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TABLE 1 Dietary Reference Intakes for Calcium by Life Stage Group DRI values (mg/day) AIa ULb Life stage groupc NDd 0 through 6 mo 210 7 through 12 mo 270 ND 1 through 3 y 500 2,500 4 through 8 y 800 2,500 9 through 13 y 1,300 2,500 14 through 18 y 1,300 2,500 19 through 30 y 1,000 2,500 31 through 50 y 1,000 2,500 51 through 70 y 1,200 2,500 > 70 y 1,200 2,500 Pregnancy £ 18 y 1,300 2,500 19 through 50 y 1,000 2,500 Lactation £ 18 y 1,300 2,500 19 through 50 y 1,000 2,500 a AI = Adequate Intake. b UL = Tolerable Upper Intake Level. Unless otherwise specified, the UL represents total intake from food, water, and supplements. c All groups except Pregnancy and Lactation represent males and females. d ND = Not determinable. This value is not determinable due to the lack of data of adverse effects in this age group and concern regarding the lack of ability to handle excess amounts. Source of intake should only be from food to prevent high levels of intake.

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PART III: CALCIUM 287 CALCIUM C alcium plays a key role in bone health. In fact, more than 99 percent of total body calcium is found in the bones and teeth. Calcium is also involved in vascular, neuromuscular, and glandular functions in the body. Since data were inadequate to determine an Estimated Average Require- ment (EAR) and thus calculate a Recommended Dietary Allowance (RDA) for calcium, an Adequate Intake (AI) was instead developed. The AIs for calcium are based on desirable rates of calcium retention (as determined from balance studies), factorial estimates of requirements, and limited data on changes in bone mineral density (BMD) and bone mineral content (BMC). The Tolerable Upper Intake Level (UL) is based on milk-alkali syndrome as the critical end- point. DRI values are listed by life stage group in Table 1. Foods rich in calcium include milk, yogurt, cheese, calcium-set tofu, calcium-fortified orange juice, Chinese cabbage, kale, and broccoli. Calcium may be poorly absorbed from foods that are rich in oxalic acid or phytic acid. The effects of calcium deficiency include osteopenia, osteoporosis, and an in- creased risk of bone fractures. The effects of excess intake include kidney stones, hypercalcemia with renal insufficiency, and a decreased absorption of certain minerals. CALCIUM AND THE BODY Function Calcium’s primary role in the body is to form the structure of bones and teeth. More than 99 percent of total body calcium is stored in the skeleton, where it exists primarily in the form of hydroxyapatite. The remainder is found in the blood, extracellular fluid, muscle, and other tissues, where it is involved in vascular contraction and vasodilation, muscle contraction, neural transmission, and glandular secretion. Absorption, Metabolism, Storage, and Excretion Calcium is absorbed by active transport and passive diffusion across the intesti- nal mucosa. Active transport of calcium into the intestine requires the active form of vitamin D (1,25-dihydroxyvitamin D) and accounts for most of the

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DRIs: THE ESSENTIAL GUIDE TO NUTRIENT REQUIREMENTS 288 absorption of calcium at low and moderate intake levels, as well as at times of great need, such as growth, pregnancy, or lactation. Passive diffusion becomes more important at high calcium intakes. As calcium intake decreases, the efficiency of calcium absorption increases (and vice versa). However, this increased efficiency of calcium absorption, or fractional calcium absorption, is generally not sufficient to offset the loss of absorbed calcium that occurs with a decrease in dietary calcium intake. Cal- cium absorption declines with aging in both men and women. Calcium is ex- creted in the urine and feces. DETERMINING DRIS Determining Requirements There is no biochemical assay that reflects calcium nutritional status. Except in extreme circumstances, such as severe malnutrition or hyperparathyroidism, circulating levels of blood calcium can actually be normal during chronic cal- cium deficiency because calcium is resorbed from the skeleton to maintain a normal circulating concentration. Since data were inadequate to determine an EAR and thus calculate an RDA for calcium, an AI was instead developed. There- fore, the adult AIs for calcium are based on desirable rates of calcium retention (as determined from balance studies), factorial estimates of requirements, and limited data on changes in bone mineral density (BMD) and bone mineral con- tent (BMC). These indicators were chosen as reasonable surrogate markers to reflect changes in skeletal calcium content and, therefore, calcium retention. The AI represents the approximate calcium intake that appears sufficient to maintain calcium nutriture, while recognizing that lower intakes may be adequate for some. However, this evaluation must await additional studies on calcium balance over broad ranges of intakes or long-term measures of calcium sufficiency, or both. During pregnancy, the maternal skeleton is not used as a reserve for fetal calcium needs. Calcium-regulating hormones adjust maternal calcium absorp- tion efficiency so that the AI does not have to be increased during pregnancy. Although increased dietary calcium intake will not prevent the loss of calcium from the maternal skeleton during lactation, the calcium that is lost appears to be regained following weaning. Thus, the AI for calcium in lactating women is the same as that of nonlactating women.

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PART III: CALCIUM 289 Criteria for Determining Calcium Requirements, by Life Stage Group Criteriona Life stage group 0 through 6 mo Human milk content 7 through 12 mo Human milk + solid food 1 through 3 y Extrapolation of data on desirable calcium retention from 4 through 8 year olds Calcium accretion / D BMC / calcium balance 4 through 8 y Desirable calcium retention / factorial / D BMC 9 through 18 y 19 through 30 y Desirable calcium retention / factorial 31 through 50 y Calcium balance Desirable calcium retention / factorial / D BMD 51 through 70 y > 70 y Extrapolation of desirable calcium retention from 51 through 70 year age group / D BMD / fracture rate Pregnancy £ 18 y through 50 y Bone mineral mass Lactation £ 18 y through 50 y Bone mineral mass D BMC is the change in bone mineral mass. D BMD is the change in bone mineral a density. The UL The Tolerable Upper Intake Level (UL) is the highest level of daily nutrient intake that is likely to pose no risk of adverse effects for almost all people. Members of the general population should not routinely exceed the UL. The UL value for calcium is based on milk-alkali syndrome (characterized by hypercalemia and renal insufficiency) as the critical endpoint and is derived from case studies of people who consumed large doses of calcium, mostly in the form of supplements. The UL for calcium represents total intake from food, water, and supplements. Although the 95th percentile of daily intake did not exceed the UL for any age group in the Continuing Survey of Food Intakes by Individuals (CSFII, 1994–1996), people with very high caloric intakes, especially if intakes of dairy products are also high, may exceed the UL of 2,500 mg/day. Although users of dietary supplements of any kind tend to also have higher intakes of calcium from food than nonusers, it is unlikely that the same person would fall at the upper end of both ranges. Prevalence of usual intakes, from foods plus supple- ments, above the UL is well below 5 percent, even for age groups with relatively

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DRIs: THE ESSENTIAL GUIDE TO NUTRIENT REQUIREMENTS 290 high intakes. However, with calcium-fortified foods becoming more common, it is important to maintain surveillance of these foods in the marketplace and to monitor their impact on calcium intake. DIETARY SOURCES Foods Dairy products, such as milk, yogurt, and cheese, are the most calcium-rich foods in Western diets. Other calcium-rich foods include calcium-set tofu, calcium-fortified plant-based beverages, Chinese cabbage, kale, calcium- fortified fruit juices, and broccoli. Although grains are not particularly rich in calcium, the use of calcium- containing additives in these foods accounts for a substantial proportion of the calcium ingested by people who consume a large amount of grains. Among Mexican Americans, corn tortillas are the second most important source of cal- cium, after milk. White bread is the second most important source among Puerto Rican adults. Dietary Supplements According to U.S. data from the 1986 National Health Interview Survey (NHIS), 14 percent of men, 25 percent of women, and 7.5 percent of children 2 to 6 years of age took supplements that contained calcium. Data from 11,643 adults who participated in the 1992 NHIS showed that calcium intakes were higher for men and women who took daily supplements with calcium (of any kind) compared with those who seldom or never took supplements. (This difference was only statistically significant for women.) However, adults who took cal- cium supplements did not have higher intakes of food calcium. Bioavailability With regard to food sources of calcium, bioavailability is generally less impor- tant than the overall calcium content of the food. Calcium absorption efficiency is fairly similar for most foods, including milk products and grains, both of which represent major sources of calcium in North American diets. Calcium may be poorly absorbed from foods rich in oxalic acid (such as spinach, sweet potatoes, rhubarb, and beans) and from foods rich in phytic acid (such as un- leavened bread, raw beans, seeds, nuts, grains, and soy isolates). Although soy- beans contain large amounts of phytic acid, calcium absorption from these le- gumes is relatively high compared with other foods rich in phytic acid. Com- pared with calcium absorption from milk, calcium absorption from dried beans is about half; from spinach it is about one-tenth.

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PART III: CALCIUM 291 As for dietary supplements, the bioavailability of calcium depends on the size of the dose, the form, and the presence or absence of a meal, with the former improving absorption. Tablet disintegration of supplements is crucial, and the efficiency of calcium absorption from supplements is greatest when calcium is taken in doses of 500 mg or less. Dietary Interactions There is evidence that calcium may interact with certain other nutrients and dietary substances (see Table 2). INADEQUATE INTAKE AND DEFICIENCY Chronic calcium deficiency can result from inadequate intake or poor intestinal absorption. During chronic calcium deficiency, the mineral is resorbed from the skeleton to maintain a normal circulating concentration, thereby compromis- ing bone health. Consequently, chronic calcium deficiency is one of several important causes of reduced bone mass and osteoporosis. In the United States each year, approximately 1.5 million fractures are associated with osteoporosis; in Canada in 1993, there were approximately 76,000 such fractures. The po- tential effects of calcium deficiency include the following: • Osteopenia (lower than normal bone-mineral density) • Osteoporosis (very low bone-mineral density) • An increased risk of fractures Special Considerations Amenorrhea: Induced by exercise or anorexia nervosa, amenorrhea results in reduced calcium retention and net calcium absorption, respectively, along with lower bone mass. Menopause: Decreased estrogen production at menopause is associated with accelerated bone loss for about 5 years. Lower levels of estrogen are accompa- nied by decreased calcium absorption efficiency and increased rates of bone turnover. However, available evidence suggests that the calcium intake require- ment for women does not appear to change acutely with menopause. Lactose intolerance: People with lactose intolerance who avoid dairy products and do not consume calcium-rich lactose-free foods may be at risk for cal- cium deficiency. Although lactose intolerance may influence intake, lactose- intolerant individuals absorb calcium normally from milk.

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DRIs: THE ESSENTIAL GUIDE TO NUTRIENT REQUIREMENTS 292 TABLE 2 Potential Interactions with Other Dietary Substances Substance Potential Interaction Notes SUBSTANCES THAT AFFECT CALCIUM Caffeine Caffeine may increase Accelerated bone loss associated with caffeine urinary loss of calcium and consumption has been seen only in postmenopausal decrease calcium absorption. women with low calcium intakes. Available evidence These effects are modest. does not warrant different calcium intake recommendations for people with different caffeine intakes. Magnesium Magnesium deficiency may In general, magnesium deficiency must become cause hypocalcemia. moderate to severe before symptomatic hypocalcemia develops. However, a 3-week study of dietary-induced experimental magnesium depletion in humans demonstrated that even a mild degree of magnesium depletion may result in a significant decrease in serum calcium concentration. Oxalic acid Oxalic acid may inhibit Foods rich in oxalic acid include spinach, sweet calcium absorption. potatoes, rhubarb, and beans. Phosphorus Excess intake of phosphorus This is less likely to pose a problem if calcium intake is may interfere with calcium adequate. Foods rich in phosphorus include dairy absorption. foods, colas or other soft drinks, and meats. Phytic acid Phytic acid may inhibit Foods rich in phytic acid include unleavened bread, calcium absorption. raw beans, seeds, nuts, grains, and soy isolates. Protein Protein may increase urinary The effect of dietary protein on calcium retention is loss of calcium. controversial. Available evidence does not warrant adjusting calcium intake recommendations based on dietary protein intake. Sodium Moderate and high sodium High sodium chloride (salt) intake results in an intake may increase urinary increased loss of urinary calcium. There is indirect loss of calcium. evidence that dietary sodium chloride has a negative effect on the skeleton. However, direct evidence linking sodium intake with bone loss and fracture is lacking. Available evidence does not warrant different calcium intake requirements for individuals based on their salt consumption.

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PART III: CALCIUM 293 TABLE 2 Continued Substance Potential Interaction Notes CALCIUM AFFECTING OTHER SUBSTANCES Iron Calcium may decrease iron Calcium inhibits iron absorption in a dose-dependent absorption. and dose-saturable fashion. However, the available human data fail to show cases of iron deficiency or even reduced iron stores as a result of calcium intake. Magnesium High intakes of calcium may Most human studies of the effects of dietary calcium decrease magnesium on magnesium absorption have shown no effect, but absorption. one has reported decreased magnesium absorption rates. Calcium intakes of as much as 2,000 mg/day (in adult men) did not affect magnesium absorption. Calcium intakes in excess of 2,600 mg/day have been reported to decrease magnesium balance. Several studies have found that high sodium and calcium intake may result in increased renal magnesium excretion. Overall, at the dietary levels recommended in this publication, the interaction of magnesium with calcium is not of concern. Phosphorus Pharmacological doses of Calcium in the normal adult intake range is not likely calcium carbonate may to pose a problem for phosphorus absorption. interfere with phosphorus absorption. Zinc Calcium may decrease zinc Dietary calcium may decrease zinc absorption, but absorption. there is not yet definitive evidence. Human studies have found that calcium phosphate (1,360 mg/day of calcium) decreased zinc absorption, whereas calcium in the form of a citrate–malate complex (1,000 mg/day of calcium) had no statistically significant effect on zinc absorption. Data suggest that consuming a calcium-rich diet does not lower zinc absorption in people who consume adequate zinc. The effect of calcium on zinc absorption in people with low zinc intakes has not been extensively studied.

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DRIs: THE ESSENTIAL GUIDE TO NUTRIENT REQUIREMENTS 294 Vegetarian diets: Vegetarian diets, which may have relatively high contents of oxalic acid and phytic acid (see Table 2), may reduce calcium bioavailability. Mothers who breastfeed multiple infants: Due to the increased milk produc- tion of a mother while breastfeeding multiple infants, increased intakes of cal- cium during lactation, as with magnesium, should be considered. EXCESS INTAKE The available data on the adverse effects of excess calcium intake in humans have primarily come from the study of nutrient supplements. Of the many possible adverse effects of excessive calcium intake, the three most widely stud- ied and biologically important are the following: • Kidney stones • Hypercalcemia and renal insufficiency (also known as milk-alkali syndrome) • The interaction of calcium with absorption of other minerals (see Table 2) Although these are not the only adverse effects associated with excess calcium intake, they do constitute the vast majority of reported effects. Special Considerations Individuals susceptible to adverse effects: Some people may be at greater risk for adverse effects related to calcium. They include those with renal failure, those who take thiazide diuretics, and those with low intakes of minerals that interact with calcium (see Table 2).

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PART III: CALCIUM 295 KEY POINTS FOR CALCIUM Calcium plays a key role in bone health. In fact, more than 99 3 percent of total body calcium found in the teeth and bones. As calcium intake decreases, the efficiency of calcium 3 absorption increases (and vice versa). However, this increased efficiency of calcium absorption is generally not sufficient to offset the loss of absorbed calcium that occurs with a decrease in dietary calcium intake. There is no biochemical assay that reflects calcium nutritional 3 status. During chronic calcium deficiency, the mineral is resorbed from the skeleton to keep the circulating concentration normal, thereby compromising bone health. Since data were inadequate to determine an EAR and thus 3 calculate an RDA for calcium, an AI was instead developed. The adult AIs for calcium are based on desirable rates of 3 calcium retention (as determined from balance studies), factorial estimates of requirements, and limited data on changes in bone mineral density (BMD) and bone mineral content (BMC). The UL is based on milk-alkali syndrome as the critical endpoint. Calcium absorption declines with aging in both men and 3 women. Although increased dietary calcium intake will not prevent the 3 loss of calcium from the maternal skeleton during lactation, the calcium that is lost appears to be regained following weaning. Thus, the AI for calcium in lactating women is the same as that of nonlactating women. The UL value is derived from case studies of people who 3 consumed large doses of calcium, mostly in the form of supplements. Foods rich in calcium include milk, yogurt, cheese, calcium-set 3 tofu, calcium-fortified orange juice, Chinese cabbage, kale, and broccoli. Calcium may be poorly absorbed from foods that are rich in oxalic acid or phytic acid. Calcium deficiency can result from inadequate intake or poor 3 intestinal absorption and can cause osteopenia, osteoporosis, and an increased risk of fractures. Excessive calcium intake can cause kidney stones, 3 hypercalcemia with renal insufficiency, and decreased absorption of certain other minerals.