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Calcium Intake Trends and Health Consequences from
Childhood through Adulthood
Theresa A. Nicklas DrPH, LN
a
a
USDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College
of Medicine, Houston, Texas
Published online: 19 Jun 2013.
To cite this article: Theresa A. Nicklas DrPH, LN (2003) Calcium Intake Trends and Health Consequences from Childhood
through Adulthood, Journal of the American College of Nutrition, 22:5, 340-356, DOI: 10.1080/07315724.2003.10719317
To link to this article: http://dx.doi.org/10.1080/07315724.2003.10719317
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Review
Calcium Intake Trends and Health Consequences from
Childhood through Adulthood
Theresa A. Nicklas, DrPH, LN
USDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas
Downloaded by [USP University of Sao Paulo] at 07:19 27 September 2013
Key words: children’s diets, calcium, dairy products, school meal participation, public policy
Issues involving low calcium intake and dairy product consumption are currently the focus of much debate
and discussion at both the scientific and lay community levels. In this review, we examine the following major
areas of interest: (1) the role of calcium intake and dairy product consumption in chronic diseases, (2) nutritional
qualities of milk and other dairy products, (3) trends in calcium intake and dairy product consumption, (4) current
status of calcium intakes and dairy product consumption in children, (5) tracking of calcium intake and diary
product consumption, (6) the impact of school meal participation on calcium intake and dairy product
consumption, (7) concerns related to calcium-fortified foods and beverages and (8) factors influencing children’s
milk consumption. To date, the findings indicate that calcium intake and dairy product consumption have
beneficial roles in a variety of chronic diseases; dairy products provide an abundant source of vitamins and
minerals; calcium intakes of children have increased over time, yet intakes are not meeting the current adequate
intake (AI) calcium recommendations; dairy consumption has decreased, and soft drink consumption and,
possibly, consumption of calcium-fortified products have increased; consumption of dairy products have a
positive nutritional impact on diets of children, particularly from school meals, and there are many factors which
influence children’s milk consumption, all of which need to be considered in our efforts to promote adequate
calcium intakes by children. Based on this review, areas that need immediate attention and future research
imperatives are summarized in an effort to further our understanding on what we already know and what we need
to know to promote healthier eating habits early in life.
Key teaching points:
•
•
•
•
Calcium intake and dairy products play an important role in prevention of several chronic diseases.
Children’s dietary intakes fall short of current adequate intake calcium recommendations.
Consumption of dairy products in school meals has a positive nutritional impact on diets of children.
Children’s milk consumption is influenced by a number of factors which need to be addressed in our promotion efforts.
ovarian cancer [29], premenstrual syndrome [30,31], insulin resistance syndrome [32], obesity [33–37] and lead poisoning [38 – 42].
Osteoporosis. In 1997, the National Osteoporosis Foundation published its first report on the prevalence of osteoporosis
[43]. Osteoporosis and low bone mass are currently perceived
major public health threats for an estimated 44 million U.S.
women and men over the age of 50. It is projected that by the
year 2010, an estimated 52 million women and men in the same
Calcium Intake, Dairy Product Consumption and
Chronic Disease
During the past 25 years, research has demonstrated the potentially beneficial roles for calcium and/or dairy foods with regard to a variety of disorders. These disorders include osteoporosis
[1–7], hypertension [8 –17], colon cancer [18 –23], breast cancer
[23,24], kidney stones [25–27], polycystic ovary syndrome [28],
Address reprint requests to: Theresa A. Nicklas, DrPH, LN, Professor, Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, 1100
Bates Street, Houston, TX 77030. E-mail: [email protected]
This research was supported by the National Heart, Lung, and Blood Institute of the U.S. Public Health Service (USPHS), HL388440. This work is a publication of the
USDA/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas, and has been funded in part by the National
Dairy Council. The contents of this publication do not necessarily reflect the views or policies of the USDA, nor does mention of trade names, commercial products, or
organizations imply endorsement by the U.S. Government.
Journal of the American College of Nutrition, Vol. 22, No. 5, 340–356 (2003)
Published by the American College of Nutrition
340
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Calcium and Health from Childhood through Adulthood
age category will be affected, a figure that will increase to over
60 million by 2020 [43]. Osteoporosis, which is associated with
low calcium intakes has been called the “pediatric disease with
geriatric consequences” [44–46]. Direct health care costs for
treatment of osteoporotic fractures are estimated at $10 to $15
billion per year [47].
Calcium intake influences the risk of osteoporosis by affecting genetically determined peak bone mass, a state that is
reached by age 30 or earlier [7,45,46,48–52]. Much of the
genetically determined peak bone mass is accumulated during
the first two decades of life; thus, childhood and adolescence
are the critical times to optimize peak bone mass [50,53].
During adolescence, 45% or more of the body’s total skeletal
mass is formed [50]. Children’s bodies need sufficient calcium
to support an accelerated growth spurt during the preteen and
teenage years. In addition, during this time period, children are
laying the foundations of their peak bone mass, which will have
a tremendous impact on their bone density during their older
years. Young girls whose dietary calcium intake was provided
primarily by dairy products had an increased rate of bone
mineralization [54]. Sandler et al. [55] found that females 49 to
66 years of age who reported drinking milk with every meal
during their childhood and adolescent years had significantly
higher bone densities than females who reported lower intakes.
It is therefore understandable that prevention begins in childhood and adolescence during growth and skeletal development.
Increased calcium intake is not the only panacea for osteoporosis
prevention. There are several other nutritional and lifestyle factors,
such as the amount of protein in the diet, energy intake, body
weight, alcohol consumption, Vitamin D intake, smoking, and
exercise, which have been shown to play a potential role in
affecting bone mass. However, the scientific reproducible evidence showing a connection between these factors and bone mass
are not as convincing as the calcium connection. The consensus
from several organizations [2,3,53,56] is that low calcium intake is
a major player in the development of osteoporosis and the incorporation of dairy products into one’s eating lifestyle is one way to
not only obtain adequate calcium but other essential vitamins and
minerals.
Hypertension. Hypertension is present in an estimated 43
million Americans in the United States [53]. Twenty-three
percent of Americans 20 to 74 years of age were diagnosed
with hypertension from 1988 to 1994. It is more prevalent in
African-Americans (AA); more than three-quarters of AA
women 75 years of age and over have been diagnosed with
hypertension [53].
After nearly 20 years of debate, there is now sufficient,
reproducible evidence supporting a beneficial role for calcium
or calcium-rich dairy foods in blood pressure regulation [8–17].
In the DASH (Dietary Approaches to Stop Hypertension) study
[57,58] 549 people consumed a combination diet rich in fruits
and vegetables and low-fat dairy products (⬃3 servings/day).
The combination diet reduced their systolic blood pressure 5.5
mm Hg and diastolic blood pressure 3.0 mm Hg more than the
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION
control diet. Among those participants diagnosed with hypertension, the combination diet reduced systolic blood pressure
by 11.4 mm Hg and diastolic pressure by 5.5 mm Hg more than
the control diet [57,59]. African-Americans, who are at a disproportionately higher risk for hypertension, had twice the
blood pressure lowering effect relative to Caucasians and none
dropped out due to intolerance to dairy products [60]. These
results from the initial DASH trial [57] were replicated in
DASH sodium [61]. Research indicates that a calcium intake at
the recommended level and a combination diet rich in fruits and
vegetables and low-fat dairy products may be helpful in preventing and treating moderate hypertension [62].
Obesity. The prevalence of obesity in the United States and
other developed countries has reached epidemic proportions
[63–66]. Between 1980 and 1990, the prevalence of obesity in
U.S. adults increased 40% [67] and continues to increase [65].
About 65% of American adults are now considered either
overweight or obese [65]. Obesity contributes to five of the ten
leading causes of death in the United States. It increases the risk
for heart disease, stroke, high blood pressure, certain types of
cancer, diabetes and many other health problems [68]. Direct
and indirect costs associated with obesity exceed $99 billion
annually [69,70].
The increasing prevalence of obesity in children parallels
that of adults [66]. The prevalence of obesity among children 6
to 11 years of age increased 54% from 1960 to 1994, while
prevalence of obesity among adolescents 12 to 17 year of age
increased 40% [71] during the same time period. The increase
in the prevalence of overweight between 1960 and 1994 was
similar to that observed between 1988–1994 and 1999–2000
[66]. Currently, 10.4% of preschool children, 15.3% of schoolage children and 15.5% of adolescents are overweight (BMI ⬎
95th percentile) [66].
Obesity tracks over time; that is, obese children, particularly
obese adolescents, tend to become obese adults [72–74]. Overweight children tend to remain overweight during follow-up
periods of up to 20 years [75–77] and, in general, have a 1.5 to
twofold increased risk of being overweight as adults. Sixty-two
percent of Bogalusa 10-year-olds in the upper quartile for BMI
continued to be in the upper quartile when they were young
adults. Children’s BMI at age 10 was significantly (p ⬍
0.0001) correlated with BMI when they were young adults (r ⫽
0.66) (data not shown).
Epidemiologic and experimental studies suggest that dairy
products may have favorable effects on body weight in children
[36,37] and adults [33,35,78,79]. Intracellular calcium has been
shown to play a key role in metabolic disorders associated with
obesity and insulin resistance [80–82]. Data from studies conducted by Zemel et al. [34] demonstrated that women with the
highest calcium (1300 mg/day) and dairy food intake (3⫹
servings/day) had an 80% lower risk of being in the highest
quartile of body fatness. A profound reduction in the odds of
being in the highest quartile of adiposity was associated with
increases in calcium and dairy product intake. The authors
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Calcium and Health from Childhood through Adulthood
showed that for any given level of energy intake and expenditure, low dietary intake of calcium favored increased efficiency
of energy storage, and higher-calcium diets favored thermogenesis. In a study of adipose cells in transgenic mice [83],
high-calcium, medium-dairy and high-dairy diets reduced lipogenesis, stimulated lipolysis and reduced body fat accumulation
at equivalent levels of energy intake. Moreover, the dairy diets
were more effective than the calcium supplemented diet. Another study of adipose cells from mice demonstrated that a high
calcium, medium-dairy and high-dairy diet produced greater
weight/fat loss in energy restricted diets compared to energy
restriction alone [34]. These findings in animal studies were
also shown in preschool children [36,37]; children with higher
dairy intakes had lower body fat. These observations suggest
that there may be a positive relationship between dietary calcium intake and the regulation of body fat/weight and that
calcium intake explains only part of this effect.
In an exercise intervention study [79], higher calcium intakes were associated with weight loss, specifically loss of fat,
in women 18 to 31 years of age. In a retrospective analysis of
five earlier trials, a placebo-controlled calcium supplementation trial found significantly greater weight loss in elderly
women supplemented with 1,200 mg of calcium/day compared
to the control group [33]. Two studies have reported the effects
of weight reduction diets with and without milk [84,85]. Both
studies suggest that a high milk intake increases the effectiveness of a weight reduction program. However, in a multicenter,
randomized controlled trial [86], adults assigned to the milksupplemented group gained slightly more weight (0.6 kg) than
the control group, although it was less than predicted, suggesting some compensation for the added energy from milk.
Clearly, more research is needed to confirm tile benefits of
calcium and dairy foods for maintaining a healthy body weight.
Osteoporosis, hypertension and obesity begin developing
early in life [35,55,87,88]. This fact suggests that prevention
efforts should begin in childhood. Because eating habits developed in childhood set the stage for similar eating habits later in
life, the adoption of healthier eating habits in childhood can
reduce the risk of developing chronic diseases in later life.
Nutritional Qualities of Milk and Other Dairy
Products
Milk and other dairy products are among the best natural
sources of calcium. They offer high calcium bioavailability,
have a high calcium content and may be obtained at low cost
relative to their nutritional value [1,2,89 –99]. Dairy products
also provide an abundant food source of phosphorus, potassium, riboflavin, vitamins B12 and A, protein, magnesium and
niacin (niacin equivalents) [93,94]. Additionally, most milk and
some yogurt are fortified with Vitamin D. Because milk and
other dairy products are nutrient-dense foods, their intake improves the overall nutritional quality of children’s [100,101]
and adolescents’ diets [102–107]. According to Healthy People
342
2010, “with current food selection practices, use of dairy products may constitute the difference between getting enough
calcium in one’s diet or not” [108].
Trends in Calcium Intake and Dairy Product
Consumption
The Bogalusa Heart study, as well as epidemiologic investigation of the early natural history of heart disease, provides a
unique opportunity to examine trends in food consumption over
the past two decades (1973–1994). In the Bogalusa Heart
Study, the percentage of 10-year-old children consuming milk
declined while the percentage consuming cheese increased. The
percentage consuming fruits/fruit juices increased and the percent consuming sweetened beverages (e.g., soft drinks, tea and
coffee with sugar, fruit flavored drinks) decreased. Mean gram
consumption of sweetened beverages, cheese and fruit/fruit
juices increased. However, the increase in mean gram consumption of sweetened beverages significantly increased in the
moderate-to-high sweetened beverage consumers over time.
Mean gram consumption of milk significantly decreased. Despite the increasing trend in cheese consumption, the decreasing trend in milk consumption resulted in an overall decrease in
dairy product consumption in 1993–94. It is important to note
that the increase in gram amount of cheese consumed was only
18 grams compared to a 64-gram decrease in milk consumption. Similar trends have been observed in other studies
[102,104,109 –111,115] and in the U.S. food supply [112].
Despite the trends observed in the percentage of children consuming dairy products and mean gram consumption of dairy
products, total calcium intake significantly increased (p ⬍
0.0001) and saturated fatty acid intake decreased [113] from
1973 to 1994 among 10-year-old children (Fig. 1). The data
suggest that despite a reduction in the percentage of children
consuming milk, calcium intake of the children was not compromised, indicating that the children obtained their calcium
from other dairy products (e.g., cheese) and possibly from
calcium-fortified foods. Although calcium intakes of children
may have increased over the past two decades, the majority of
children are not meeting current dietary or adequate intake (AI)
recommendations for calcium [109].
Trends in beverage consumption among children and adolescents suggest that soft drinks may be replacing more nutritious beverages, such as milk and fruit juices [101,102]. A
comparison between milk drinkers and soda drinkers showed
that increased soda consumption had a negative impact on milk
consumption and on intakes of many essential micronutrients
[102]. This is a matter of concern because intake of these
beverages and some of the nutrients contained in them, like
calcium, is suboptimal for a substantial proportion of children
in the United States. Data from national surveys indicate that,
particularly in teenagers, the calcium intake is below the recommended dietary allowance. Findings from one study [114]
indicated that children whose intake of calcium was less than
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Calcium and Health from Childhood through Adulthood
Fig. 1. Mean Calcium Intake by 10-year-olds: 1973–1994. Source: The Bogalusa Heart Study.
the RDA consumed more soft drinks than milk and dairy
products.
Current Calcium Intakes of Children
Current dietary recommendations for calcium are 800 mg/
day for children 4 to 8 years of age, and 1,300 mg/day for
children and adolescents 9 to 18 years of age [53]. At all ages,
dietary calcium intake declines as children get older and females consume less calcium than males. Data from the 1994 –
1996 CSFII showed that the majority of children have a usual
intake of calcium that is less than 100% of the calcium AI
[109]. Seventy-one percent of girls and 62% of boys 6 to 11
years of age do not meet 100% of the AI for calcium [109].
Similar results were observed for 10-year-old children in Bogalusa, Louisiana, where 69% did not meet the dietary recommendation of 1300 mg/day; the percentage was higher among
females (76%) than males (62%) (p ⬍ 0.001) (Table 1). In two
young adult surveys, more females than males did not meet the
calcium recommendation (Table 1). Among older females and
males 12 to 19 years of age, 88% and 68%, respectively, did not
meet the calcium recommendation [109]. That means nearly
nine out of ten adolescent girls and seven out of ten adolescent
boys failed to meet the AI for calcium. Caucasians and Hispanics had higher calcium intake levels than African-Americans and “others” [109,115,116]. Among young adults (19 to
28 years of age), 77% did not meet the AI for calcium, particularly females (82%) (Table 1).
Food Sources of Calcium Intake. Calcium is widely distributed in both plant and animal foods. In the United States,
about 50% of total dietary calcium intake was supplied by milk
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION
and milk products [95,117]. Milk and cheese used as ingredients in meat, grain and vegetable mixtures contributed another
20% of dietary calcium. The remaining 30% of calcium was
provided by grains, meat, fish, poultry, vegetables, fruits, eggs,
legumes, nuts and seeds. Similarly, in Bogalusa 10-year-olds, a
variety of foods contributed to calcium intake (Fig. 2), the
majority of which came from milk products. The proportion of
dietary calcium contributed by milk and milk products decreased with age; children between 1 and 2 years of age
obtained 83% of calcium from milk and milk products, teenage
girls 77% and adults between 65% and 72%.
Comparison with Food Guide Pyramid. Because of the
health benefits of increased calcium consumption, national
dietary guidelines recommend that Americans, including children 2 years and over, consume three to four servings of dairy
Table 1. Percentage of Children and Young Adults Not
Meeting the AI Calcium Recommendation
Total
Ethnicity
EA
AA
Gender
Male
Female
Children
N (%) ⫹
Young Adult
(1989–91)
N (%)⫹⫹
Young Adult
(1995–96)
N (%)
150 (69)
386 (77)
1030 (77)
89 (70)
61 (69)
265 (75)
121 (80)
765 (79)
266 (73)*
63 (62)
87 (76)*
145 (69)
241 (82)***
368 (72)
662 (80)**
* p ⬍ 0.05, ** p ⬍ 0.01, *** p ⬍ 0.001
⫹ ⱖ 1300 mg Calcium
⫹⫹ ⱖ 1000 mg Calcium
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Calcium and Health from Childhood through Adulthood
Fig. 2. Contribution of Food Sources to Calcium Intake In 10-Year-Olds in 1994. Source: The Bogalusa Heart Study.
products daily [119]. Data from the 1994–1996 CSFII showed
that on the average school-aged children were consuming daily
2.0 servings of dairy products, three-fourths of which were
milk (1.5 servings), with cheese providing most of the remaining servings (0.5 servings) [110,115]. On average, children
consumed twice as much low-fat and nonfat milk combined
(0.8 servings) as whole milk (0.4 servings) [110,115]. Less than
half of children 6 to 11 years of age (47% males, 36% females)
consumed the recommended number of servings of dairy foods/
day [110,115]. Among adolescents 12 to 19 years of age, only
28% of males and 11% of females consumed the recommended
number of servings/day of dairy foods [110,115].
Dennison et al. [120] reported that 75% of children drank
whole milk. The use of whole milk was associated with
younger child age, Black race or Hispanic ethnicity. Dairy
intake was found higher in whites than in Blacks [53], and
whites tended to consume more reduced-fat dairy products than
Blacks.
Children’s consumption of regular and diet soda and fruitflavored drinks is high. On average, children consume nearly as
much soda as they do milk on a given day [110,115]. The mean
number of servings of regular and diet soda equals that for all
servings of fruit consumed for the day, while the mean number
of servings of soda and fruit drinks is more than half that for
total servings of fruit consumed [110,115].
Tracking of Calcium Intake and Dairy Product
Consumption
Epidemiologic studies show that chronic diseases have their
origin during infancy and childhood and progress into adulthood [121–130]. Accordingly, the adoption of healthier eating
lifestyles in early childhood may help prevent development of
chronic diseases later in life. Previous studies of dietary tracking or consistency of diet have focused primarily on nutrients
344
[122–126], food preferences [127] and more recently on intakes
of fruit and vegetables and sugary foods [128]. There is an
indication that consistency occurs in the diets of children [129],
but intake may vary depending on the selected nutrient or food
groups consumed [129].
It is well known that the transition from childhood to young
adulthood consists of great behavioral and physiological
changes [128,130]. For example, during childhood, eating patterns are greatly influenced by participation in school meals
and parental control of foods served in the home. As children
age, they become increasingly autonomous; there are decreased
family influences on dietary habits, and children become increasingly reliant on fast-food sources [131,132]. One could
reasonably hypothesize that with this transition from childhood
to young adulthood, eating behaviors may change, resulting in
inconsistent eating patterns across the age periods. In contrast,
another hypothesis is that since food preferences are formed
early in life [133,134] and food preferences predict food consumption [135,136], then the food consumption patterns in
childhood would be similar to those of young adulthood.
One study showed that there were age differences in dairy
product consumption patterns. Mean consumption of milk decreased, as children became young adults, while consumption
of sweetened beverages and cheese increased [129]. Only 42%
and 8% of the children who consumed milk or cheese, respectively, at age 10 consumed the same dairy products when they
were young adults, based on one 24-hour dietary recall at each
age period. When milk and cheese were combined into one
dairy products group, only 62% of the children who consumed
a dairy food/beverage at age 10 consumed the same dairy
products when they were young adults.
Tracking of calcium intake and dairy product consumption
has been reported in a number of studies [137,138]. In a cohort
of 106 one-year-old children who were followed for 15 years,
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Calcium and Health from Childhood through Adulthood
there was significant tracking of calcium intake (r ⫽ 0.50 –
0.62) at various age intervals (p ⬍ 0.001) [137]. In another
study of adolescents who were followed over a 15-year period
[128], the degree of tracking for calcium intake was much
lower (r ⫽ 0.43 males, 0.38 females). Thirty-three percent of
males and females originally in the lowest quartile for calcium
intake remained in the lowest quartile, and 41% of the subjects
that began in the highest quartile remained in the highest
quartile for calcium intake. Tracking coefficients for intake of
cheese, milk, and milk products ranged from 0.22 to 0.54
depending on age. In the Bogalusa Heart Study, the correlation
coefficients were even smaller for intakes of calcium (0.14),
cheese (⫺0.003), milk (0.11) and total dairy (0.21) from childhood to young adulthood (data not shown). These very low
correlations reflect the large number of children and young
adults who did not consume dairy products in a 24-hour period.
Based on data from the Bogalusa Heart Study, a dramatic
shift occurred in dietary quality from childhood to young
adulthood [129]. Despite the increase in total gram amount of
food consumed in a 24-hour period, the total gram amount of
low-quality foods (i.e., fats/oils, candy, desserts, sweetened
beverages, salty snacks) consumed increased twofold from
childhood to young adulthood, with a 10% decrease in the total
gram amount of high-quality foods (i.e., meats, fruits, vegetables, dairy, breads/grains) consumed. It was surprising to find
that out of the total gram amount of food consumed in young
adulthood, approximately 50% reflected low-quality foods and
50% high-quality foods. These data showed that children’s
dietary quality decreased when they became young adults.
To assess adherence to the Food Guide Pyramid, one study
[129] looked at the percentage of individuals who consumed at
least one food from the five high-quality food groups during
childhood and young adulthood [129]. At age 10, only 50% of
the children consumed a food from each of the five high-quality
food groups; this decreased to only 19% by young adulthood.
Although the data reflected one 24-hour dietary recall at each
time period, it indicated that an alarming percentage of individuals were not consuming a food from each of the five
high-quality food groups [129] on a daily basis in both childhood and young adulthood. The food groups that were not
being consumed in childhood were fruit/fruit juices or vegetables; in young adulthood, the food groups missing were fruit/
fruit juices or dairy. There were strikingly high percentages of
individuals who consumed a food item from at least three of the
low-quality food groups (representing the apex of the Food
Guide Pyramid) in childhood (92%) and young adulthood
(67%).
These results have important implications for intervention
research targeting children and young adults. Results suggest
that efforts are needed to promote daily consumption of foods
from the major high-quality food groups in the Food Guide
Pyramid for a healthy eating pattern in an attempt to prevent or
delay the onset of chronic diet-related diseases later in life.
Moreover, consuming foods from the low-quality foods in
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION
moderation, coupled with increased consumption of fruits, vegetables and dairy, may be one approach to meeting the Food
Guide Pyramid recommendations.
Impact of School Meals on Calcium Intake and
Dairy Product Consumption: National School Meals
Programs
As early as 1972, it was reported [139] that school lunches
provided significantly more protein, calcium, vitamin A, thiamin, riboflavin, niacin and ascorbic acid than bag lunches
brought from home. These results were later confirmed in 1995
[140] and 2001 [115] showing that students consuming school
lunches had higher intakes of vitamin A, riboflavin, vitamin
B-12, calcium, magnesium, phosphorus, and zinc compared to
non-participants [115,141]. The nutrient density of vitamin D,
vitamin B12 and calcium in NSLP lunches was relatively high
[115,141]. National School Lunch Program (NSLP) participation was associated with an increase in the percentage meeting
the calcium standard (54%) compared to nonparticipants (42%)
[115]. NSLP participants consumed substantially more fluid
milk, meats, grain-based mixtures containing meat or cheese,
and vegetables at lunch than nonparticipants. NSLP participants consumed significantly larger amounts of whole milk and
low fat milk [115]. This, together with higher intake of unspecified types of milk, resulted in much higher overall mean milk
consumption specifically, four times as large as that of nonparticipants (0.8 servings versus 0.2 servings). The higher consumption of fluid milk by NSLP participants resulted in higher
lunchtime intakes of vitamin A, calcium, and magnesium [141].
On average, participants consumed larger amounts of cheese
(0.3 servings) than nonparticipants (0.2 servings). For overall
dairy consumption at lunch meals, participants consumed more
servings (1.1 servings) than nonparticipants [115] (0.4 servings). It appeared that the nonparticipants were more likely to
consume soda (0.4 servings) and/or fruit drinks (0.3 servings)
in greater quantities than the participants (0.2 and 0.1 servings,
respectively). These significant differences in calcium intake
and dairy product consumption based on NSLP participation
were similar to those found in overall 24-hour intake [115].
Students who participated in the School Breakfast Program
(SBP) had higher intakes of food energy, protein, thiamin,
riboflavin, calcium, phosphorus and magnesium than individuals who did not [140]. SBP participants consumed 100% of
the calcium AI and 152% of the phosphorus RDA compared to
83% and 132%, respectively, for nonparticipants. SBP participants obtained more calcium and magnesium at breakfast than
nonparticipants, largely because they drank more milk
[115,141]. At breakfast, participants’ mean milk intake was 1.0
servings compared to 0.6 servings among nonparticipants. This
difference in milk consumption was due primarily to a difference in the consumption of low-fat milk. Thus, the higher milk
intake of SBP participants did not result in significantly higher
fat intake among the group. Similar findings were observed in
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Calcium and Health from Childhood through Adulthood
overall 24-hour dietary intake of calcium and dairy products
[115].
For those individuals who participated both in the SBP and
NSLP, the differences in calcium intake were striking. Mean
calcium intake among participants in both meal programs was
75% of the AI compared to 37% among nonparticipants. For
overall 24-hour dietary intake of calcium, participants met
109% of the AI compared to 73% among nonparticipants.
Participants consumed 1.9 servings of milk from the two
meals compared with 0.7 servings among nonparticipants. Instead of milk, nonparticipants consumed more soda and fruit
drinks for breakfast and lunch (average of 0.9 servings for
nonparticipants versus 0.2 servings for participants). For total
amount of dairy products consumed, participants consumed 2.2
servings compared to 0.9 servings for nonparticipants. Similar
differences were observed in overall 24-hour dietary intake of
dairy products.
Concerns Related to Calcium-Fortified Food and
Beverages
Fortification of foods has contributed substantially to nutrient intakes [151–160] and reduced risk for disease and nutrient
deficiencies [53,161,162]. Calcium-fortified foods can be a
reasonable option to help some high-risk people increase their
low calcium intakes [161]. However, it is generally agreed that
choosing calcium-fortified foods, particularly at the expense of
foods naturally containing calcium, is not the best way to meet
calcium recommendations. Several concerns have been raised
regarding the use of calcium-fortified foods and beverages
[52,163]. These concerns are valid ones and center on the risk
of calcium excess [52,160], unknown calcium bioavailability
[163–165] and the potentially negative effects of excessively
high calcium diets on other nutrients such as trace minerals
[53,164,166]. Substitution of calcium-fortified orange juice,
calcium-fortified breakfast cereal and calcium-fortified mineral
water for their traditional counterparts doubled calcium intake
[52]. Thus, calcium intake above the upper limit of 2500 mg
could result if calcium-fortified foods are added to a diet
already containing calcium dense foods [160]. Calcium bioavailability from calcium-fortified foods may vary, depending
on the food [167]. In a study of 16 healthy men, the calcium
from soy beverages was absorbed at only 75% the efficiency of
calcium from cow’s milk [168]; thus, more servings of nondairy foods high in calcium or fortified with calcium may be
needed to meet calcium recommendations. For example, one
would need to consume eight cups of spinach, nearly five cups
of red beans or 21⁄2 cups of broccoli to obtain the same amount
of calcium absorbed from one cup of milk [164,165]. Additionally, phytic acid can significantly reduce calcium bioavailability in calcium-fortified breads and cereals [164,165]. There
is some concern that fortifying foods with large quantities of
calcium, especially over the long term, may adversely affect the
utilization of iron, zinc and magnesium [53,164]. The nutrient
346
profile of calcium-fortified foods compared to milk can vary
considerably [169]. For example, the amount of phosphorus in
eight ounces of 2% milk meets 23% RDI compared to ⬍5%
RDI for eight ounces of calcium-enriched orange juice or one
slice of calcium-enriched bread. Similar variations are found in
the amount of magnesium (8% DRI), vitamin A (14% DRI),
vitamin B (25% DRI) and riboflavin (24% DRI) in 2% milk
compared to calcium-enriched orange juice (7%, 5%, 0%, 4%
DRI, respectively) and calcium-enriched bread (2%, 0%, 0%,
6% DRI, respectively). Consumption of milk and other dairy
products appear to be an excellent way, not only to achieve
more calcium, but to reap the benefits of the other nutrients
they provide compared to calcium-fortified products. With
regard to low-nutrient-dense foods, the FDA discourages fortification of those foods because of the risk that consumers
consuming such fortified products will ignore the rest of their
diet, resulting in nutrient deficiencies and imbalances [170].
Factors Influencing Children’s Milk Drinking
Behavior
Availability of Competitive Foods. In addition to the
school breakfast and lunch programs, many schools also offer
foods and beverages a la carte during breakfast or lunch, and
in after-school programs, school stores or snack bars, vending
machines, and concession stands. Students at nearly all senior
high schools, most middle/junior high schools, and more than
one-fourth of elementary schools have access to foods and
beverages at school through vending machines [171–173].
More than 40% of elementary schools allowed students to
purchase food and beverages through either vending machines
or a school store, canteen or snack bar [171]. Eighty-seven
percent of high schools had vending machines and almost
one-third had a school store [171]. The majority of the vending
machines in high schools offered juice drinks, carbonated beverages and foods of minimal nutritional value [171]. Only 6%
of the vending machines offered a milk beverage [171]. Items
sold in school stores were snacks of low nutrient density and
high in fat and sodium, and drinks that were high in energy and
added sugars [174]. Forty percent of beverages consumed by
students consisted of soft drinks [171,172,174]. Furthermore,
nearly half of the school stores were open during lunch hours,
competing with the school lunch program [172]. More than
two-thirds (68.4%) of schools allowed students to buy soft
drinks, sport drinks or fruit drinks that were not 100% juice
during the lunch period [171], thereby providing an obvious
disincentive for consuming milk provided by the school lunch
program. About half of all districts and schools had contracts
that allowed companies to sell soft drinks at schools [175].
In addition to the SBP and NSLP, many schools offered
foods and beverages a la carte [176,177]. Ninety-six percent of
55 schools surveyed had an a la carte line [171]. Foods in a la
carte menus varied greatly in their nutritional value, ranging
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from extra servings of reimbursable meal components to highenergy, high fat choices [176,177]. One study showed that 24%
of the a la carte food items in junior and senior high schools
were snacks, 16% were nondairy drink items, 13% were dessert
items and 12% were entrée items [176]. Sales data indicated
that, on the average, 34% of the students purchased one or more
a la carte food items daily [176]. Although more than threefourths of the schools sold milk, the best-selling a la carte
beverages were fruit juice and juice drinks [176]. School Nutrition Dietary Assessment Study II (SNDA II) found that
weekly a la carte revenue was inversely related to overall
NSLP participation, while another study found an inverse association between soft drink consumption and milk/fruit juice
consumption [173].
There has been a movement to eliminate competitive foods
in schools [178], to create national policies [178] and/or develop nutrient standards for competitive foods [175]. Although
these efforts appear reasonable, there is a concern among the
public and scientific communities that limiting food options in
schools to only those that reflect healthy eating recommendations or some nutrient standards may not be the most practical
solution. Moreover, based on food preference studies, it has
been shown that restricting children’s access to foods will in
fact increase children’s preference and consumption of those
restricted foods when they become available [179,180], so
restricting the availability of less nutrient-dense foods may not
result in an increased consumption of more nutrient-dense
foods.
Eating away from Home. Over the past decade, there has
been an increased popularity of eating meals/snacks away from
home [181]. The greater numbers of meals/snacks consumed
away from home (excluding school meals) have adversely
affected the nutritional quality of the diet [181]. Away-fromhome foods/beverages consumed by children were higher in fat
and saturated fat, and lower in fiber and calcium [181]. Calcium density in home foods showed a general upward trend
from 1977 to 1995, while in away-from-home foods, calcium
density declined slightly [181]. The calcium density of school
foods has always been considerably higher, from 1977 to 1995,
than that of restaurant or fast foods, or even home foods [181].
In one study of adolescents in grades 7 and 10, students said
that they rarely ordered milk when eating at fast-food establishments because milk was unavailable, not promoted or not as
visible as other beverage options such as soft drinks [182].
Encouraging children to improve their away-from-home food
choices and to eat more meals at home may increase their
intake of dairy foods and improve the overall nutritional adequacy of their diets [183].
Concern about Body Weight. There is a misperception
that milk and other dairy foods are fattening, which can lead
children, particularly adolescent females, to limit their intake of
dairy foods and calcium in an attempt to lose and/or maintain
weight [182,184,185]. Frequent dieting was associated with
inadequate consumption of dairy products among both males
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION
and females [182], with a high percentage of chronic dieters
reporting inadequate intake. This association is of concern,
given the high prevalence of low consumption of dairy products and high prevalence of dieting among adolescent females
[182]. Studies in children and adolescents demonstrate that
dairy foods can be consumed without increasing body weight
or fat mass [184,186]. Moreover, it has been observed that
higher dairy consumption is associated with a reduced risk of
being overweight or obese [8,33,35–37,54,79]. More studies
are needed to better understand the associations among dieting,
calcium intake and dairy product consumption.
Nutritional Concerns with Reduced Fat Foods. Studies
have shown that individuals who consumed less energy from
fat had lower intakes of total energy, saturated fat, cholesterol
and several micronutrients [187–190]. In contrast, others have
shown that the vitamin and mineral content of the diet can
potentially be improved when fat is reduced in the diet [191–
193]. One study showed that the total fat intake of skim and
low-fat milk drinkers was significantly lower than that of whole
milk drinkers; males but not females compensated for energy
by increasing carbohydrate intake, and reduced-fat-milk drinkers consumed more fruit and vegetables and less meat and
sweets than whole milk drinkers [194]. Other studies have
shown that children who reduced their total fat intake consumed fewer dairy foods and had lower calcium intakes than
children with higher fat intakes [195,196]. Contrary to these
findings, dietary calcium intakes can be increased to recommended levels with dairy foods without increasing total energy
or fat intakes [54,186,197]. All types of dairy foods, regardless
of fat content, can be incorporated into a healthy eating pattern
that meets the current recommendations for total fat, specifically saturated fat [54,186].
Lactose Intolerance. It is estimated that 25% of the U.S.
population and 75% of adults worldwide are reported to be
lactose-intolerant. In the United States, the prevalence of lactose intolerance is lowest in Caucasians (15%), and highest in
African-Americans (80%) and Asian-Americans (90%). A
common fear or fallacy perceived by people with lactose intolerance is that they cannot consume dairy products because
they will produce gastrointestinal symptoms [198,199]. As a
result, milk and other dairy foods are often eliminated or
restricted from the diet [200]. One study found that those with
adequate lactase levels absorbed 92% of milk’s lactose while
those with low lactase levels absorbed only 25% to 58%
[198,199].
The majority of the incidence figures for lactose intolerance
represent the proportion of people who are diagnosed with
lactose maldigestion after consuming a challenge dose of lactose in water (50 grams). A much smaller number of people
experience intolerance symptoms when they consumed usual
amounts of milk (12 grams lactose). Current research findings
show that the majority of individuals with low lactase levels
can ingest at least eight ounces of milk with a meal and even 16
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Calcium and Health from Childhood through Adulthood
ounces per day without distress [198–200]. Other studies conclude that most lactose maldigesters can consume small
amounts of lactose as found in four ounces of milk or hard
cheeses and that greater quantities can be tolerated if consumed
with other foods [201–206]. Furthermore, habitually including
milk and other dairy products in the diet can actually improve
one’s tolerance to lactose [198,199]. Colonic adaptation to
daily lactose feeding in lactose maldigesters reduces lactose
intolerance [207]. Considering that lactose intolerance is reportedly high among African-Americans and they have a disproportional higher risk for calcium-related diseases, such as
colon cancer, hypertension and obesity, it appears that AfricanAmericans would greatly benefit from improved intake of
calcium and dairy products [208].
An individual’s tolerance for dairy foods varies by type
[198–200]. Whole milk appears to be better tolerated than
lower-fat milks, chocolate milk better than unflavored milk,
and cheeses and cultured/culture-containing dairy foods better
than milk [198,200]. Calcium intake levels of most Americans
are far below recommended levels [109,110], and lactose intolerant people are at particular risk of low calcium intakes;
dairy products are important sources of calcium. Although
lactose intolerance may partly explain the low calcium intakes
due to reduced dairy product consumption by minority populations [208], culturally determined food preferences and dietary practices learned early in life may also play a role.
Therefore, we need to educate people with lactose intolerance
that dairy products can, in most cases, be gradually added to
their everyday eating lifestyles [209].
Breakfast Consumption. Eating breakfast has a positive
impact on milk intake [115,210]. Eating breakfast increases
calcium intakes [210–214]. In one study, children 6 to 19 years
of age consumed 23% to 30% of their daily calcium intake at
breakfast [110]. Unfortunately, 25% of adolescent girls and
22% of adolescent boys were found to skip breakfast [110].
Ready-to-eat (RTE) cereals have traditionally been considered
breakfast foods. A positive effect of RTE cereal consumption
was the usual (92%) addition of milk [210]. In the Bogalusa
Heart Study [210], 96% of 10-year-old children who consumed
RTE cereals also consumed an item from the milk group,
whereas only 83% of the non-cereal eaters consumed milk. The
difference was more striking in young adults: 74% of those
who ate cereal also consumed a milk product, whereas only
31% of non-cereal-eaters did so.
Another important observation is that the nutrient contribution of the breakfast meal varied by source, (i.e., home compared with school) [213]. The percentage of 10-year-old children not meeting two-thirds of the RDA for calcium was
significantly higher among children consuming a home breakfast compared to children consuming a school breakfast. A
larger percentage of children consumed sweetened beverages at
home for breakfast than those who consumed school breakfast.
Of the children who drank milk for breakfast, whole milk was
348
generally consumed with breakfast at home, versus low-fat
chocolate milk at school.
Parents. Parents, particularly mothers, can influence their
children’s intake of milk by drinking it themselves and by
making it readily available [215]. A recent study of 180 mothers and their five-year-old daughters demonstrated that the
mothers’ own beverage consumption patterns determined the
extent to which their daughters’ intake of milk was displaced
by soft drinks [215]. Mothers, by serving as role models, can
shape their daughters’ beverage choices, calcium intake and
risk for osteoporosis in later life. For both mothers and daughters, intake of soft drinks was negatively associated with both
milk and calcium intake.
Taste. Taste is an important factor influencing children’s
and adolescent’s food choices, including their decision to consume milk [54,182,184]. Milk’s flavor affects children’s milkdrinking behavior. A recent study of elementary school children found that children preferred chocolate milk [215] and
adolescents preferred flavored milk over plain milk [184].
Children who consumed flavored milk had lower intakes of soft
drinks and fruit drinks and higher calcium intakes than children
who did not consume the flavored milk [100].
Lack of Knowledge. Lack of knowledge about how much
calcium is needed and dietary sources of this nutrient is another
factor that can influence children’s consumption of dairy foods
and calcium intake. A survey of 1,117 adolescents found that
those who were knowledgeable about calcium consumed more
of this nutrient than adolescents who were less aware of calcium [216,217]. Only 19% knew how many dairy foods they
should consume, and only 10% knew the calcium content of
various dairy foods, while 45% were knowledgeable about
nondairy sources of calcium [216,217].
Other Factors Related to Milk Consumption by Children. Asian adolescents reported that the important motivators
of consuming calcium-rich foods were parental encouragement,
taste, type of food accompanying the calcium-rich food and the
media [218]. Key barriers were certain locations, cost, hot
weather and inconvenience [218]. Several of these factors
varied in importance by gender and age [218]. Family connectedness, low socioeconomic status and average or below-average school grades were also associated with low consumption
of milk and dairy products [218]. Others [120] have shown that
behavioral modeling of milk consumption and perceptions of
others’ opinions were factors associated with calcium intakes
and dairy product consumption. A recent pilot study found that
some adolescents rarely consumed meals with their families
and that many watched television during meals [219]. Watching television while eating was associated with increased intake
of soft drinks and other foods of low nutritional value [219].
More recently, focus groups were conducted among Asian,
Hispanic and Caucasian preadolescent and adolescent females
in ten states to understand influences on adolescents’ consumption of calcium-rich foods [220]. A barrier to milk consumption
was the limited expectation within families for drinking milk,
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Calcium and Health from Childhood through Adulthood
particularly among older girls and Asians. Little role modeling
by parents was indicated. A large percentage of the participants
indicated that they controlled their own beverage selection at
home, and a variety of beverage options were available. Caucasian girls had the most positive comments relative to the taste
of milk and Hispanic girls had the most negative comments. All
ethnic groups positively associated milk with health, both general and bone specifically. Milk was also associated with breakfast, school lunches, cereal and desserts. Another interesting
finding was that Hispanic girls were more likely to consume
milk in milk shakes, whereas Asian girls liked warm, sweetened milk or in combination with tea.
A national study showed that school milk had some negative physical and imagery characteristics and associations for
many students [221]. Students reported eight key reasons for
not drinking milk which included: (1) they preferred to drink
something else; (2) the milk was sometimes warm or “bad”
(poor product quality); (3) there was an absence of the preferred type of milk (e.g., skim, flavored); (4) insufficient portions were offered; (5) a negative association was made with
school food; (6) the milk was given unattractive and juvenile
packaging; (7) the containers were hard to open/drink from, and
(8) there was a perceived value of “free” milk versus other
beverages costing money. In comparison with soda, students’
image of soda was rated “good” based on being sweet, coming
in a variety of flavors, having bubbles and caffeine, coming in
“neat” packaging and coming in teen-size portions [221]. Based
on these findings, a school milk pilot test was conducted with
roughly 100,000 students from 146 schools in nine states [221].
At a majority of sites, a single new flavor of milk was offered
(e.g., strawberry, vanilla, caramel, orange, mocha, cappuccino
and coffee) free or at a reduced price in addition to white and
chocolate milk on the serving line. The containers were more
attractively packaged (8- or 10-ounce resealable plastic); other
aspects of product quality and presentation were enhanced
including refrigeration, display, freshness and merchandising.
In some test schools where value-added milk products were not
part of the school milk bid program, 16-ounce flavored milk in
plastic resealable bottles were offered as a la carte selections
and/or from vending machines, were physically located in close
proximity to the serving line and were priced competitively
with non-milk beverage selections. Results showed the children
reported the plastic resealable bottle to be more appealing than
the traditional carton and that the container was easier to open
and to drink from. With an improved milk offering at lunch
time, particularly when a third flavor and a 10-ounce serving
was offered, more children bought and drank more milk. Moreover, those students were more likely to take two or more milk
servings. The initial increase in milk consumption continued to
increase throughout the study; resulting in decreased milk
waste. More studies are needed to confirm these findings and to
examine potential impact on average daily participation in
school lunch and dietary intakes of children.
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION
Call For Action
Based on these findings several areas need immediate attention:
1.
2.
3.
4.
5.
6.
7.
8.
9.
Reauthorization of the school meals program.
Increasing or maintaining participation in school meals.
Encouraging breakfast consumption.
Creating “healthy school nutrition environments” [222]
that foster healthy food consumption [175].
Decreasing plate waste of school meals by increasing meal
flexibility, expanding the use of self-service and regulating
options for customizing portion sizes to children’s grade
level, offering a variety of milk options, improving the
quality, appearance and/or acceptability of foods, and
promoting consumption of healthier food choices.
Balancing nutritional and financial considerations with
regard to the sale of competitive foods in schools.
Offering some healthy competitive food options rather than
eliminating less nutrient-dense foods/beverages altogether.
Integrating behavior-focused nutrition education into the
curriculum.
Increasing the public’s knowledge and awareness through
effective media and marketing messages about how much
calcium is needed, as well as dietary sources of calcium.
Future Research Imperatives
1. Determine whether or not high intakes of calcium result
in calcium-mineral interactions that affect the mineral
status of vulnerable populations.
2. Determine the impact of calcium-fortified foods on overall nutritional adequacy of the diet.
3. Determine the impact of competitive foods in schools on
food consumption and dietary intakes.
4. Conduct further studies to determine whether a reduction
in sweetened beverage consumption results in increased
milk consumption.
5. Develop effective behavioral interventions designed to increase calcium intake with milk and other dairy products.
6. Confirm whether there is a positive relationship between
dairy consumption and weight loss, and further validate
the mechanism for this relationship.
ACKNOWLEDGMENTS
The authors wish to thank Pamelia Harris for help in preparing the manuscript, Leslie Loddeke for technical writing
assistance and Su-Jau Yang for statistical analyses of the Bogalusa Heart Study data. We also extend a special thanks to Dr.
Gerald Berenson, Director of the Bogalusa Heart Study, and to
the children and young adults of Bogalusa, without whom this
work could not have been accomplished.
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Received December 12, 2002; revision accepted April 4, 2003.
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