Introduction

Calcium, the most abundant mineral in the body, is found in some foods, added to others, available as a dietary supplement, and present in some medicines (such as antacids). Calcium is required for vascular contraction and vasodilation, muscle function, nerve transmission, intracellular signaling and hormonal secretion, though less than 1% of total body calcium is needed to support these critical metabolic functions [1]. Serum calcium is very tightly regulated and does not fluctuate with changes in dietary intakes; the body uses bone tissue as a reservoir for, and source of calcium, to maintain constant concentrations of calcium in blood, muscle, and intercellular fluids [1].

The remaining 99% of the body's calcium supply is stored in the bones and teeth where it supports their structure and function [1]. Bone itself undergoes continuous remodeling, with constant resorption and deposition of calcium into new bone. The balance between bone resorption and deposition changes with age. Bone formation exceeds resorption in periods of growth in children and adolescents, whereas in early and middle adulthood both processes are relatively equal. In aging adults, particularly among postmenopausal women, bone breakdown exceeds formation, resulting in bone loss that increases the risk of osteoporosis over time [1].

Recommended Intakes

Intake recommendations for calcium and other nutrients are provided in the Dietary Reference Intakes (DRIs) developed by the Food and Nutrition Board (FNB) at the Institute of Medicine of the National Academies (formerly National Academy of Sciences) [1]. DRI is the general term for a set of reference values used for planning and assessing the nutrient intakes of healthy people. These values, which vary by age and gender, include:

• Recommended Dietary Allowance (RDA): average daily level of intake sufficient to meet the nutrient requirements of nearly all (97%–98%) healthy individuals.
• Adequate Intake (AI): established when evidence is insufficient to develop an RDA and is set at a level assumed to ensure nutritional adequacy.
• Estimated Average Requirement (EAR): average daily level of intake estimated to meet the requirements of 50% of healthy individuals. It is usually used to assess the adequacy of nutrient intakes in populations but not individuals.
• Tolerable Upper Intake Level (UL): maximum daily intake unlikely to cause adverse health effects [1].

The FNB established RDAs for the amounts of calcium required for bone health and to maintain adequate rates of calcium retention in healthy people. They are listed in Table 1 in milligrams (mg) per day.

* Adequate Intake (AI)

Sources of Calcium

Food
Milk, yogurt, and cheese are rich natural sources of calcium and are the major food contributors of this nutrient to people in the United States [1]. Nondairy sources include vegetables, such as Chinese cabbage, kale, and broccoli. Spinach provides calcium, but its bioavailability is poor. Most grains do not have high amounts of calcium unless they are fortified; however, they contribute calcium to the diet because they contain small amounts of calcium and people consume them frequently. Foods fortified with calcium include many fruit juices and drinks, tofu, and cereals. Selected food sources of calcium are listed in Table 2.

* DV = Daily Value. DVs were developed by the U.S. Food and Drug Administration to help consumers compare the nutrient contents among products within the context of a total daily diet. The DV for calcium is 1,000 mg for adults and children aged 4 years and older. Foods providing 20% of more of the DV are considered to be high sources of a nutrient, but foods providing lower percentages of the DV also contribute to a healthful diet. The U.S. Department of Agriculture's Nutrient Database Web site lists the nutrient content of many foods. It also provides acomprehensive list of foods containing calcium.
** Calcium content varies slightly by fat content; the more fat, the less calcium the food contains.
*** Calcium content is for tofu processed with a calcium salt. Tofu processed with other salts does not provide significant amounts of calcium.

In its food guidance system, MyPlate, the U.S. Department of Agriculture recommends that persons aged 9 years and older eat 3 cups of foods from the milk group per day [3]. A cup is equal to 1 cup (8 ounces) of milk, 1 cup of yogurt, 1.5 ounces of natural cheese (such as Cheddar), or 2 ounces of processed cheese (such as American).

Dietary supplements
The two main forms of calcium in supplements are carbonate and citrate. Calcium carbonate is more commonly available and is both inexpensive and convenient. Due to its dependence on stomach acid for absorption, calcium carbonate is absorbed most efficiently when taken with food, whereas calcium citrate is absorbed equally well when taken with or without food [4]. Calcium citrate is also useful for people with achlorhydria, inflammatory bowel disease, or absorption disorders [1]. Other calcium forms in supplements or fortified foods include gluconate, lactate, and phosphate. Calcium citrate malate is a well-absorbed form of calcium found in some fortified juices [5].

Calcium supplements contain varying amounts of elemental calcium. For example, calcium carbonate is 40% calcium by weight, whereas calcium citrate is 21% calcium. Fortunately, elemental calcium is listed in the Supplement Facts panel, so consumers do not need to calculate the amount of calcium supplied by various forms of calcium supplements.

The percentage of calcium absorbed depends on the total amount of elemental calcium consumed at one time; as the amount increases, the percentage absorption decreases. Absorption is highest in doses ≤500 mg [1]. So, for example, one who takes 1,000 mg/day of calcium from supplements might split the dose and take 500 mg at two separate times during the day.

Some individuals who take calcium supplements might experience gastrointestinal side effects including gas, bloating, constipation, or a combination of these symptoms. Calcium carbonate appears to cause more of these side effects than calcium citrate [1], so consideration of the form of calcium supplement is warranted if these side effects are reported. Other strategies to alleviate symptoms include spreading out the calcium dose throughout the day and/or taking the supplement with meals.

Medicines
Because of its ability to neutralize stomach acid, calcium carbonate is found in some over-the-counter antacid products, such as Tums® and Rolaids®. Depending on its strength, each chewable pill or softchew provides 200 to 400 mg of elemental calcium. As noted above, calcium carbonate is an acceptable form of supplemental calcium, especially for individuals who have normal levels of stomach acid.

Calcium Intakes and Status

In the United States, estimated calcium intakes from both food and dietary supplements are provided by the National Health and Nutrition Examination Survey (NHANES), 2003–2006 [6]. Mean dietary calcium intakes for males aged 1 year and older ranged from 871 to 1,266 mg/day depending on life stage group; for females the range was 748 to 968 mg/day. Groups with mean intakes falling below their respective EAR—and thus with a prevalence of inadequacy in excess of 50%—include boys and girls aged 9–13 years, girls aged 14–18 years, women aged 51–70 years, and both men and women older than 70 years [1,6]. Overall, females are less likely than males to get adequate amounts of calcium from food [7].

About 43% of the U.S. population (including almost 70% of older women) uses dietary supplements containing calcium, increasing calcium intakes by about 330 mg/day among supplement users [1,6]. According to NHANES 2003–2006 data, mean total calcium intakes from foods and supplements ranged from 918 to 1,296 mg/day for people aged 1 year and older [6]. When considering total calcium intakes, calcium inadequacy remains a concern for several age groups. These include females aged 4 years and older—particularly adolescent girls—and males aged 9 to 18 years and older than 51 years [1,8]. At the other end of the spectrum, some older women likely exceed the UL when calcium intakes from both food and supplements are included [1].

Not all calcium consumed is actually absorbed in the gut. Humans absorb about 30% of the calcium in foods, but this varies depending upon the type of food consumed [1]. Other factors also affect calcium absorption including the following:

• Amount consumed: the efficiency of absorption decreases as calcium intake increases [1].
• Age and life stage: net calcium absorption is as high as 60% in infants and young children, who need substantial amounts of the mineral to build bone [1,9]. Absorption decreases to 15%–20% in adulthood (though it is increased during pregnancy) and continues to decrease as people age; compared with younger adults, recommended calcium intakes are higher for females older than 50 years and for both males and females older than 70 years [1,9,10].
• Vitamin D intake: this nutrient, obtained from food and produced by skin when exposed to sunlight of sufficient intensity, improves calcium absorption [1].
• Other components in food: phytic acid and oxalic acid, found naturally in some plants, bind to calcium and can inhibit its absorption. Foods with high levels of oxalic acid include spinach, collard greens, sweet potatoes, rhubarb, and beans. Among the foods high in phytic acid are fiber-containing whole-grain products and wheat bran, beans, seeds, nuts, and soy isolates [1]. The extent to which these compounds affect calcium absorption varies. Research shows, for example, that eating spinach and milk at the same time reduces absorption of the calcium in milk [11]. In contrast, wheat products (with the exception of wheat bran) do not appear to lower calcium absorption [12]. For people who eat a variety of foods, these interactions probably have little or no nutritional consequence and, furthermore, are accounted for in the overall calcium DRIs, which factor in differences in absorption of calcium in mixed diets.

Some absorbed calcium is eliminated from the body in urine, feces, and sweat. This amount is affected by such factors as the following:

• Sodium and protein intakes: high sodium intake increases urinary calcium excretion [13,14]. High protein intake also increases calcium excretion and was therefore thought to negatively affect calcium status [13,14]. However, more recent research suggests that high protein intake also increases intestinal calcium absorption, effectively offsetting its effect on calcium excretion, so whole body calcium retention remains unchanged [15].
• Caffeine intake: this stimulant in coffee and tea can modestly increase calcium excretion and reduce absorption [16]. One cup of regular brewed coffee, for example, causes a loss of only 2–3 mg of calcium [14]. Moderate caffeine consumption (1 cup of coffee or 2 cups of tea per day) in young women has no negative effects on bone [17].
• Alcohol intake: alcohol intake can affect calcium status by reducing its absorption [18] and by inhibiting enzymes in the liver that help convert vitamin D to its active form [19]. However, the amount of alcohol required to affect calcium status and whether moderate alcohol consumption is helpful or harmful to bone is unknown.
• Phosphorus intake: the effect of this mineral on calcium excretion is minimal. Several observational studies suggest that consumption of carbonated soft drinks with high levels of phosphate is associated with reduced bone mass and increased fracture risk. However, the effect is probably due to replacing milk with soda rather than the phosphorus itself [20,21].
• Fruit and vegetable intakes: metabolic acids produced by diets high in protein and cereal grains increase calcium excretion [22]. Fruits and vegetables, when metabolized, shift the acid/base balance of the body towards the alkaline by producing bicarbonate, which reduces calcium excretion. However, it is unclear if consuming more fruits and vegetables affects bone mineral density. These foods, in addition to reducing calcium excretion, could possibly reduce calcium absorption from the gut and therefore have no net effect on calcium balance.

Calcium Deficiency

Inadequate intakes of dietary calcium from food and supplements produce no obvious symptoms in the short term. Circulating blood levels of calcium are tightly regulated. Hypocalcemia results primarily from medical problems or treatments, including renal failure, surgical removal of the stomach, and use of certain medications (such as diuretics). Symptoms of hypocalcemia include numbness and tingling in the fingers, muscle cramps, convulsions, lethargy, poor appetite, and abnormal heart rhythms [23]. If left untreated, calcium deficiency leads to death.

Over the long term, inadequate calcium intake causes osteopenia which if untreated can lead to osteoporosis. The risk of bone fractures also increases, especially in older individuals [1]. Calcium deficiency can also cause rickets, though it is more commonly associated with vitamin D deficiency [1].

Groups at Risk of Calcium Inadequacy

Although frank calcium deficiency is uncommon, dietary intakes of the nutrient below recommended levels might have negative health consequences over the long term. The following groups are among those most likely to need extra calcium.

Postmenopausal women
Menopause leads to bone loss because decreases in estrogen production both increase bone resorption and decrease calcium absorption [10,24,25]. Annual decreases in bone mass of 3%–5% per year frequently occur in the first years of menopause, but the decreases are typically less than 1% per year after age 65 [26]. Increased calcium intakes during menopause do not completely offset this bone loss [27,28]. Hormone replacement therapy (HRT) with estrogen and progesterone helps increase calcium levels and prevent osteoporosis and fractures. Estrogen therapy restores postmenopausal bone remodeling to the same levels as at premenopause, leading to lower rates of bone loss [24], perhaps in part by increasing calcium absorption in the gut. Several medical groups and professional societies support the use of HRT as an option for women who are at increased risk of osteoporosis or fractures [29-31]. Such women should discuss this matter with their health care providers. In addition, consuming adequate amounts of calcium in the diet might help slow the rate of bone loss in all women.

Amenorrheic women and the female athlete triad
Amenorrhea, the condition in which menstrual periods stop or fail to initiate in women of childbearing age, results from reduced circulating estrogen levels that, in turn, have a negative effect on calcium balance. Amenorrheic women with anorexia nervosa have decreased calcium absorption and higher urinary calcium excretion rates, as well as a lower rate of bone formation than healthy women [32]. The "female athlete triad" refers to the combination of disordered eating, amenorrhea, and osteoporosis. Exercise-induced amenorrhea generally results in decreased bone mass [33,34]. In female athletes and active women in the military, low bone-mineral density, menstrual irregularities, certain dietary patterns, and a history of prior stress fractures are associated with an increased risk of future stress fractures [35,36]. Such women should be advised to consume adequate amounts of calcium and vitamin D. Supplements of these nutrients have been shown to reduce the risk of stress fractures in female Navy recruits during basic training [37].

Individuals with lactose intolerance or cow's milk allergy
Lactose intolerance refers to symptoms (such as bloating, flatulence, and diarrhea) that occur when one consumes more lactose, the naturally occurring sugar in milk, than the enzyme lactase produced by the small intestine can hydrolyze into its component monosaccharides, glucose and galactose [38]. The symptoms vary, depending on the amount of lactose consumed, history of consumption of lactose-containing foods, and type of meal. Although the prevalence of lactose intolerance is difficult to discern [39], some reports suggest that approximately 25% of U.S. adults have a limited ability to digest lactose, including 85% of Asians, 50% of African Americans, and 10% of Caucasians [36,40,41].

Lactose-intolerant individuals are at risk of calcium inadequacy if they avoid dairy products [1,38,39]. Research suggests that most people with lactose intolerance can consume up to 12 grams of lactose, such as that present in 8 ounces of milk, with minimal or no symptoms, especially if consumed with other foods; larger amounts can frequently be consumed if spread over the day and eaten with other foods [1,38,39]. Other options to reduce symptoms include eating low-lactose dairy products including aged cheeses (such as Cheddar and Swiss), yogurt, or lactose-reduced or lactose-free milk [1,38,39]. Some studies have examined whether it is possible to induce adaptation by consuming incremental lactose loads over a period of time [42,43], but the evidence in support of this strategy is inconsistent [38].

Cow's milk allergy is less common than lactose intolerance, affecting 0.6% to 0.9% of the population [44]. People with this condition are unable to consume any products containing cow's milk proteins and are therefore at higher risk of obtaining insufficient calcium.

To ensure adequate calcium intakes, lactose-intolerant individuals and those with cow's milk allergy can choose nondairy food sources of the nutrient (such as kale, bok choy, Chinese cabbage, broccoli, collards and fortified foods) or take a calcium supplement.

Vegetarians
Vegetarians might absorb less calcium than omnivores because they consume more plant products containing oxalic and phytic acids [1]. Lacto-ovo vegetarians (who consume eggs and dairy) and nonvegetarians have similar calcium intakes [45,46]. However, vegans, who eat no animal products and ovo-vegetarians (who eat eggs but no dairy products), might not obtain sufficient calcium because of their avoidance of dairy foods [47,48]. In the Oxford cohort of the European Prospective Investigation into Cancer and Nutrition, bone fracture risk was similar in meat eaters, fish eaters and vegetarians, but higher in vegans, likely due to their lower mean calcium intake [49]. It is difficult to assess the impact of vegetarian diets on calcium status because of the wide variety of eating practices and thus should be considered on a case by case basis.

Calcium and Health

Many claims are made about calcium's potential benefits in health promotion and disease prevention and treatment. This section focuses on several areas in which calcium is or might be involved: bone health and osteoporosis; cardiovascular disease; blood pressure regulation and hypertension; cancers of the colon, rectum, and prostate; kidney stones; and weight management.

Bone health and osteoporosis
Bones increase in size and mass during periods of growth in childhood and adolescence, reaching peak bone mass around age 30. The greater the peak bone mass, the longer one can delay serious bone loss with increasing age. Everyone should therefore consume adequate amounts of calcium and vitamin D throughout childhood, adolescence, and early adulthood. Osteoporosis, a disorder characterized by porous and fragile bones, is a serious public health problem for more than 10 million U.S. adults, 80% of whom are women. (Another 34 million have osteopenia, or low bone mass, which precedes osteoporosis.) Osteoporosis is most associated with fractures of the hip, vertebrae, wrist, pelvis, ribs, and other bones [50]. An estimated 1.5 million fractures occur each year in the United States due to osteoporosis [51]. Supplementation with calcium plus vitamin D has been shown to be effective in reducing fractures and falls (which can cause fractures) in institutionalized older adults [1,52].

When calcium intake is low or ingested calcium is poorly absorbed, bone breakdown occurs as the body uses its stored calcium to maintain normal biological functions. Bone loss also occurs as part of the normal aging process, particularly in postmenopausal women due to decreased amounts of estrogen. Many factors increase the risk of developing osteoporosis, including being female, thin, inactive, or of advanced age; smoking cigarettes; drinking excessive amounts of alcohol; and having a family history of osteoporosis [53].

Various bone mineral density (BMD) tests are available. The T-score from these tests compares an individual's BMD to an optimal BMD (that of a healthy 30-year old adult). A T-score of -1.0 or above indicates normal bone density, -1.0 to -2.5 indicates low bone mass (osteopenia), and lower than -2.5 indicates osteoporosis [54]. Although osteoporosis affects individuals of all races, ethnicities, and both genders, women are at highest risk because their skeletons are smaller than those of men and because of the accelerated bone loss that accompanies menopause. Regular exercise and adequate intakes of calcium and vitamin D are critical to the development and maintenance of healthy bones throughout the life cycle. Both weight-bearing exercises (such as walking, running, and activities where one's feet leave and hit the ground and work against gravity) and resistance exercises (such as calisthenics and that involve weights) support bone health.

In 1993, the U.S. Food and Drug Administration authorized a health claim related to calcium and osteoporosis for foods and supplements [55]. In January 2010, this health claim was expanded to include vitamin D. Model health claims include the following: "Adequate calcium throughout life, as part of a well-balanced diet, may reduce the risk of osteoporosis" and "Adequate calcium and vitamin D as part of a healthful diet, along with physical activity, may reduce the risk of osteoporosis in later life" [55].

Cancer of the colon and rectum
Data from observational and experimental studies on the potential role of calcium in preventing colorectal cancer, though somewhat inconsistent, are highly suggestive of a protective effect [1]. Several studies have found that higher intakes of calcium from foods (low-fat dairy sources) and/or supplements are associated with a decreased risk of colon cancer [56-59]. In a follow-up study to the Calcium Polyp Prevention Study, supplementation with calcium carbonate led to reductions in the risk of adenoma (a nonmalignant tumor) in the colon, a precursor to cancer [60,61], even as long as 5 years after the subjects stopped taking the supplement [62]. In two large prospective epidemiological trials, men and women who consumed 700–800 mg per day of calcium had a 40%–50% lower risk of developing left-side colon cancer [63]. But other observational studies have found the associations to be inconclusive [59,64,65].

In the Women's Health Initiative, a clinical trial involving 36,282 postmenopausal women, daily supplementation with 1,000 mg of calcium and 400 International Units (IU) of vitamin D3 for 7 years produced no significant differences in the risk of invasive colorectal cancer compared to placebo [66]. The authors of a Cochrane systematic review concluded that calcium supplementation might moderately help prevent colorectal adenomas, but there is not enough evidence to recommend routine use of calcium supplements to prevent colorectal cancer [67]. Given the long latency period for colon cancer development, long-term studies are needed to fully understand whether calcium intakes affect colorectal cancer risk. Continue here