduction was significantly greater (up to 24%) in trials in which the compliance rate was high. The treatment effect was better with calcium doses of 1200 mg or more than with doses of less than 1200 mg and with vitamin D doses of 20 mg or more than with doses of less than 20 μg per day.

In conclusion, calcium supplementation combined with vitamin D is effective in reducing osteoporosis and fracture risk in older people. In contrast, vitamin D deficiency causes muscle weakness, increasing the risk of falls and fractures. Therefore, because sun exposure is generally reduced in the elderly and cutaneous synthesis of vitamin D is reduced by ageing,14 patients being treated for osteoporosis should be adequately supplemented with calcium and vitamin D to maximize the benefit of treatment.15

Proteins
In addition to an adequate intake of vitamin D and calcium, dietary proteins represent key nutrients for bone health, and thereby function, in the prevention or treatment of osteoporosis. Whereas a gradual decline in caloric intake with age can be considered as an adequate adjustment to the usual progressive reduction in energy expenditure, the parallel reduction in protein intake is certainly detrimental in maintaining the integrity and functioning of several systems or organs, including bone mass and skeletal muscle.

As mentioned above, dietary protein is crucial for bone and muscle development.16 In a large number of studies, a positive relationship between protein intake and bone mineral content (BMC) or BMD has been found, while low protein intake has been documented in elderly subjects at risk of fragility fractures, and more so in those who have sustained a hip fracture. In particular, Munger et al17 found that between those in the highest quartile of protein intake and those in the lowest quartile, the reduction in the incidence of hip fractures was 67% and 79% for total and animal protein intake, respectively, representing 1.3 vs 1.0 g protein/kg of body weight per day. Moreover, recent evidence suggests that increasing protein above the recommended dietary allowance may help to prevent loss of bone and muscle mass in the elderly. Increased essential amino acid or protein availability can enhance muscle protein synthesis and anabolism, as well as improve bone homeostasis in older subjects.18 Thus, in primary or secondary prevention of osteoporosis, protein repletion, by positively influencing both bone and muscle mass and bone and muscle strength, could contribute to the prevention of falls and the subsequent occurrence of osteoporotic fractures.

Vitamin K
The results of studies that focused on the relationship and effects of vitamin K on bone mass and fracture risk are controversial. Therefore, it is difficult to draw a definite conclusion about the effectiveness of this micronutrient in the prevention and/or treatment of osteoporosis and osteoporosis-associated fractures.

In observational studies, vitamin K insufficiency is generally associated with lower bone mass and an increased incidence of hip fracture. Moreover, the findings of a number of cross-sectional studies suggest that high vitamin K intake has benefits on bone. However, these findings are not supported by the results of randomized controlled trials,19 as some important intervention studies have cast some doubts on the benefits of high vitamin K intake on bone health later in life. In fact, based on the studies described in a review carried out by Cashman et al,20 it would appear that vitamin K supplementation does not protect against loss of BMD in some skeletal sites such as lumbar spine, mid-distal radius and whole body in older subjects. However, in other meta-analyses of randomized controlled trials, vitamin K was shown to be effective in increasing BMD at the lumbar spine but not at the femoral neck.21 In relation with combined supplementation programs, it has been shown that those receiving the combination of calcium, vitamin D, and vitamin K had an increase in BMC and BMD at the radius.11 In another study, the group taking a supplementation of calcium, magnesium, zinc, vitamin D, and vitamin K showed decreased bone loss at the femoral neck.22 However, it is difficult to know if this beneficial effect was due to vitamin K supplementation or due to the well-reported positive influence of calcium and vitamin D on bone mass. Specific randomized controlled trials are needed to test the independent effect of vitamin K or the strengthening role of this vitamin.

Vitamin C
Vitamin C has also been studied in relation to bone mass in elderly people, although to a lesser extent. Sahni et al23 evaluated the associations of total, supplemental, and dietary vitamin C intake with BMD at the hip, radius, and spine and changes in BMD over 4 years. There was a possible protective role of vitamin C on bone health among older men; however, null associations were observed in women. The same authors also evaluated the associations of vitamin C with incident hip fracture and nonvertebral osteoporotic fracture over a 15- to 17-year follow-up in a cohort of elderly men and women.24 They found that subjects in the highest tertile of total and supplemental vitamin C intake had significantly fewer hip fractures and nonvertebral fractures compared with those in the lowest tertile.

Other antioxidants
During the ageing process there is an increase in oxidative stress, which impacts many age-related degenerative processes, such as bone and muscle loss. As the antioxidant defenses are significantly decreased in elderly people, oral supplementation with antioxidant agents may mitigate bone loss in osteopenic or osteoporotic population,25 while at the same time improving muscle mass, thereby reducing the risk of falls and fractures. However, this conclusion is premature given that the data is so limited.

Physical activity, bone mass and fracture risk
The promotion of regular physical activity has been advocated as one of the main nonpharmaceutical measures proposed to older subjects for successful ageing. In this regard, much research has been carried out in order to test the influence and effects of physical activity and exercise on bone mass and osteoporotic fractures.

Physical activity and bone mass
Several cross-sectional studies have found that lifetime physical activity is positively related to bone mass later in life. It has been shown that in healthy men and women, higher levels of sporting activity during youth were associated with greater lumbar spine BMD, and that femoral neck BMD was greater in subjects who reported regular sports participation over the previous 20 years and during their whole lifetime.26 On the other hand, occupational physical activity in the past has also been positively related to bone mass in senescence, showing that physical activity during adolescence and the young adult years contributes to the preservation of BMD in adults and older people.27,28

Not only does lifetime physical activity seem to have positive associations with bone mass among elderly people, but so does current physical activity. In a large cohort of elderly women Bauer et al29 showed that weight-bearing physical activity was associated with increased BMD. Furthermore, a 2000-kcal/ week increase in vigorous activity (approximately 20 minutes of jogging per day) was associated with a 4% increase in calcaneal BMD and a 2% increase in distal radius BMD. Bone geometry of the radius, tibia,30 and hip31 is positively associated with leisure time physical activity in postmenopausal women, and metacarpal and ultradistal radius BMD correlates with occupational activity in men.32,33


Table I
Table I. Aerobic-training protocol.


On the other hand, prospective studies have also been carried out to test the impact of maintaining an active lifestyle throughout life on the bone mass of older adults and elderly people. Morseth et al34 studied a cohort of adults to find out whether leisure-time physical activity was associated with BMD and risk of osteoporosis 22 years later. In both sexes, those who participated in recreational sports at least 4 hours per week or those who regularly participated in hard-training or sports competitions had a higher BMD at both hip and forearm sites than their sedentary peers. Furthermore, the prevalence of osteoporosis decreased with increasing levels of physical activity by 8%, 6%, and 4% for sedentary, moderately active, and active subjects, respectively.

Physical activity and fracture risk
Because of the important implications that hip fractures have in elderly people, most of the studies that evaluated the association between physical activity and fracture risk have focused on the hip. Several authors have tested the importance of physical activity throughout life in prospective studies with follow-ups ranging from 4 to 35 years; they found that past and recent physical activity are important predictors of osteoporotic fractures.8,35,36 In a large cohort of elderly women Gregg et al37 showed that an increase in total physical activity was associated with a reduced relative risk of hip fracture. Specifically, very active women (>2201 kcal/week of physical activity) had a 42% reduction in the risk of hip fractures compared with the least active women (<340 kcal/week). In contrast, inactivity was associated with a higher risk of fracture; women who sat for at least 9 hours per day had a 43% higher risk of hip fracture than those who sat for less than 6 hours per day.37 Finally, a recent review has shown that moderate- to-vigorous physical activity is associated with a hip fracture risk reduction of 45% among men and 38% among women.38,39

Specific training programs
Bone-related variables can be increased—or at least the common decline in bone mass during ageing attenuated—by following specific training programs, especially in postmenopausal women.40

Because walking is a low-impact form of exercise, most of the studies that investigated the relationships between BMD and this type of activity reported no increase in bone parameters after a training program.41,42 However, the fact that aerobic exercise may maintain or slow down the loss of bone mass in elderly people must be considered an important outcome of this kind of exercise (Table I).

Strength training is one of the most frequent types of exercise programs applied in order to improve bone mass in elderly people.40 The increased mechanical stress provided by this type of training on the bone has been demonstrated as a causal factor of osteogenesis. Therefore, strength training seems to be a powerful stimulus for the improvement and maintenance of bone mass during the ageing process (Table II).43,44 Whereas benefits for the femoral neck, lumbar spine, and radius have been reported, whole-body BMD does not seem to be affected by this kind of training program, since none of the studies showed increments in this parameter.


Table II
Table II. Strength-training protocol.


Research shows that combined exercise programs can improve, or at least prevent, bone decline in postmenopausal women.45,46 However, men seem to be less susceptible to changes in bone mass, probably because of their higher initial BMD, or even because they may need exercise stimulus of higher intensity.

Whole-body vibration, which is a type of exercise that uses high-frequency mechanical stimuli generated by a vibrating platform and transmitted through the body, seems to be effective in improving BMD at different sites in postmenopausal women40; however, more research is needed to prove that this is also the case in men and for bone structure and geometry.47 Moreover, whole-body vibration training appears to have some extra benefits such as improved balance and a decrease in the number of falls, which are extremely important in preventing osteoporotic fractures.48 However, the wide differences found between studies in the current literature makes it difficult to make an in-depth comparison, and it is therefore difficult to establish which protocol of vibration has a more beneficial effect on bone mass (Table III, page 174).


Table III
Table III. Protocols of whole-body vibration found in the literature.

Summary of findings

Adequate nutrition is of great importance to guarantee optimal development and maintenance of bone structures. Combined calcium and vitamin D supplementation is effective at preventing osteoporosis as both nutrients help to reduce bone loss during the ageing process. For best therapeutic effect, minimum doses of 1200 mg of calcium and 20 μg of vitamin D (for combined calcium plus vitamin D supplementation) are recommended. In addition to calcium and vitamin D, proteins can also impact skeletal mass and the risk of fractures. On the other hand, although intake of other nutrients such as vitamin C, vitamin K, or antioxidants has been associated with increased bone mass, more research is needed in order to understand their independent associations with bone-related variables and osteoporotic fractures.

As well as appropriate nutrition, physical activity and specific training programs represent key factors for bone health, and thereby function, in the prevention or treatment of osteoporosis. Bone mass in older adults and elderly people seems to benefit from present and past physical activity. Sport practice at the time of bone mass development increases subsequent BMD, and more recent sporting activity contributes to the preservation of bone-related variables. There are two different ways by which physical activity may contribute to a higher bone mass during the ageing process; firstly, those who were active during youth have a greater BMD later in life; secondly, men and women with high levels of physical activity during adulthood and senescence experience less bone loss. Therefore, those men and women who are more active throughout life have a higher bone mass and subsequently a reduced risk of osteoporosis later in life. Moreover, physical activity appears to be a powerful stimulus to prevent osteoporotic fractures during the ageing process, especially at the hip site, while an excessive time spent in sedentary activities seems to be a potential risk factor for developing an osteoporotic fracture. In addition, specific training programs are useful to ameliorate the decline in bone mass during senescence, especially in postmenopausal women.

Finally, a combined effect and interaction between physical exercise and calcium supplementation has been shown in younger populations,49 and it seems to be more efficacious in bone development than just exercise or calcium. However, to our knowledge, the effect on bone mass acquisition of the interaction between exercise and food intake or specific diets has not been deeply studied in the elderly population; new studies are therefore needed to test this combined effect during the ageing process.

Conclusion

In conclusion, adequate nutrition and physical activity or specific training programs are good nonpharmacological treatments for preventing the decline in bone mass associated with ageing and also for the amelioration of osteoporosis and osteoporotic fractures. ■

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Keywords: ageing; bone density; calcium; exercise; fracture; nutrients; osteoporosis; proteins; training; vitamin D


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