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Review |
National Dairy Council, Rosemont, Illinois (G.D.M., J.K.J.)
Nutrition Consultant, Ann Arbor, Michigan (L.D.M.)
Address reprint requests to: Gregory D. Miller, PhD, FACN, Vice President, Nutrition Research and Technology Transfer, National Dairy Council, 10255 West Higgins, Suite 900, Rosemont, IL 60018-5616. E-mail: gregorymrosedmi.com.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONTHE CALCIUM CRISIS IN...FACTORS INFLUENCING DIETARY...SOURCES OF CALCIUMHEALTH BENEFITS OF CONSUMING...CONCLUSIONREFERENCES |
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Key words: calcium, dairy products, fortified-foods, supplements, calcium deficiency disorders
Key teaching points:
• Calcium has earned the title of "super nutrient" because of its role in reducing the risk for osteoporosis, hypertension and possibly colon cancer, as well as other disorders.
• Food is the first priority in meeting calcium needs.
• Dairy foods are the major source of calcium in the U.S. Because these foods also provide several other essential nutrients, their intake improves the overall nutritional quality of the diet.
• Foods such as some green leafy vegetables provide calcium, but generally in lower amounts per serving than milk and other dairy foods. Also, some components, for example, oxalate in spinach, can reduce calcium’s bioavailability.
• Calcium-fortified foods and calcium supplements can help improve calcium intake, especially for individuals whose intake of foods naturally containing calcium is limited. However, care must be taken to ensure that needs for other essential nutrients provided by foods such as dairy foods are also met.
• Americans’ low calcium intake has reached a crisis level.
• Educational interventions are necessary to help individuals and the general public meet their calcium needs without risk of calcium toxicity or underconsumption of other essential nutrients.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONTHE CALCIUM CRISIS IN...FACTORS INFLUENCING DIETARY...SOURCES OF CALCIUMHEALTH BENEFITS OF CONSUMING...CONCLUSIONREFERENCES |
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There no longer is a question about calcium’s health benefits. The major concern is how best to meet calcium needs. Calcium can be obtained from foods naturally rich in calcium such as dairy foods, from calcium-fortified foods and beverages, from supplements or from a combination of these sources. Health professional organizations as well as medical experts agree that food is the first priority in meeting calcium needs [6,7,8]. This review discusses the calcium crisis, factors influencing dietary calcium consumption, sources of calcium and the health benefits of consuming calcium-rich foods. Lastly, some strategies to help improve Americans’ calcium status are presented.
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THE CALCIUM CRISIS IN AMERICA |
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TOPABSTRACTINTRODUCTIONTHE CALCIUM CRISIS IN...FACTORS INFLUENCING DIETARY...SOURCES OF CALCIUMHEALTH BENEFITS OF CONSUMING...CONCLUSIONREFERENCES |
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Many population groups, particularly adolescent and older females and older adults, consume diets containing significantly less calcium than recommended (Fig. 1). At all ages, males consume more calcium than females, presumably because of their higher energy intake. Data from the Continuing Survey of Food Intakes by Individuals (CSFII) 1994–96 indicate that only 12% of females ages 12 to 19 and 32% of similar aged males are meeting 100% of the AI for calcium [10]. According to this same survey, only 16% of women ages 20 to 29 years, 14% of women ages 30 to 39 years, and 11.5% of women 40 to 49 years are meeting 100% of the AI for calcium [10]. Although less than 15% of older adults are consuming 100% of the calcium AI, more men than women are meeting calcium recommendations. Approximately 15% of males aged 50 to 59, 13% of males aged 60 to 69, and 13% of males over 70 years consume 100% of the calcium recommendations. In contrast, only 5% of women ages 50 to 59, 4% of women aged 60 to 69, and 4% of women ages 70 and older consume 100% of the calcium recommendation [10]. The low dietary calcium intake of adolescents is of particular concern because it coincides with a period of rapid skeletal growth—a "window of opportunity" to maximize peak bone mass and protect against future risk for osteoporosis [12,13,14,15]. About 90% of females’ total body bone mineral content is achieved by age 16.9 years, 95% by age 19.8 years, and 99% by age 26.2 years, depending on the site measured [15]. Consequently, the period for optimizing peak bone mass by calcium rapidly declines after adolescence.
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FACTORS INFLUENCING DIETARY CALCIUM CONSUMPTION |
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TOPABSTRACTINTRODUCTIONTHE CALCIUM CRISIS IN...FACTORS INFLUENCING DIETARY...SOURCES OF CALCIUMHEALTH BENEFITS OF CONSUMING...CONCLUSIONREFERENCES |
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Substitution of Soft Drinks for Milk
The calcium crisis may be attributed, at least in part, to changes in the food consumption pattern of the U.S. population over the past century, in particular the trend toward consuming less milk and more soft drinks [14,16,19,21,22,23]. As shown in Fig. 2, in 1945 Americans consumed more than four times as much milk as carbonated soft drinks. In contrast, in 1998, 2
times more soda than milk was consumed [23]. The recent NIH consensus panel on osteoporosis [21] attributes Americans’ low calcium intake to "restriction of dairy products, a generally low level of fruit and vegetable consumption, and a high intake of low calcium beverages such as sodas."
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Unfortunately, intake of dairy foods is lower than recommended. According to USDA’s Healthy Eating Index, which evaluates the quality of the average U.S. diet, Americans two years of age and over consumed an average of 1.5 servings/day of dairy foods in 1994–1996, instead of the 2 to 3 servings/day recommended by USDA’s Food Guide Pyramid [22,30]. Moreover, fewer people consumed the recommended number of servings of dairy foods in 1996 than in 1989 [22]. In 1996, only 26% of people consumed the recommended number of servings of dairy foods on a given day [22]. Also, intake of milk and other dairy products begins to decrease around the age of 6 to 11 years [10,22,27]. Without liberal intake of dairy products it is difficult to meet calcium needs [4,6,8,13,16].
Substituting soft drinks for milk compromises calcium intake and contributes to adverse health effects [14,29,31,32,33,34]. Nationwide food intake survey data reveal that consumption of soft drinks and other beverages has increased over the past decade for all age groups [35,36]. However, the increase is highest among teenagers and younger adults [16]. A study of adolescent food trends between 1965 and 1996 found that total milk consumption decreased by 36% [14]. This decline in milk consumption was not compensated for by an increase in other dairy products, but rather by soft drinks and noncitrus juices and drinks [14]. When the eating patterns of children were followed from third to eighth grade, researchers at the University of Minnesota found that children’s daily milk consumption decreased from 2.5 times a day in third grade to less than 1.9 times a day in eighth grade [32]. Yet, during this time, consumption of soft drinks more than tripled, most often replacing milk and fruit juice [32]. Data on more than 1,800 children aged 2 to 18 years indicate that children who substitute soft drinks for milk limit their intake of calcium as well as other nutrients such as riboflavin, folate, vitamin A and phosphorus [31]. These findings led the researchers to recommend that "nutrition education messages targeted to children and/or their parents should encourage limited consumption of soft drinks" [31]. Policies to limit children’s access to soft drinks at day care centers and schools should also be implemented [31]. Intake of soft drinks at the expense of calcium-rich beverages such as milk not only compromises calcium intake and increases future risk for osteoporosis, but may also have more immediate adverse consequences [33]. A recent investigation of the relationship between soft drink consumption and fracture risk in 460 ninth and tenth grade students demonstrated that the students who consumed more soft drinks had a higher risk for fractures than those who consumed fewer soft drinks [33].
Eating Away From Home
The growing popularity of eating away from home is a threat to meeting dietary recommendations for nutrients such as calcium [37,38]. Data from USDA’s 1994–96 CSFII [10] indicate that the calcium density of restaurant or fast foods is appreciably lower than that for home foods [37 (Fig. 3)]. For example, in 1995, the calcium density of away from home foods was 343 mg per 1,000 kilocalories, whereas home foods had a calcium density of 425 mg per 1,000 kilocalories. An exception is school foods which provide higher amounts of calcium than foods served elsewhere [37 (Fig. 4))]. In 1995, school foods had a calcium density of 689 mg per 1,000 kilocalories, which is considerably higher than the calcium density of home or away from home foods [37]. This observation is supported by studies demonstrating that participation in school feeding programs such as the National School Lunch Program and the School Breakfast Program increases students’ calcium intake [39,40]. The decreased availability of milk or limited choices of milk, as well as the availability of other beverage options at restaurants and fast food establishments, contributes to the low calcium density of meals served in these establishments [34,41]. According to a recent study of 141 adolescents in grades seven and ten in Minneapolis, students said that they rarely order milk at fast food establishments because milk is not available, not promoted or is not as visible as other beverage options such as soda [42]. The consumption of soda associated with fast food eating displaces some milk in the diet, thereby compromising calcium intake [43]. Consumers may also abandon healthful eating when consuming foods away from home because they view eating out as an opportunity to splurge, regardless of how often it occurs [38].
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Parental and Peer Influence
Parents, and particularly mothers, strongly influence young children’s intake of milk, a major dietary source of calcium, by making it available and by drinking it themselves. One study found that, if mothers drink milk, their daughters are also likely to consume this beverage [44]. Although parents can still influence adolescents’ food choices, as children grow older, peer influence on food choices becomes of greater importance [2]. According to a recent study of factors influencing adolescents’ food choices, the adolescents said that parents influenced their food choices by the food they ate, cooked and purchased, rules regarding eating and meals, overall parent-child relationships and familial cultural and religious practices [42]. The adolescents in the study recommended that parents teach healthful eating habits to children when they are young, but cautioned that forcing children to eat certain foods would backfire, causing children to avoid these foods later on [42]. Similarly, a study of Asian adolescents in Hawaii found that parents and grandparents, by encouraging consumption of milk and preparing calcium-rich foods, can help increase children’s calcium intake [43]. However, if parents do not consume milk themselves, they represent a barrier to their children’s calcium intake [43]. By serving as role models and by teaching children, particularly preschoolers, to consume a healthful diet, parents and other care providers can help children make food decisions consistent with meeting their calcium needs. According to a study examining the nutritional quality of diets of 16,202 children ages 9 to 14, eating meals such as dinner with their family increases children’s calcium intake, [45]. Compared to children who rarely or infrequently ate dinner with their family, children who ate dinner with their family each day had a greater calcium intake and were less likely to consume sodas [45].
A recent study by USDA’s Economic Research Service on the diet quality of children ages 2 to 17 years found that a mother’s influence over her child’s nutrient intake diminishes as the child ages [46]. According to this same study, the more a mother knows about health and nutrition, the better the overall quality of her children’s diet. This relationship was stronger for preschoolers than for older children [46]. Parents generally have less influence on older children’s diets because older children tend to make more dietary decisions independent of the family and they eat away from home more often. The researchers suggest that health and nutrition education addressing young children be targeted toward mothers, but for school-age children it can be targeted directly [46]. Interestingly, the mothers’ knowledge of health and nutrition did not have an appreciable influence on children’s calcium intake in this study [46]. The researchers speculate that the mothers may not consider low calcium intake to be a serious problem for children.
As children reach adolescence, their drives for independence and peer acceptance have an increasingly greater influence on their food choices [2,45,47]. How adolescents view particular foods may influence their intake of nutrients such as calcium [47]. According to a recent study of factors influencing adolescents’ food choices, students said that if you want young people to do something (e.g., drink milk) it must be viewed as "cool" or the "thing to do" [42]. To encourage adolescents to make more healthful food choices, it is important to consider teens’ image of particular foods and present healthful food choices in a context appealing to the teen culture.
Skipping Meals
Skipping meals such as breakfast may limit calcium intake if care is not taken to consume sufficient calcium throughout the rest of the day [48,49]. Researchers have demonstrated that school-age children who skip breakfast consume less milk and compromise their overall diet quality [48].
Knowledge and Attitudes
Knowledge of the relationship between calcium and health, of dietary recommendations for calcium and of personal calcium intake is a first step toward increasing consumption of calcium-rich foods [10,20,34,38,46,50,51,52,53,54]. Nutrition knowledge was positively associated with drinking milk more often, according to a telephone survey of 495 older adults, ages 60 to 94 [54]. In a study involving 472 women aged 50 years and over, those who knew that calcium helps to protect bone health consumed more calcium than women who were unaware of this association [51]. Other investigations indicate that being misinformed or unaware of the health benefits of a calcium-rich diet may contribute to a low intake of this mineral [52,53]. In a study involving older women in New Zealand with low calcium intakes, the women believed that intake of milk or milk products either had no or possibly an adverse effect on health [53]. According to an investigation involving 1,117 adolescents in Rhode Island, those who were knowledgeable about their recommended intake of calcium, the bone health benefits of calcium and the importance of adolescence as a critical time to increase bone mass consumed more calcium than adolescents who were unaware of this information [52]. In this study, only 10% of the adolescents knew the calcium content of various dairy foods, less than half (45%) were aware of nondairy sources of calcium (e.g., vegetables such as broccoli), and only 19% knew how many servings of dairy foods a day are recommended [52].
Although individuals may have knowledge of or be aware of calcium’s protective effect against disease, they may have an erroneous perception of the calcium adequacy of their diets. Many adults overestimate their calcium intake, according to data from USDA’s 1994–96 Diet and Health Knowledge Survey [10]. When adults participating in this survey were questioned regarding whether their diets were too low, too high, or about right in calcium, only 26% of males and 43% of females thought their calcium intake was too low [10]. Yet, about two out of three men and eight out of ten women have diets low in calcium, according to the accompanying CSFII [10]. Interestingly, 26% of males and 20% of females did not consider it to be very important to consume two servings of dairy foods a day [10]. Knowledge may provide consumers with the information to implement a behavior change to improve their calcium status, but it is the individual’s attitude or belief that ultimately determines whether or not he or she is motivated to implement a dietary change [38]. For example, adolescents who believe that they are too young to be worried about their health are unlikely to take steps to improve their calcium status, despite knowledge of calcium’s importance [42]. Also, as discussed in this review, knowledge is only one of several factors shaping dietary behavior.
Weight and Fat Concerns
The misperception that milk and other dairy foods are fattening, along with strong societal pressures to be thin, can lead people, especially adolescent females, to decrease their intake of dairy foods [20,26,27,43,50,53,55,56]. According to a recent study of Asian adolescents in Hawaii, girls were concerned that drinking milk would make them fat [43]. In another investigation involving 91 adolescent females, 25% in the control group and 15% in the dairy supplemented group expressed the view that dairy foods are fattening [56]. Losing weight was given as a reason to consume fewer dairy products. However, no significant differences in total body fat or body weight were found between the two groups [56]. In a study of over 36,000 students in grades 7 through 12, dieting among both males and females was strongly linked to low intake of dairy foods [27].
The AAP, in its recent report on calcium requirements of children, acknowledges that preoccupation with being thin, especially among adolescent females, and the misperception that all dairy foods are fattening, is contributing to low calcium intakes in this age group [20]. The AAP adds that "... many children and adolescents are unaware that low-fat milk contains at least as much calcium as whole milk" [20]. To improve their calcium status, adolescents may need to be reminded that low-fat dairy foods generally contain just as much or slightly more calcium than traditional whole milk [20]. Because low fat diets may compromise calcium intake, researchers recommend that guidance to reduce fat intake be counterbalanced by advice to promote optimal calcium intake [57].
Increasing calcium intake through dairy foods can be accomplished without necessarily increasing calorie or fat intake, body weight, or percent body fat [58,59,60,61,62,63]. A randomized, placebo-controlled intervention study of adults ages 18 to 70 years in Oregon demonstrated that calcium intake could be increased to 1,500 mg/day with dairy foods without weight gain [58]. Recent investigations involving older adults aged 55 to 85 years who were advised to increase their milk intake by three servings per day for 12 weeks using skim or 1% milk found that the small increase in body weight (0.6 kg) was less than predicted [62,63]. The timing of the study (i.e., in the fall and winter months when weight gain often occurs) or a temporary period of adjustment to the additional food may have contributed to the small weight gain [62,63]. Studies in children and adolescents demonstrate that dairy foods can be increased without increasing body weight or dietary fat intake [59,61]. When 9 to 13 year old girls in Utah increased their calcium intake to 1,437 mg per day by consuming additional dairy foods (i.e., milk, yogurt, cheese), there was no increase in weight gain, body fat, or dietary fat intake compared to the girls who followed their usual diets containing 728 mg calcium [59]. Similarly, when 12 year old girls consumed an additional two cups of either whole or lowfat milk a day, there was no increase in weight gain [61]. As discussed below, new research findings indicate that increasing calcium intake, especially from calcium-rich dairy foods, may help to control body fat [3].
Taste
Taste is the primary factor influencing consumers’ food choices [26,38,42,43,56,64,65]. According to the Food Marketing Institute’s annual Trends survey, taste continues to be of greater importance to consumers than nutrition when choosing foods [64]. Consumers who enjoy the taste of calcium-rich foods such as dairy foods are likely to consume these foods more often and consequently have higher calcium intakes [26,43,53,56]. According to a two year study of the effect of calcium intake on adolescent females’ bone health, taste was identified as the primary reason for liking or disliking a dairy product [56]. Similarly, taste was an important factor influencing intake of dairy foods among Asian adolescents in Hawaii [43]. These adolescents said that milk and other calcium-rich foods are best enjoyed when served at the right temperature and with certain "matching" foods [43]. To improve the calcium status of children and adults, it is important to increase their awareness of the wide variety of dairy foods and other calcium sources in the marketplace and provide them with opportunities to taste these foods.
Lactose Intolerance
Some people who avoid milk and other dairy foods because of lactose intolerance (i.e., gastrointestinal symptoms following intake of lactose in those with lactase deficiency) may have low calcium intakes [66,67]. However, accumulating scientific research indicates that many individuals diagnosed with lactose maldigestion because of lactase deficiency can consume recommended intakes of calcium from dairy foods [67,68,69,70,71,72,73]. Studies demonstrate that lactose maldigesters can consume the amount of lactose in one or two servings of milk, especially in divided doses with meals, without developing symptoms [67,68,69,70,71]. A recent investigation of African American adolescent females with lactose maldigestion found that they were able to consume 1,200 mg calcium per day from dairy foods without experiencing symptoms of intolerance [71]. Based on these findings, the researchers concluded that "... lactose maldigestion should not be a restricting factor in developing adequate calcium diets for this population" [71]. They also add that lactose maldigestion does not result in lactose intolerance when this population consumes a dairy-rich diet [71].
In addition to consuming milk in small amounts with meals, lactose maldigesters can comfortably tolerate other calcium-rich dairy foods such as aged cheeses (e.g., Cheddar, Colby, Swiss, Parmesan), yogurt with active cultures and lactose-reduced or lactose-free milks and other dairy products [67,71,72,73]. Also, gradually increasing intake of lactose-containing foods actually improves tolerance to lactose [67,71]. Increasing intake of calcium-containing nondairy products, such as some vegetables, may help lactose maldigesters meet their calcium needs [20]. Individuals with lactose maldigestion or intolerance need to understand that dairy foods, the major source of calcium in the diet, need not be eliminated from their diet [73].
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SOURCES OF CALCIUM |
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TOPABSTRACTINTRODUCTIONTHE CALCIUM CRISIS IN...FACTORS INFLUENCING DIETARY...SOURCES OF CALCIUMHEALTH BENEFITS OF CONSUMING...CONCLUSIONREFERENCES |
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Other federal government agencies recommend foods as the first priority in meeting calcium needs. According to the NICHD [17], "low-fat milk or low-fat milk products are the best sources of calcium because they contain large amounts of calcium along with additional nutrients to help the body better absorb calcium. They also are already a part of the diet of most Americans. Along with calcium, milk provides other essential nutrients, including vitamin D, potassium, and magnesium, all essential for optimal bone health and human development." The NICHD has undertaken an educational effort called "Milk Matters" to increase calcium awareness of pediatricians and other healthcare professionals, as well as children, adolescents and their parents. To help children and adolescents meet their calcium needs, the "Milk Matters" program encourages this population to drink three to four servings of milk throughout the day [17].
The NAS, in its dietary recommendations for calcium and related nutrients, recognizes the importance of "unfortified foodstuffs" as the major source of calcium [4]. The NAS explains that meeting calcium needs through foods offers such advantages as providing intakes of other beneficial nutrients and unidentified food components and possibly enhancing the body’s use of nutrients through nutrient interactions [4]. The 2000 Dietary Guidelines for Americans, issued by the USDA and United States Department of Health and Human Services (USDHHS), identifies dairy foods such as yogurt, milk and cheeses as major sources of calcium and cautions the American public to "... not let soft drinks or other sweets crowd out other foods you need to maintain health, such as low-fat milk or other food sources of calcium" [74].
The USDHHS’ Healthy People 2010 also recognizes dietary sources of calcium such as milk and milk products, canned fish with soft bones such as sardines, dark green leafy vegetables such as kale, mustard and turnip greens, tofu made with calcium, tortillas made from lime-processed corn and calcium fortified foods and beverages [19]. This report states that "with current food selection practices, use of dairy products may constitute the difference between getting enough calcium in one’s diet or not" [19].
Several health professional organizations recommend food as the preferred source of calcium. The American Dietetic Association (ADA) recognizes that intake of a wide variety of foods is preferable to supplements to meet needs for nutrients such as calcium [75]. A recent position statement on women’s health and nutrition issued by ADA and Dietitians of Canada states that "... inclusion of low-fat dairy products in the diet is the most desirable way to meet calcium goals" [76]. The American Medical Association [7] concurs, stating that "... the preferred source of calcium is through calcium-rich foods such as dairy products."
The AAP, Committee on Nutrition, in a recent policy statement on calcium requirements of infants, children and adolescents, encourages pediatricians to recommend milk, cheese, yogurt and other calcium-rich foods for children’s daily diet [20]. The AAP recommends that physicians ask children what type of milk (white or chocolate) they drink with meals and if they consume cheese, yogurt, broccoli, tofu and/or other sources of calcium [20]. To meet calcium needs, the National Osteoporosis Foundation states that "increasing dietary calcium is the first-line approach, but calcium supplements should be used when an adequate dietary intake cannot be achieved" [77]. The Osteoporosis Society of Canada also agrees that food is the best source of calcium [78].
Numerous nutrition and medical experts recommend foods as the best source of calcium for health [8,60,62,79,80,81]. Recommended calcium intakes can easily be met from food sources [8]. As stated in a recent review by Robert P. Heaney, M.D., "While it is possible to arrange an adequate diet using available Western foods, it is usually difficult to do so without including dairy products. Few individuals succeed, and, in general, a diet low in dairy foods means a diet that is poor in several respects beyond insufficiency of calcium. Additionally, in the industrialized nations with a dairy industry, milk is almost always less expensive per calorie than the average of all foods in the diet. Thus a high dairy food intake is cost-efficient as well as cost-effective" [82]. This medical researcher recommends that dietitians and other healthcare professionals encourage their clients to meet calcium recommendations through increased intake of low fat dairy products [62].
Dairy Foods as a Source of Calcium
Milk and other dairy foods are the major source of calcium in the U.S., providing 72% of the calcium available in the food supply [24 (Table 1)]. Few other foods provide calcium naturally in such concentrated amounts as in milk. Also, some food sources such as some vegetables contain phytates and oxalates, which can reduce the intestinal absorption of calcium [83,84]. Without consuming dairy products, it is difficult to meet dietary calcium recommendations [6,7,13,25,26,27,34]. In an analysis of food sources of calcium, milk and milk products provided 83% of the calcium in the diets of young children, 77% of the calcium in adolescent females’ diets, and between 65% and 72% of the calcium in adults’ diets [25]. In another study involving approximately 800 high school students, milk and other dairy foods provided 79% of their calcium intake [26]. Similar findings are reported for adults [34]. A study of over 2,000 women who participated in USDA’s 1990–91 CSFII found that women whose diets met recommendations for calcium intake consumed more servings of milk and milk products [34]. These women also had higher intakes of several essential nutrients when compared to women whose diets did not meet their calcium needs [34].
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Because milk and other dairy foods are excellent sources of calcium as well as many other essential nutrients (Table 1), their intake improves the overall nutritional quality of the diet [25,34,58,60,62,82,85]. A longitudinal study involving 64 postmenopausal women in Australia found that the women who were randomly assigned to receive 1,000 mg of additional calcium per day by consuming fat free milk powder increased not only their calcium intake, but also their intake of other essential nutrients such as protein, potassium, phosphorus, magnesium, riboflavin, thiamin and zinc [60]. In contrast, the women who took calcium supplements (calcium lactate gluconate) increased only their intake of calcium and sodium [60]. Although both milk powder and calcium supplements increased calcium intake, consuming the fat free skim milk powder improved the women’s total diet as well.
Other studies involving women support these findings [34,63,85]. A recent randomized open trial at six medical centers across the country found that increasing milk intake improved the overall nutritional quality of older adults’ diets [63]. This study involved healthy women and men aged 55 to 85 years who consumed 1.5 servings or fewer of dairy products per day. The study participants, who were advised to increase their fluid milk intake (fat free or 1%) by three eight-ounce servings/day for 12 weeks, significantly increased their intake of not only calcium, but of other nutrients such as protein, vitamins A, D, and B12, riboflavin, phosphorus, magnesium, zinc and potassium as well (Fig. 5). The greatest improvements were observed for calcium and vitamin D [63]. Increasing milk intake also reduced the prevalence of dietary shortcomings for a number of nutrients. The findings led the researchers to conclude that "older adults can successfully increase milk intake, thereby meaningfully improving their nutrient intake" [63]. Similarly among children and adolescents, consumption of milk has been demonstrated to increase both calcium intake and improve the overall nutrient adequacy of their diet [25,29]. When children included milk as part of their noon meal, intake of calcium as well as other "problem" nutrients such as vitamin A, vitamin E and zinc also increased [29]. Clearly, if milk and other dairy foods are not consumed in recommended amounts, calcium and other nutrients usually supplied by dairy foods may be deficient. Diets low in calcium are generally low in other essential nutrients as well and are a marker for overall poor diet quality [58,59,85]. Thus, improving dietary patterns is likely to be the best solution to increasing calcium intake.
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cups of broccoli to obtain the same amount of calcium absorbed from one cup of milk [84 (Table 2)]. Components in foods such as phytates in unleavened bread, seeds, nuts and most cereals and oxalates in spinach, rhubarb, sweet potatoes and walnuts can form insoluble complexes with calcium, reducing its bioavailability [83,84]. In general, the absorption of calcium from a food is inversely associated with its oxalic acid content [84]. For example, the bioavailability of calcium from high oxalate foods such as spinach and rhubarb is low, whereas calcium bioavailability is relatively high from low oxalate vegetables such as kale, broccoli and bok choy [84]. Most forms of fiber, especially at usual intakes of 5 to 15 g/day, have little or no effect on calcium absorption [4,6,87]. Likewise, protein and phosphorus intake do not affect fractional calcium absorption, according to a recent longitudinal study [88].
Calcium-Fortified Foods
For individuals who limit or avoid foods naturally rich in calcium, such as milk and other dairy foods, calcium-fortified foods and/or calcium supplements can be consumed to help achieve adequate calcium intakes [5,84]. However, use of calcium-fortified foods and calcium supplements does not solve the underlying problem of inadequate dietary patterns of food selection, which account for Americans’ generally low calcium intakes [1]. It is important for individuals who choose to meet their calcium needs through calcium-fortified foods and/or supplements to ensure that their needs for other nutrients supplied by foods, such as dairy foods, are also met. Calcium-fortified foods and calcium supplements are a supplement to, not a substitute for, foods naturally containing calcium.
Consumers’ enthusiasm to maintain or improve their health through diet has created a so-called food "fortification frenzy" [89]. Between 1997 and 1999, the percentage of consumers including fortified foods in their diet increased by 10% [89]. The highest users of fortified foods are the "Generation Xers" (20 to 30 year olds), followed by "Baby Boomers" (68%) and the more "Mature" (60%) [89]. This trend in use of fortified foods is exemplified by the increasing availability of calcium-fortified foods [90,91]. In 1999, 234 calcium-fortified foods and beverages were introduced, or nearly four times more than in 1995, according to the new products database, Productscan Online [90]. Orange juice, juice drinks, cereal, rice, pasta, pancake and waffle mixes, energy bars, snack foods, margarine, chocolate and caramel chews, soy beverages, dairy products and even bottled water are among the foods and beverages currently fortified with calcium.
The increased availability and use of calcium-fortified foods raises several concerns, including the potential for calcium toxicity, lower calcium absorbability than expected and inadequate intakes of other essential nutrients. Currently, the amount of calcium consumed from calcium-fortified foods is unknown. In 1997, the NAS set 2,500 mg calcium per day as the Tolerable Upper Limit for calcium [4]. Calcium intakes in excess of this amount can potentially increase risk for milk-alkali syndrome (i.e., a condition of hypercalcemia and renal insufficiency), aggravate kidney stone formation in stone-formers who hyperabsorb calcium from the intestine and inhibit the body’s absorption of iron and zinc [4]. The plethora of calcium-fortified foods and beverages in the marketplace, especially of products fortified with high levels of calcium, has caused some people to question whether calcium fortification has gone too far [92,93,94]. Although frank calcium toxicity is rare, excessive use of calcium-fortified foods, especially by individuals who are already meeting their calcium needs, is a possibility [4,93,94]. To avoid calcium toxicity, calcium should be added to fortified foods in small amounts [92]. Also, individuals should base their decision on whether or not to use calcium-fortified foods or supplements on their current dietary calcium intake, which can be assessed by examining the Nutrition Facts labels on foods and beverages. The NAS, recognizing the increase in calcium-fortified foods in the marketplace, states that "... it is important to maintain surveillance of the calcium-fortified products in the marketplace and monitor their impact on calcium intake" [4].
The bioavailability of calcium from calcium-fortified food products is another consideration. A variety of calcium salts are used to fortify foods and beverages [84]. Although the bioavailability of calcium from various salts is similar to that from milk [83], the bioavailability of calcium from calcium-fortified foods may differ from that expected. A recent study found that calcium-fortified soy beverage is not comparable to cow’s milk as a source of calcium [95]. Unlike cow’s milk, soy beverages naturally contain very little calcium (i.e., about 10 mg per serving). As such, manufacturers often fortify soy beverages with calcium, although the amount is not regulated and levels can vary from 80 mg calcium to 500 mg calcium per serving [95]. When the bioavailability of calcium in fortified soy beverage was compared to that of calcium in cow’s milk in 16 healthy men, the calcium from the soy beverage was absorbed at only 75% the efficiency of calcium from cow’s milk [95]. Soy manufacturers can add enough calcium to achieve a comparable absorption level as cow’s milk, but most brands do not [95]. According to this study, 60% more calcium (i.e., 500 mg per serving) is needed in soy beverages to have comparable absorption to cow’s milk (i.e., 300 mg per serving) [95].
Although calcium-fortified foods provide calcium, they usually are not nutritionally equivalent to dairy foods [92,95]. For example, calcium-fortified soy beverages do not have the same nutrient profile as cow’s milk [95]. Individuals using calcium-fortified foods, particularly low nutrient foods, as a replacement for dairy foods, may miss out on dairy’s other nutrients such as vitamin D (if fortified), potassium, and riboflavin. Also, use of calcium-fortified foods may give people a false sense of security that their nutrient needs are being adequately met or that they can disregard the rest of their diet [93]. Calcium-fortified foods can be used to enhance calcium intake, especially for individuals whose intake of dairy foods is limited. However, the public needs to be educated about the use of calcium-fortified foods to avoid excess intake of calcium and underconsumption of other nutrients essential for health.
Calcium Supplements
Although all individuals should be encouraged to meet their calcium needs with dietary sources whenever possible, calcium supplements may be needed by some individuals who restrict or eliminate dairy foods from their diets [16,31,96]. Some questions to raise when considering calcium supplementation include the following. Are calcium supplements necessary? If so, which calcium supplement is best for a particular individual? Other considerations include the elemental calcium content, absorption, the dose and timing, potential side effects, such as interactions with other nutrients and medications, and compliance.
Calcium in supplements is found in various forms including calcium carbonate (e.g, in antacids), citrate, citrate malate, phosphate, gluconate, lactate, and calcium from dolomite (calcium magnesium carbonate) or bone meal [96,97]. The percentage of elemental calcium provided by these different sources of calcium ranges from as high as 40% from calcium carbonate to as low as 9% from calcium gluconate [96]. Supplement labels often indicate the percentage of elemental calcium provided. In addition to the amount (dosage) of calcium in various supplements, the absorption of calcium is a consideration. In general, the absorption of calcium from milk and various salts is similar [83]. Although small differences in calcium absorption from various salts such as calcium carbonate and calcium citrate malate have been observed, findings are inconsistent and likely explained by differences in methods used to measure calcium absorption, among other factors [98,99,100,101]. Cost is a factor in choosing a calcium supplement. Because calcium carbonate contains the highest percentage of calcium, it often is the least expensive. Some calcium supplements may also contain vitamin D, which helps the body absorb calcium [96,97]. Calcium supplements containing vitamin D may be especially beneficial for homebound, institutionalized older adults who lack exposure to sunlight [96]. For most individuals, intake of vitamin D in amounts of 400 to 600 IU/day is sufficient to meet needs [4]. However, because vitamin D is harmful in high doses (i.e., 2,000 IU/day), excessive intake of this vitamin should be avoided [4].
In terms of dosage and timing, calcium is best absorbed in doses of 500 mg or less, taken according to manufacturer’s instructions [81,96,97]. Individuals requiring more than 500 mg of elemental calcium from supplements should take the supplements in multiple doses for efficient utilization. Taking calcium carbonate with meals improves calcium absorption [81]. This is especially true for individuals with decreased gastric acid production. Other supplements such as calcium citrate malate, which is readily absorbed regardless of stomach acid, need not be taken with meals [81,96,97].
Use of calcium supplements may contribute to potential side effects including constipation and bloating, as well as nutrient imbalances [4,94,96]. Calcium can interact with other minerals such as iron and zinc, but evidence to date fails to demonstrate that excess intake of calcium contributes to deficiencies of these minerals in humans, especially over the long-term and when their intake is adequate [4,97,102,103,104]. Nevertheless, medical experts recommend that calcium supplements not be consumed at the same time as iron supplements or iron-rich meals [96]. Although detectable levels of lead have been found in some calcium supplements, particularly from natural sources [105], calcium supplements make only a small contribution to total daily lead intake [106]. Further, the presence of calcium reduces lead absorption [106]. Also, in recent years the supplement industry has taken measures to reduce the lead content of calcium supplements [106].
Because calcium supplements can diminish the effectiveness of some medications such as Fosamax, used to treat osteoporosis, or the antibiotic Tetracycline, calcium supplements should not be consumed at the same time as these medications [97]. Individuals should talk to their physician or pharmacist regarding drug-nutrient interactions. Similar to calcium-fortified foods, calcium supplements may increase the risk of kidney stones in individuals with a history of this disorder [96]. Calcium supplements are not recommended for individuals with absorptive or renal hypercalciuria, primary hyperparathyroidism or sarcoidosis [96]. When choosing a calcium supplement, check the label for the USP (US Pharmacopeia) designation which signifies that the calcium supplement meets voluntary standards for quality (i.e., purity, composition) [75].
Compliance, or the likelihood that use of calcium supplements will be maintained, is another factor to consider when making the decision to use calcium supplements [20]. Also, if calcium supplements are substituted for calcium-rich foods such as dairy products to meet calcium needs, attention needs to be given to other nutrients provided by foods. As discussed above, using calcium supplements to meet calcium needs increases the intake of calcium but few, if any, other nutrients [60].
Educational interventions are needed to help individuals best meet their calcium needs. Although dietary supplements may help increase calcium intake, their use may not be sufficient to meet recommendations for calcium. A recent study of 423 adolescents found that, regardless of calcium supplement use, a significant number of the adolescents had low intakes of calcium as well as other nutrients [107]. The researchers recommend that efforts to improve adolescents’ calcium intake focus on encouraging them to consume more calcium-rich foods such as low fat dairy products, fortified whole grains and cereals, fruits and vegetables [107]. Consumers also need to be convinced that meeting calcium needs can be accomplished by consuming foods naturally containing this mineral. According to an investigation exploring motivations for using vitamin and mineral supplements, about half of the calcium users reported consuming a nutritionally balanced diet, but they believed that optimal intake of nutrients such as calcium could not be obtained from food alone [108].
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HEALTH BENEFITS OF CONSUMING CALCIUM-RICH FOODS |
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• Osteoporosis
Accumulating scientific evidence indicates that consuming an adequate intake of calcium or calcium-rich foods such as milk and other dairy foods throughout life helps to optimize peak bone mass achieved by age 30 or earlier, slow age-related bone loss and reduce osteoporotic fracture risk in later adult years [2,4,6,7,21]. A recent analysis of 139 papers relating to calcium intake and bone health published since 1975 provides convincing evidence of the beneficial role of calcium and calcium-rich foods in skeletal health [82]. In 50 of the 52 investigator-controlled, calcium intervention trials, increasing calcium intake positively affected bone gain during growth, reduced bone loss in later years or lowered fracture risk [82]. The six studies that used dairy sources of calcium were all positive [82]. Similar beneficial effects of calcium were demonstrated in approximately three-quarters of 86 observational studies, most of which used food sources of calcium [82]. Recognizing the beneficial effects of dairy foods on bone health and their overall nutrient contribution to the diet, the researchers concluded that "a high dairy-food intake is cost-efficient as well as cost-effective" [82].
• Hypertension
Substantial scientific evidence supports a beneficial role for calcium or calcium-rich dairy foods in blood pressure regulation [2,109,110,111,112,113,114]. In 1997, the landmark government-sponsored DASH (Dietary Approaches to Stop Hypertension) study revealed that intake of a low fat diet containing almost three servings of dairy foods (predominately low fat milk) in combination with fruits and vegetables significantly and quickly (within two weeks) reduced blood pressure in persons with high normal blood pressure [109,110]. Systolic and diastolic blood pressures were reduced by 5.5 mm Hg and 3.0 mm Hg, respectively, in adults who consumed the DASH diet compared to the control group. In hypertensive participants, the blood pressure lowering effects of the DASH diet were even greater, evidenced by reductions of 11.4 mm Hg in systolic and 5.5 mm Hg in diastolic pressure compared to the control diet [109,110]. Researchers estimate that if Americans follow the DASH diet, coronary heart disease and stroke could be reduced by 15% and 27%, respectively [109]. As reviewed by Miller et al. [114], since publication of the DASH diet, several health professional organizations have issued support for the DASH diet to reduce the risk for or treat hypertension.
• Colon Cancer
Several different types of studies support a beneficial role for calcium against colon cancer [2,115,116,117,118]. In an investigation of 70 patients with a history of developing polyps or noncancerous growths in the colon, increasing food sources of calcium, specifically low fat dairy foods, reduced the risk for colon cancer [117]. The study participants were divided into two groups, one of which maintained its baseline diet and the other which increased its dietary calcium intake to about 1,500 mg/day, mostly from dairy foods. Compared to the control group, significant reductions in cell proliferation and in two markers of cell differentiation occurred in the group consuming additional dairy foods [117]. A randomized, double-blind trial of 930 adults with a recent history of colorectal adenomas found that increasing calcium intake by 1,200 mg/day reduced the incidence of recurrent adenomatous polyps by 19% and the total number of tumors by 24% in less than one year [118]. Whether similar beneficial effects on the recurrence of colonic adenomatous polyps would be found following intake of food sources of calcium such as dairy products is unknown.
• Stroke
Calcium intake, particularly from dairy foods, may potentially reduce the risk for stroke, the third leading cause of death worldwide [119,120]. Calcium intake was inversely associated with the incidence of stroke in nearly 86,000 middle-aged women who participated in the Nurses’ Health Study [119]. This inverse association was stronger for dairy calcium (i.e., calcium from milk, yogurt, hard cheese, ice cream) than for nondairy calcium or calcium supplements [119]. These findings support earlier observations linking milk intake to a lower risk for stroke [120]. Additional investigations, including clinical trials, are needed to substantiate these observational findings.
• Kidney Stones
Although calcium restriction was once recommended to treat patients with kidney stones, new research indicates that this approach may actually increase the risk for kidney stones [121]. Two prospective observational studies have demonstrated that increasing dietary calcium intake, particularly from dairy foods, reduces the incidence of kidney stones in adult males and females [122,123]. In both of these studies, food sources of calcium such as skim and lowfat milk were protective against kidney stones, whereas calcium supplements increased the risk for kidney stones [122,123]. A high calcium intake is thought to reduce kidney stone risk by forming an insoluble calcium-oxalate complex, thereby decreasing the intestinal absorption and excretion of oxalate found in foods such as vegetables, beans and whole grains [124,125]. The researchers speculate that calcium supplements may increase kidney stone risk because they tend to be taken between meals when there would be little or no opportunity to bind with oxalate in the intestine. Increasing dietary calcium, especially from dairy foods, offers to be a promising strategy to reduce the risk for kidney stones. However, clinical trials are needed to demonstrate the effectiveness of this approach [121].
• Weight Control
Calcium, and particularly dairy foods, may play a beneficial role in controlling body fat and reducing the risk for obesity [3]. When transgenic mice expressing the agouti gene in adipocytes were fed diets varying in the amount and source (i.e., calcium carbonate or nonfat dry milk) of calcium for six weeks, the high calcium diets reduced weight gain and fat pad mass by 26% to 39% [3]. Also, in the mice fed the high calcium diets the expression and activity of adipocyte fatty acid synthase, as well as stimulation of lipolysis, were reduced by 3.4- to 5.2-fold. In this study, calcium in the form of dairy foods (i.e., nonfat dry milk) reduced the animals’ fat deposition more than did elemental calcium [3].
To determine whether these findings in experimental animals apply to humans, the researchers examined epidemiological data from NHANES III [3]. An inverse association was found between calcium intake and body fat, particularly for women, after controlling for energy intake, physical activity, age, and other variables. Additional study is necessary to confirm these findings, particularly the potential advantage of dairy foods in controlling body fat.
• Other Disorders
Potential beneficial roles for calcium in other disorders such as premenstrual syndrome [126,127], polycystic ovarian syndrome [128], lead intoxication [129] and periodontal disease [130] have been demonstrated. Most of these studies used calcium supplements. However, because dairy foods are a major source of calcium in the diet, it is expected that these food sources of calcium also confer beneficial effects in the above disorders.
• Health-Promoting Components
Meeting calcium needs through foods can increase intake of newly identified components with potential health benefits. These components, as well as others yet to be discovered in foods, are not present in calcium supplements. Dairy foods not only are a major source of calcium, but these foods also contain a number of health-promoting components including conjugated linoleic acid (CLA) and sphingolipids in milk fat and bacterial cultures such as Lactobacillus acidophilus in cultured dairy products such as yogurt.
CLA, a derivative of the fatty acid linoleic acid, may have a number of potential health benefits, including inhibition of certain cancers (e.g., skin, stomach, mammary gland, colon), retardation and regression of atherosclerosis, modulation of certain aspects of the immune function, changes in body fat metabolism and partitioning, anti-diabetic effects and enhancement of bone formation [131,132,133,134]. Sphingolipids, particularly sphingomyelin, may help to lower blood cholesterol levels and reduce the risk for certain cancers [135,136]. Evidence for these potential health benefits of CLA and sphingolipids is based primarily on in vitro and experimental animal studies.
Lactic acid bacteria in cultured (e.g., yogurt, buttermilk) or culture-containing (e.g., unfermented or sweet acidophilus milk) foods have been reported to improve lactose digestion, inhibit pathogenic organisms in the intestine which cause diarrhea and other intestinal disorders, restore a normal intestinal microflora, protect against cancer and modestly lower elevated blood cholesterol levels [137,138,139,140].
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CONCLUSION |
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TOPABSTRACTINTRODUCTIONTHE CALCIUM CRISIS IN...FACTORS INFLUENCING DIETARY...SOURCES OF CALCIUMHEALTH BENEFITS OF CONSUMING...CONCLUSIONREFERENCES |
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Calcium-fortified foods and calcium supplements are an option for individuals who cannot meet their calcium needs from foods naturally containing this mineral. However, their use does not correct the poor dietary patterns of food selection which are the underlying cause of Americans’ low calcium consumption. Also, intake of calcium-fortified foods and calcium supplements may increase the risk for calcium toxicity, especially among individuals who already meet their calcium needs from foods naturally containing this mineral.
Considering calcium’s expanding beneficial roles in health, optimizing calcium intake, without risk of calcium toxicity or underconsumption of other essential nutrients, is of critical importance. Americans’ generally low calcium intake calls for educational interventions to help close the calcium gap between actual and recommended intakes. A first step toward developing effective educational strategies is to understand factors impacting dietary calcium consumption. Substituting soft drinks for milk, eating away from home, lack of support from parents and/or peers, skipping meals, inadequate knowledge regarding calcium and health, concerns about fat intake and body weight, taste preferences and lactose intolerance can compromise calcium intake.
Nutrition education strategies to increase calcium intake should use different approaches tailored to specific concerns and/or population groups based on age, among other factors. For adolescents and young adults who are high consumers of soft drinks, interventions should aim to make calcium-rich beverages such as milk "cool" or appealing to this population. Also, limiting soft drinks and making dairy foods such as a variety of milks more accessible, especially in schools, restaurants and fast food establishments, may help increase calcium intake. For older adults who are concerned about their health and, in particular, their risk for chronic diseases such as osteoporosis and hypertension, different educational approaches to improve calcium intake are warranted. For example, a recent study of postmenopausal women found that osteoporosis education and bone mineral density testing improved their self-reported lifestyle behaviors, including increasing intake of milk [141]. For children or adults who are concerned about body weight, educational strategies should increase awareness that lowfat dairy products generally contain at least as much calcium as their traditional counterparts. Further, meeting calcium needs with foods such as dairy foods can be accomplished without increasing fat intake or body weight [58,59,60,61,62,63] and may aid weight loss [3].
Optimizing Americans’ calcium intake is a challenge, one recognized by the Calcium Summit [18]. The American public needs to understand why it is important to meet calcium needs and why consuming foods containing calcium is the foremost and best way to accomplish this objective. Participants at the Calcium Summit identified several strategies to increase the American public’s intake of calcium-rich foods. These include the need to
Clearly, nutrition and other health professional organizations need to assume an advocacy role to improve Americans’ calcium status. In particular, efforts must be made to correct dietary misinformation being proliferated via the internet and readily communicated through the media. Much of the vocal opposition to the consensus that calcium is important throughout life has an ideological, not a scientific, origin [142]. A priority for health professional organizations is to work to ensure that scientifically sound information is being communicated to the general public.
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