American Journal of Clinical Nutrition, Vol. 70, No. 3, 539S-542S,
September 1999
© 1999 American Society for Clinical Nutrition
Plant-based diets and bone health: nutritional implications1,2
John JB Anderson
1 From the Department of Nutrition, Schools of Public Health and Medicine, University of North Carolina at Chapel Hill.
2 Reprints not available. Address correspondence to JJB Anderson, Department of Nutrition, University of North Carolina, Chapel Hill, NC 27599-7400. E-mail: janderso{at}sph.unc.edu.
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ABSTRACT
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Hip fracture incidence rates are predicted to increase dramatically in the first half of the 21st century, especially in Asia, Latin America, Africa, and the Middle East. These increased rates will result primarily from the effects of public health efforts to improve nutrition and infectious-disease control, both of which contribute to improved longevity of populations. An example of a rapid increase in hip fracture incidence rates has been reported in Hong Kong. Findings of studies there suggest that environmental changes, ie, westernization, urbanization, or both, are strongly related with declines in bone mineral density and increases in fractures. Hip fracture incidence rates in Western nations are typically increasing at much more modest rates than those in Hong Kong and other Asian nations. Epidemiologic investigations have identified multiple risk factors, including exposures earlier in life to adverse factors that are considered to contribute to the development of osteoporosis in both Western and Asian nations. The major risk factors are inadequate nutrition, limited physical activity, and low lifetime estrogen exposure. A dietary shift toward a more plant-based diet in Western nations may be beneficial to bone health, but is not likely to counter the adverse effects of limited physical activity and low estrogen exposure.Am J Clin Nutr 1999;70(suppl):539S42S.
Abbreviations: Bone mineral density osteoporosis hip fractures nutrient intakes physical activity lifetime estrogen exposure westernization urbanization lifestyle vegetarian diets fracture prevention
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INTRODUCTION
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Projections of increases in hip fracture rates throughout the world over the next 50 y are astounding. The huge projected increases of these fractures resulting from osteoporosis highlight the potential enormity of their effect on health-care systems (13). Many hospitals in the United States will be dedicating a much greater percentage of their beds to elderly patients with fractures of the proximal femur (hip), and will rank second only to heart disease as the reason for hospital admission for those >70 y of age. The greatest increase in hip fractures is expected to occur in Asia, where it is estimated that 50% of all such fractures in the world will be recorded by the year 2050 (2). In Western nations, hip fracture incidence and prevalence rates will continue to increase, but at much more modest rates than in Asia because of the slower increases in life expectancies in both sexes (2).
Osteoporosis-associated fractures occur at several skeletal sites in addition to the proximal femur. These fractures result primarily from low bone mineral density (BMD; 1), but deleterious changes in the bone microarchitecture, especially of trabecular tissue, also contribute significantly to the cause of fractures because of increased trabecular fragility (4).
The annual cost of medical care for osteoporosis in the United States in 1990 exceeded $10 billion and is estimated to double by the year 2000 and more than triple by 2020 (5). These projections are based on current dollars but they may underestimate considerably the actual costs because of the projected increase in the number of elderly persons (ie, >60 y of age) by the year 2020.
This review discusses factors contributing to the development of osteoporosis in women and attempts to provide explanations of the roles of the major risk factors contributing to low bone mass, measured as bone mineral content (BMC) or BMD, and fractures. Inadequate nutrition, low lifetime estrogen exposure, and limited physical activity patterns are the major factors that contribute to the current rate of osteoporotic fractures throughout the world.
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INCREASING NUMBERS OF ELDERLY PERSONS AND INCREASING HIP FRACTURE RATES
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The increasing numbers of older people in populations of many nations of the world are largely responsible for the emerging epidemic of hip fractures. In the United States, for example, an estimated 24% of the entire population will be >60 y of age by 2030. This "aging out" will occur earlier in Western nations, Japan, Hong Kong, and other nations with similarly developed economies than in developing nations, and so the crisis of hip fractures will continue well into the last half of the 21st century. The newly gained affluence of many populations since the end of World War II has given rise to westernization, or adoption lifestyle patterns common in nations like the United States, such as increased consumption of animal proteins, increased use of mechanical aids, and a general decline in physical activity. Declines in infectious disease rates in these newly affluent nations also contribute to an increase in the chronic disease of osteoporosis.
Examples of adverse effects resulting from these lifestyle changes are well illustrated by the data from Hong Kong reported by Lau and Cooper (6). These epidemiologists have linked the westernization of citizens of Hong Kong to increased hip fracture rates in both sexes over recent decades (7). Age-specific hip fractures in women in Hong Kong have increased steadily between 1966 and 1991, especially in 7080-y-olds (Table 1
).
Racial and ethnic factors also contribute to bone mass and therefore to the risk of fractures. Maggi et al (8) reviewed the published literature and showed that greatly different hip fracture rates in selected geographic areas of the world are due, in large part, to ethnicity rather than to affluence or even place of residence. The age-adjusted fracture rates of women from different parts of the world are shown in Table 2
. Rates in whites from Minnesota and California were significantly higher than those in California Asians, African Americans, or Hispanics.
In addition, usual physical activity level probably has a major influence on bone-measurement variables, but the difficulties in assessing these activities has typically made investigators leery of the data generated by such assessments, which is generally assumed to be "soft." Nevertheless, Lau and Cooper (6) amassed the findings of 3 studies that support a protective effect of customary physical activities against hip fractures (Table 3
). A report of pre- and postmenopausal Japanese women also suggests that regular physical activity increases radial BMC and BMD (9).
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ADVERSE INFLUENCE OF PLANT-BASED DIETS ON BMD
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The nutritional intakes of populations are known to vary considerably because of the availability and consumption of different foods. For example, in Asian nations, total energy and protein intakes have traditionally been lower than in Western nations, and lower intakes of these nutrients before the late 1940s, and not hereditary differences, were largely responsible for the reduced growth acceleration in height during the first 2 decades of life. A comparison of typical nutrient intake patterns between Asians, as illustrated by Japanese data, and Western populations, such as in the United States, is shown in Table 4
(10). Some of the same concepts are presented in a different way by Fujita and Fukase (11) in relation to osteoporotic fractures among Japanese.
Usual diet is another factor that has an important effect on the bone tissue of women, ie, estrogen status. Asian women have traditionally consumed diets that are predominantly vegetarian, and these women tend to have significantly lower body mass indexes (BMIs) and also lower body fat composition, ie, percentage fat (10). The lower fat mass also contributes to the lower lifetime total estrogen exposures of Asian women compared with Western women by reducing the peripheral production of estrogens. Lower lifetime exposure to estrogen is estimated from the following components: age at menarche, menstrual cycle length (especially the follicular phase), age at menopause, and peripheral production of estrogens in fat and other tissues assuming there is no estrogen replacement therapy (12) (Table 5
). Asian females, as exemplified by the Japanese, have traditionally had a later age of menarche than have Western females. In addition, onset of menopause occurs at an earlier age in Japanese than in Western women. Both menarche and menopause are influenced by the amount of accumulated body fat, which typically is lower in Asian than in Western females. The net result is that Asian women have lower BMIs, less muscle mass, and less bone mass than do Western women. The resultant lower lifetime estrogen exposure may also help explain, at least in part, why lactoovovegetarians in the United States have, in general, lower mean BMDs than similarly matched omnivores within a population (12). A meta-analysis of 3 different reports of BMD measurements of the midradius in postmenopausal US women showed that the mean BMD of lactoovovegetarians was
2% lower than that of nonvegetarians (1315).
It is still an enigma why Asian women, who have lower BMDs, currently have lower hip fracture rates than do Western women. However, the hip fracture rates of women in Japan and Hong Kong are climbing rapidly. Some potential explanations for the lower hip fracture rates in Asian women are greater physical activity, a diet with less animal protein and more phytoestrogens (from soy products), greater exposure to ultraviolet light and thus enhanced vitamin D production in the skin, and a shorter dimension of the axis from the greater trochanter of the proximal femur to the lesser trochanter. In addition, Asian women, especially the Japanese (10), consume more fish than do American women. All of these factors benefit bone mass but do not totally compensate for the typically low calcium intakes in Asian populations.
In summary, of the risk factors cited above that contribute to low BMD, Asian women have a more favorable status with respect to balanced dietary intakes from plant foods than do Western women, and possibly with respect to vitamin D status from fish consumption and sunlight exposure as well. Western women, however, have greater intakes of calcium and other nutrients from dairy foods than do Asian women. In addition, Western women have greater intakes of animal proteins and fats, but lower intakes of sodium. Compared with Western women, Asian women have a lower lifetime estrogen exposure and lower BMIs, which increase their risk of osteoporosis, particularly their BMI status.
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COMMENTS
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The concept of a healthy diet, providing adequate amounts of practically all nutrients from diverse foods, deserves mention. In several research studies, lactoovovegetarian women whose diets were apparently rich in vegetables and fruit, which supply many of the micronutrients essential for bone health, had good age-specific bone measurements, but not as good as those of nonvegetarians (1315). The bone-loss rates over time, however, appeared to be the same in these 2 groups in one study (16). In addition, many molecules found in plant foods that are not considered nutrients, eg, isoflavonesa type of phytoestrogen found in soy productsmay have a positive effect on vertebral and other sites of trabecular bone tissue of postmenopausal women, if consumed in adequate amounts (17). This isoflavone-bone relation is currently under investigation in several research centers. The important association between an adequate diet, with respect to nutrients and other components in plant foods, and bone mass needs to be emphasized because many consumers mistakenly think that calcium alone is important for bone development and maintenance.
In the future, Western nations will likely shift their dietary patterns toward greater consumption of plant foods, including soy products, and less consumption of meats, other animal products, and dairy products. These changes may be beneficial for the health of the skeleton and other organ systems, as long as total calcium intake is not compromised. In Japan, for example, the most significant sources of dietary calcium are tofu, green vegetables, small bony fish, and dairy products, mainly milk. This pattern differs greatly from that in the United States, where dairy products account for
6070% of total calcium intake (10). Dietary intake patterns for maximizing bone health are still evolving, but a consensus of thought toward the selection of optimal diets for the healthy functioning of all organ systems must eventually emerge. Asian populations may have moved closer to this goal of the optimal diet than Western societies have, except that their calcium intakes are too low and their sodium intakes are too high.
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CONCLUSIONS
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Hip fracture incidence rates are predicted to increase the most in non-Western countries. Some experts have projected that 50% of all hip fractures in the world will occur in Asia and in other less-developed regions of the world during the 21st century. These increases will likely occur in nations undergoing changes in dietary patterns, including decreased intakes of plant food and increased intakes of animal meats but not dairy products. Hip fracture rates are increasing only slightly in most Western nations, but higher rates of increases have been reported in Finland (3). Prevalence rates for hip fractures are, however, increasing in Western nations because of aging populations (1).
Broad-based preventive strategies designed to lower the risks of hip fractures need to be established and implemented in nations throughout the world if hip fracture rates are to be reduced over the next half century. A public health approach aimed at the general population appears more desirable than interventions focused on individuals. Premenarcheal girls should especially be targeted for optimal nutrient intakes and physical activities to maximize peak bone mass development, which takes place over a short period of
6 y. The tremendous growth during the passage through puberty and into late adolescence accounts for almost 50% of the total bone mass gained over a lifetime.
Western nations may benefit from changing patterns of food consumptionfrom a meat-based to a plant-based dietthat include greater consumption of products derived from soybeans and other plant foods and adequate calcium intakes. A broader recognition of the variety of nutrients essential for bone health should also emerge from ongoing research into the biological roles of several micronutrients, and even nonnutrients, that are obtained almost exclusively from plants.
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ACKNOWLEDGMENTS
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I gratefully acknowledge the contributions of Sanford Garner and Martin Kohlmeier, who helped focus the main conclusions of this review through discussion of these issues, and thank Angela M Stem for assistance with the literature search.
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