Scand J Rheumatol 1996; 25 (Suppl 103): 65-74
6. Nutrition, Life Style and Quality of Life
Roles of Diet and Physical Activity in the Prevention of Osteoporosis
J.J.B. Anderson, P. Rondano, and A. Holmes
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Department of Nutrition, Schools of Public Health and Medicine,
[lniversiv of North Carolina, at Chapel Hill, USA.
In recent years, much attention has been directed toward the prevention of osteoporosis, since this disease has become a
leading cause of morbidity and mortality in elderly women. Research has demonstrated that the prevention of osteoporosis
and osteoporosis-related fractures may best be achieved by initiating sound health behaviors early in life and continuing them
throughout life. Evidence suggests that osteoporosis is easier to prevent than to treat. In fact, healthy early life practices,
including the adequate consumption of most nutrients, regular physical activity, and other healthy behaviors, contribute to
greater bone mineral measurements and optimal peak bone mass by the fourth decade of life of females, and, perhaps,
also of males. Several reports have shown that the adequate consumption of nutrients, calcium in particular, during the
pre-pubertal and early post-pubertal years of females contribute to increased peak bone mass. Indeed, skeletal benefits from
long-term calcium supplementation have been reported for females at practically every period of the life cycle. Vitamin D,
which may be either consumed or produced endogenously through the action of sunlight, promotes calcium absorption and
thereby enhances bone mineralization. Thus, the adequate consumption of calcium, in conjunction with vitamin D, in early
life will likely optimize peak bone mass, and adequate intakes of these two nutrients should continue through the remainder
of life to help maintain bone mass. On the other hand, excess phosphorus consumption may deter bone mineral accrual
because of the resultant elevation of serum parathyroid hormone levels. Additionally, high intakes of protein, sodium, and
caffeine may decrease bone mineral mass through increased urinary excretion of calcium. Vitamin K may also have an
important positive effect on the development and maintenance of bone through its role in promoting carboxylations of the
matrix protein, osteocalcin. In conclusion, the prevention of osteoporosis needs to begin during the pre-pubertal years and
it should be continued throughout life. Bone mass can better be maintained later in life through adequate consumption of
several nutrients with specific roles in calcium and bone metabolism, regular physical activity, and the practice of a healthy
lifestyle. Mechanisms through which the nutrients and exercise affect bone mass will be explored.
Key words: osteoporosis, nutrition, physical activity, calcium, prevention, bone mineral density
The prevention of osteoporosis through dietary
means and physical activity, though simple in concept, is especially challenging in technologically
advanced societies. Although the many barriers to
instituting successful programs for the prevention
of osteoporosis remain complex, societies and their
governmental agencies must commit .to initiating
preventive programs through broadly conceived
mechanisms. For example, much preventive activity has been achieved in the United States through
the National Cholesterol Education Program to reduce cardiovascular diseases. Multiple agencies
must be mobilized within a nation to generate a focused attack on the problem of primary prevention
through school education and activity programs,
and through other agencies such as public health
and medical care systems. Members of the medical
profession, in particular, need to invest in osteoporosis prevention by incorporating lifestyle beCorrespondence: J.J.B. Anderson, Department of Nutrition, Schools of
Public Health and Medicine, University of North Carolina at Chapel
Hill, Chapel Hill, NC 27599-7400, USA.
havior modification tactics in their practices, with
a focus on diet and physical activity. Epidemiologic and prospective trial data are sufficiently
convincing that societies can now make important
advances in reducing the morbidity and mortality
of this disease in future generations.
This review focuses on the impacts of nutritional
factors, and less so of physical activity, on bone
health across the life cycle and the potential improvement in bone mass through healthy behaviors
(Fig. 1). Females are highlighted because osteoporosis is almost twice as prevalent in females as
in males. In addition, this review develops the concept that optimal nutrition, in its broadest context,
must be considered in any osteoporosis prevention
program.
Concept of Optimal Nutrition
for Bone Health
Nutritional requirements of individuals cannot
65
J.J.B. Anderson, P. Rondano, and A. Holmes
mation and new interpretations of current and past
research data (32).
Although it may be impossible to establish with
precision the truly optimal diet of a population,
ranges or windows of reasonable intakes for good
bone health can be approximated for the macronutrients and many, but certainly not all, of the micronutrients (Fig. 2). Furthermore, very little quantitative data are available to establish recommenda-
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easily be determined. Population estimates of
needs, however, have been established and reasonable recommendations, based on the currently
available scientific data, have been made by the
World Health Organization and many nations. In
the United States the Recommended Dietary Allowances (RDAs) were last published in 1989 (35).
These RDAs, such as the one for calcium, have
been seriously questioned because of new infor-
Figure 1: The impact of multiple environmental factors - diet, physical activity, and behavior - on bone health.
66
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Roles of Diet and Physical Activity in the Prevention of Osteoporosis
tions for dietary fiber and a great variety of phytochemicals found in foods of the plant kingdom that
may benefit health in diverse ways.
Numerous macro- and micronutrients play critical roles in bone development and maintenance
(Table I). Unfortonately, knowledge of specific
amounts of these nutrients necessary to support optimal bone development and preservation is limited
by the dearth of research on most nutrients, except
for calcium, phosphorus, and vitamin D. Whereas
most investigations of bone have focused primarily
on calcium, clearly an important nutrient for bone
health, other nutrients and their relationships to
bone tissue have been practically ignored. Very little is known about the nutritional needs of bone tissue for zinc, manganese, magnesium, folate, other
B vitamins, vitamin C, vitamin K, and iron, all
of which have been established to have essential
functions in this tissue. The importance of these
micronutrients must not be ignored in our enthusiasm for calcium, Achieving optimal intakes of all
nutrients (or as near to optimal intakes as possible)
must be coupled with other optimal health behaviors, including regular physical activities, and the
avoidance of adverse behaviors, such as cigarette
smoking and excessive alcohol and drug use.
It has been reported that excessive calcium intakes from supplements may impair the absorption
of utilization of trace minerals, such as iron (12).
Therefore, focusing attention on calcium alone to
the detriment of the significance of other nutrients in bone development and maintenance may
be counterproductive in an osteoporosis prevention
program.
The remainder of this review examines the
known needs of nutrients at the critical stages of
the life cycle beyond infancy in relation to optimal
measurements of bone mineral content (BMC) or
density (BMD) at multiple skeletal sites. Wherever possible, reference to the benefits of physical
activity on bone will be cited. Data on females
Figure 2: Diverse roles of nutrients -both macro and micro-nutrients - in the optimal development and maintenance
of bone tissue, along with physical activity and hormones, which contribute to bone health.
67
J.J. B. Anderson, P. Rondano, and A. Holmes
Table I: Effects of specific nutrients on bone.
Positive Effects
1 Calcium
I Mineralization cell regulation
Magnesium
Multiple Enzymes
Iron
Cell energetics collagen maturation
Zinc
Multiple enzymes
Manganese
Multiple enzymes bone development
Mineralization cell energetics
Phosphorus
~~
I
~
Protein
Cell development
Vitamin D
Ca absorption
Folate
Cell maintenance
ni2
Cell matntenance
Vitamin K
Osteocalcin productlon carboxylations
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~~~
I
Vitamin C
Hydroxylation of proline & lysine
Fluonde
Bone strength
Adverse effects
1 Protein
1 Phosphorus
Sodium
1 Fluonde
I
I Hypercalciuria
Secondary hyperparathyroidism
Hsnercalciuria
I Brittle bones. fractures
I
are emphasized; yet occasional reference will be
made to males.
Prepubertal Females and
Bone Development
The demand for calcium during this critical period
of skeletal growth is probably greater than at any
other period of the life cycle. During this time females, as well as males at the similar developmental
stage, typically accumulate a significant amount of
bone mass. This increment41 amount of BMC is
highly correlated with calcium intakes at or above
the current RDAs for calcium, as demonstrated by
the study of Johnston et al. (17). No other prospective study of peripubertal females has been published on the relationship of bone measurements to
calcium or any other nutrient. Table I1 lists tha
highlights of this and one other study (1). Observational data by Chan (8) suggest that low calcium
intakes by prepubertal girls compromise their accrual of bone mass.
An association between physical activity and
BMC has not been prospectively investigated
among prepubertal girls, but positive benefits of
regular physical activities at almost every period
of the life cycle are presumed.
The beneficial effects of health behavior modifications through intervention studies have been
demonstrated to be successful in children as early as
9 years of age (19). For example, children between
9 and 12 years improved their nutritional habits
and showed better awareness of healthy foods in
response to participation in a nutrition program designed for themselves and their parents (21). On
the other hand, serious disordered eating patterns
may begin as early as 9 years of age, according to
one study (28). Therefore, implementing nutrition
programs for young school-aged children and their
parents may be the most effective means of instituting behavior modification and promoting life-long
healthy eating habits.
Postpubertal Females (Teens) and
Peak Bone Mass Development
Although the major impact of adequate calcium intakes on bone development occurs before menarche, accrual of bone mass continues at a fairly high
rate for approximately four more years (6,41). The
relationship of calcium intake to BMC or BMD during this pubertal growth spurt is much less robust
than during prepuberty (17,23,25). The onset of the
sex hormones related to post-menarcheal growth
apparently dominates the growth pattern so long as
nutrients and energy are supplied in amounts sufficient to support growth (13). Fig. 3 illustrates the
limited effect of calcium and probably other nutrients on bone during this hormone-dominant period.
Tublr 11: Prepubertal females: effects of specific nutrients on bone mineral content/density.
Calcium supplement
Johnsion et al 1992
Positive on each
Prospective
Cdlcrum diet-
Abrams et al 1994
Positive on each
Prospective
*Diet: usual dierary intake. with no supplementation.
68
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Roles of Diet and Physical Activity in the Prevention of Osteoporosis
Bone accumulation with adequate calcium intakes,
i.e., approaching the RDA, continues from 16 to 20
years in females, but at a greatly reduced rate (42).
Inadequate intakes of vitamin D have been reported in Finnish children and adolescents who do
not have vitamin D-fortified milk products available
in their country (22). Calcium absorption and bone
mass accumulation, therefore, may have been impaired in these youths, especially during the winter
months. Excessive dietary fiber consumption may
also deleteriously impact bone mass accumulation
in adolescent girls (13). Table 111 highlights the
effects of these nutrients.
Adverse effects of high intakes of phosphate,
(and also protein and sodium) may occur in adolescent females. Heavy consumption of soft drinks
containing phosphoric acid, coupled with low cal-
cium intakes, may negatively affect the skeletal
accumulation of calcium (7). Many females during the teenage years avoid milk and other dairy
products because of a concern about dietary fat
consumption. These post-pubertal girls oftentimes
modify their diets through the inclusion of cola-type
beverages and other high-phosphorus, low-calcium
food products, and consequently develop a chronic
elevation of serum parathyroid hormone (PTH),although PTH remains within the normal range. For
example, soda drinks, but not dairy products, were
among the most preferred foodhverages of adolescents in the study of midwestem teenagers in the
United States (39). These girls typically not only
compromise their calcium intakes to a significant
extent but also their intakes of several other essential nutrients provided by dairy products (4). Persistently elevated PTH levels may have an adverse
Effects of
Calcium and Other Nutrients
Over Time
Figure 3: Hourglass figure illustrating the limited effectiveness of calcium (and probably other nutrients), administered
as a supplement, on bone mass during two critical periods of the life cycle, namely, puberty (menarche and
early postmenarche), and menopause, including the early postmenopause of approximately five years. These two
constrictions represent periods when increases in hormones - growth-related hormones, especially sex steroids
- or losses of ovarian hormones so dominate bone cell functions that calcium supplementation is without much
effect on bone mass or density.
69
J.J.B. Anderson, P . Rondano, and A. Holmes
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effect on the apposition of bone mineral, thereby
impairing the development of optimal bone mass
in these growing females. Long-term studies are
needed to confirm the relationship between elevated
PTH and the potential reduction of peak bone mass
(PBM), i.e. reduced BMC.
Regular physical activity patterns have been
shown to make important contributions to bone
mass accrual in adolescents (42). A positive interaction between physical activity and calcium intake
during this growth phase, suggested by several earlier reports (15,18,42), has not been verified by
a recent study employing retrospective questionnaires of adult women (31).
The modification of adolescent health habits has
been notoriously difficult to achieve, not only in nutrition but in other areas of behavior as well. Adolescents with the best attitudes about food-related
behaviors and balanced nutritional intakes typically
have parents who take an interest in these issues
(39). Adolescents themselves defined lack of time,
lack of self-discipline, and lack of self-urgency as
barriers to attaining healthy eating behaviors (39).
Research findings suggest that in order to practice
good nutrition adolescents must improve decisionmaking skills, to become more assertive, and to
resist peer pressure. These improved skills must
be positively reinforced by teachers, parents, and
peers. Additionally, much literature suggests that
females must learn to have a more positive image about their own body conformations and to
strengthen their own locus of control about health
and positive eating habits (39).
Early Adult Females, Bone
Consolidation, and Peak
Bone Mass Accrual
Bone consolidation continues in females after
growth in height ceases at approximately 16 to
18 years of age. Therefore, an adequate supply of
dietary calcium is necessary for calcium accumulation in the skeleton. Calcium intakes during both
the teen years and the current time were found to
correlate highly with BMC and BMD of women
in their 30s (31). Baran et al. (3) demonstrated in
a three-year prospective study that diets, improved
by the daily addition of dairy products each day,
contributed to better bone measurements of women
in their 30s compared to control women who did
not receive additional calcium-rich foods. Calcium
acts independently on bone to enhance PBM at
least up to age 30, especially in the forearm bones
(15) and in the total body BMC, but probably not
in the lumbar vertebrae or proximal femur (hip)
after adolescence ends (6,41). Although the RDA
in the United States is set at 1200 mg per day up
to age 25, published studies suggest that intakes
of 800-1000 mg per day are most likely sufficient
to support optimal development of PBM in young
adult females (30,36). These estimates coincide
with calcium balance data determined by Matkovic
and Heaney (26). Adverse skeletal effects of high
intakes of phosphorus, protein (only animal protein,
probably), and sodium have been reported (29,30).
Table IV lists the effects of several nutrients on
bone.
Data on the relationships of other nutrients to
bone mass, especially PBM development, are lacking. In an intriguing study of young adult male and
female dialysis patients, fractures were found to be
more common in those who had poor vitamin K
status (20).
Table Ill: Postpubertal females: effects of specific nutrients on bone mineral contentldensity.
Nutnent
Study
Effects on BMCBMD
Comments on study
Calcium supplement
Johnston et al 1992
None on either
Prospective
Calcium supplement
Lloyd et al 1993
Positive on each
Prospective
Calcium supplement
Matkovic et al 1990
Positive on each**
Prospective
Calcium diet*
Tylavsky et al 1992
Positive on each
Cross-sectional
Phosphorus diet*
Tylavsky et al 1992
Negative on each
Cross-sectional
Protein diet*
Tylavsky et al 1992
Negative on each
Cross-sectional
Ftber diet*
Dhuper et al 1990
Negative on each
Prospective
*Diet: usual dietary intake, with no supplementation.
**Not significant.
70
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Roles of Diet and Physical Activity in the Prevention of Osteoporosis
investigated for ten years while in their mid-60s
lost bone mass at about the same rate, but the highcalcium consumers lost BMC at a slightly greater
rate than the low-calcium consumers. Furthermore,
the high consumers of calcium who started the
study with greater BMC had significantly less at
the end of the ten-year period compared to the low
consumers (5). The nutrient-bone findings of these
studies are given in Table V.
Investigations of the effects of other nutrients on
the skeleton during the first decade or so after the
menopause are essentially non-existent.
Postmenopausal women who have volunteered
for prospective exercise or strength conditioning
programs have typically shown improvements in
their bone measurements after a year of study, but
they lost this accrued bone after the program was
discontinued (10). The obvious conclusion is that
exercise or stress on the skeleton is beneficial as
long as it is continued on a regular basis.
Physical activity, when practiced regularly, has
a positive effect on BMC and BMD in young
adult women (15,18,30,31). Prospective studies are
clearly needed on the exercise-bone relationship in
young adult women.
When females reach adulthood at age 20, they
appear to be more open to improving their health
behaviors. Women who exercise regularly are more
likely to maintain their bone mass as they proceed
toward the menopause or, in the case of radial
bone, they may even improve their BMC and BMD
(I 5,43). Avoidance of cigarette smoking, minimal
or no alcohol consumption, and the absence of other
adverse behaviors support the maintenance of PBM
achieved by age 30 right up to the menopause.
Menopausal and Early
Postmenopausal Women
Several studies have reported that calcium supplementation during the early menopause has had little or no effect on BMC or BMD (11,33,38), as
illustrated in Fig. 3. Elders et al. (14) showed,
however, that additional calcium administered to
perimenopausal women did significantly reduce the
amount of bone loss. Lukert et al. (24) demonstrated that an adequate vitamin D nutritional status
of perimenopausal women was partially protective
against bone loss during the menopausal transition
by reducing the serum concentration of parathyroid
hormone.
Dawson-Hughes et al. (1 1) demonstrated that
calcium supplementation of women five years beyond the menopause resulted in significant gains of
BMD at several sites compared to placebo-treated
control subjects. Unsupplemented Dutch women
Late Postmenopausal Women
The report of Chapuy et al. (9) demonstrated unequivocally that elderly women living in nursing
homes benefit from supplemental calcium, as calcium phosphate, and vitamin D. The French women
in this study showed significant gains in BMD at
several sites and, perhaps more importantly, reductions in hip and other non-vertebral fractures. The
obvious conclusion derived from these findings is
that elderly shut-ins in much of the developed world
do not have adequate intakes of these nutrients to
maintain their bone tissue. Secondary prevention
of fractures in such elderly subjects through dietary
means is relatively simple and economical, as the
Table ZV: Early adult females, bone consolidation, and peak bone mass accrual: effect of
specific nutrients on bone mineral contentldensity.
Nutrient
Study
Effects on BMCBMD
Coinments on study
Calcium diet*
Recker et al. 1992
Positive on each
Prospective
Calcium diet*
Halioua et al. I989
Positive on each
Cross-sectional
Calcium diet*
Metz et al. 1993
Positive on each
Cross-sectional
Phosphorus diet*
Metz et al. 1993
Negative on each
Cross-sectional
Protein diet*
Recker et al. 1992
Negative on each
Prospective
Protein diet*
Metz et al. 1993
Negative on each
Cross-sectional
Sodium diet*
Metz et al. 1995
Negative on each
Cross-sectional
Calcium foods**
Baran et al. 1990
Positive on each
Prospective
*Diet: usual dietary intake, with no supplementation.
**Foods: calcium-rich foods added to diets of experimental subjects only.
71
J.J.B. Anderson, P. Ronduno,and A. Holmes
Table V: Menopausal and early postmenopausal women: effects of specific nutrients on bone mineral contentldensity.
Nutrient
Study
Effects on BMCBMD
Comments on study
Calcium supplement
Nilas et al. 1984
None on either
Prospective
Calcium supplement
Riis et al. 1987
None on either
Prospective
Calcium supplement
Dawson-Huges et al. 1990
None on either
Prospective
Calcium supplement
Dawson-Huges et al. 1990
Positive on each
Prospective
Calcium diet*
Beresteijn et al. 1991
Negative on each
Prospective
Vitamin K status**
Kohlmeier et al. 1995
Positive
Fracture reduction
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+5 years
usual dietary intake, with no supplementation
**Status Subjects diets were not analized, only serum vitamn K concentrations
Table VI: Late postmenopausal women: effects of specific nutrients on bone mineral contentldensity.
1
Study
Effects on BMClBMD
Comments on study
j Calcium and Vitamin D
supplements
Chapuy et al 1992
Positive on each
Prospective; fracture reduction
j Calcium diet"
Reed et al. 1994
Negative on each
Prospective follow-up
Matkovic et al 1979
Positive on each
Cross-sectional
Onmo et al 1995
Positive on each
Prospective
4
Nutnent
I
~
Calcium diets
, Vitamin
K supplement
*Diet usual dietary intake. with no supplement
investigators of this study so readily demonstrated.
The retrospective study of Matkovic and colleagues
(27) in two communities of Yugoslavia (now Croatia), one consuming dairy products regularly and
the other not, supports the findings of the French
investigators.
A five-year prospective study of free-living elderly women (mean age of 77 to 82 years) revealed
that they all lost BMC and BMD, despite variations
in their calcium intakes (37). Both low- and highcalcium consuming women exhibited bone mass
loss rates of approximately 1% per year. In addition, lacto-ovo-vegetarian women, representing approximately 25% of the subjects, lost BMC and
BMD at essentially the same rate as the omnivorous
women. These results, in support of the Beresteijn
findings of younger postmenopausal women, suggest that calcium alone, even at or above recommended intake amounts, is not sufficient to slow
the inexorable rate of bone mass loss late in life.
inadequate consumption of others micronutrients,
of course, may have skewed or confounded the results. Potentially important in the Reed study may
have been inadequate consumption of vitamin D or
vitamin K, neither of which was measured. Several
72
trace elements have been supplemented to the diets
of elderly female subjects in one study (40), but the
marginal improvements in BMD have not yet been
substantiated by other studies. The reported data
on the diet-skeletal relationships of these studies
are provided in Table VI.
Prospective studies of the effects of physical activity programs on changes in bone measurements
of elderly women have not been so illuminating
because of the equivocal results reported.
Concluding Remarks
A focus on behavior modification must be adopted
by societies to effectively lower incidence rates
of hip and other fractures in future generations.
Pre- and postpubertal girls can gain the most in
their bone mass values by adopting healthy nutritional and physical activity behaviors, but they need
support from parents, teachers, coaches, and other
mentors in their communities. Programs for the
primary prevention of osteoporosis need to be instituted and implemented in practically all nations
of the world, especially those which are technologically advanced (2). Goals must be set which can
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Roles of Diet and Physical Activity in the Prevention of Osteoporosis
be measured at 5- or 10-year intervals. Primary
prevention strategies aimed at the general public
may be the most cost-effective in the long run, although evidence to support this contention is not
yet available.
Secondary prevention strategies must also be implemented and supported by nations to delay or reduce fractures among postmenopausal women and
the elderly of both genders. Simple dietary strategies, such as supplementation of calcium, essential
vitamins, and trace elements, may be sufficient to
maintain or even improve BMD (9). Tertiary prevention (or treatment) through the use of drugs will
also become more important in future generations,
but the use of drugs and related medical care is less
cost-effective than simpler nutritional supplementation and fortification of foods.
Finally, the clinical significance of optimal intakes of all nutrients should be acknowledged and
acted upon in populations of elderly subjects if fracture rates are to be substantially reduced. Heaney
(16) pointed out a decade ago that nutritional support of the skeleton was essential for the maintenance of bone mass and the reduction of bone loss
and bone fragility in late life. What is needed now
is the will of societies to put into effect the prevention strategies, especially behavioral-change initiatives, that can reduce the burden of hip fractures in
the twenty-first century.
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