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JOURNAL OF FOOD COMPOSITION AND ANALYSIS


Journal of Food Composition and Analysis 20 (2007) 717724 www.elsevier.com/locate/jfca

Short Communication

A system to assess the quality of food sources of calcium


C. Alan Titchenal, Joannie Dobbs
Human Nutrition, Food and Animal Sciences, University of Hawaii at Manoa, 1955 East-West Rd. #216, Honolulu, Hawaii 96822, USA Received 10 January 2006; received in revised form 23 April 2006; accepted 24 April 2006

Abstract Since the bioavailability of calcium varies greatly among various types of foods, information merely listing the amounts of calcium in foods can be very misleading. Using published values for calcium fractional absorption, a simple two-criteria system is presented and used to assess foods as reasonable calcium sources. For a food to be a good calcium source, two criteria must be met: a standard serving must contain at least 30 mg of absorbable calcium, less than 418 kJ (100 kcal) of the food must provide 30 mg of absorbable calcium. Calcium-containing foods are divided here into good calcium sources (both criteria are met), potential calcium sources (only one criterion is met), and poor calcium sources. Good sources include most milk products, most types of tofu, some dark green leafy cabbage family vegetables, turnip greens and canned sh such as salmon and sardines that include bones. Potential calcium sources include ice cream and most green leafy vegetables. Poor calcium sources include cottage cheese, all beans, some types of tofu, almonds, and sesame seeds. Using this system to identify calcium-rich food sources avoids the misuse of nutrient data when foods are listed simply by their calcium content. r 2006 Elsevier Inc. All rights reserved.
Keywords: Calcium; Bioavailability; Calcium food sources; Recommended intake

1. Introduction Largely because of public health achievements, people in developed countries are living much longer than in the recent past. During the 20th century, the average American lifespan increased by more than 30 years (Centers for Disease Control and Prevention, 1999). As a result of living longer lives, many more people are at great risk for osteoporosis. Consequently, obtaining adequate amounts of bioavailable calcium throughout life is of growing importance as a major component in osteoporosis prevention. The diets of some cultures and many people selecting vegetarian diets include many foods that contain signicant amounts of calcium, but with limited bioavailability. Contemporary textbooks and nutrition education materials frequently provide lists of foods that are considered to be sources of particular nutrients such as calcium.
Corresponding author. Tel.: +1 808 956 7411; fax: +1 808 956 4024.

E-mail address: titch@hawaii.edu (C.A. Titchenal). 0889-1575/$ - see front matter r 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.jfca.2006.04.013

However, the criteria used to compile such lists are rarely expressed. Apparently, including a food on such a list is simply based on the fact that a commonly consumed amount of a food contains a signicant amount of the particular nutrient. Such vague criteria can result in a list of foods that include items that are not reasonable sources of a nutrient from a physiological or practical perspective. This can occur for a nutrient like calcium when the calcium in a food has low bioavailability, the energy content of the food is excessive compared to the amount of absorbable calcium present, or an excessive volume of the food must be consumed to obtain a signicant amount of calcium. Various criteria for stating that a food is a good source of a particular nutrient have been proposed for food labeling purposes. Using calcium as an example, in the United States, the established serving size (reference amount used for labeling) must contain 20% or more of the daily value (200 mg calcium) to be labeled high in calcium, rich in calcium, or excellent source of calcium (United States Code of Federal Regulations).

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The Codex Alimentarius, Guidelines for Use of Nutrition Claims, provides the following criteria as percentages of the nutrient reference value (NRV) of 800 mg for calcium (FAO/WHO, 2001): Source of calcium: 15% of NRV (120 mg) per 100 g solid food, 7.5% of NRV (60 mg) per 100 mL liquids, 5% of NRV (40 mg) per 100 kcal, 12% of NRV (96 mg) per 1 MJ, 15% of NRV (120 mg) per serving. High in calcium ( twice the values for source of calcium foods): 30% 15% 10% 24% 30% of of of of of NRV NRV NRV NRV NRV (240 mg) per 100 g solid food, (120 mg) per 100 mL liquids, (80 mg) per 100 kcal, (192 mg) per 1 MJ, (240 mg) per serving.

2. Methods Criteria were established for good calcium sources based on the amount of absorbable calcium in foods and the amount of calcium that most adults should absorb each day. This determination was based on common recommendations for daily dietary calcium intake by healthy adults. In Canada and the United States, the dietary reference intakes (DRIs) are four sets of reference values established by the Institute of Medicine (Food and Nutrition Board, 2003). These reference values include adequate intake (AI) values, which are recommended as average daily nutrient intakes for nutrients for which formal recommended dietary allowances (RDAs) have not been established. Calcium is one of the nutrients with AI values. The AI for calcium for young and middle-aged adults (1850 years) is 1000 mg per day (Food and Nutrition Board, 1997). The comparable value used for nutrition labeling in Europe is the NRV of 800 mg (FAO/ WHO, 2001). Assuming that approximate fractional absorption of calcium from a mixed diet is 30% (Weaver and Heaney, 1999), the typical daily absorption of calcium from a diet containing the AI of 1000 mg of calcium is estimated at 300 mg. Thus, 300 mg is a reasonable approximation of the amount of calcium that adults need to absorb daily. Based on the above framework for daily calcium needs, foods commonly listed as good sources of calcium in nutrition textbooks and other reputable sources were evaluated for their overall quality as calcium sources. This was accomplished by using the following criteria to determine if a food should be considered to be a good calcium source: (1) A standard serving of the food should provide at least 30 mg of absorbable calcium per serving (approximately one-tenth of the total calcium most people should absorb each day). (2) A 418 kJ (100 kcal) of the food should provide at least 30 mg of absorbable calcium. Consequently, 300 mg of absorbable calcium can be obtained from 4180 kJ (1000 kcal) (or less) of foods that meet or exceed this criterion. Based on these criteria, calcium-containing foods were divided into good calcium sources (meet both criteria), potential calcium sources (meet one of the two criteria), and poor calcium sources (meet neither of the two criteria). Values for the calcium content of foods were obtained primarily from the USDA Nutrient Database for Standard Reference (USDA/ARS, 2005). Values for the fractional absorption of calcium from specic foods were obtained from a variety of published scientic articles (Heaney et al., 1993, 2000, 2005a,b; Weaver et al., 1993, 1997, 1999, 2002). Since the fractional absorption of calcium is inversely related to the amount of calcium in a test food (Heaney et al., 1990b), more than one value may have been

It is well known that adequate nutrition depends on a balance between the amount of a nutrient that is absorbed into the body from food and the amount of the nutrient that is lost from the body. A number of food and dietary factors inuence both absorption and retention of calcium. For example, oxalate and phytate in foods can reduce the absorption of calcium (Heaney and Weaver, 1989; Kenneck and Cashman, 2000; Siener et al., 2001; Larsen et al., 2003). Other factors may enhance absorption. Dietary protein and sugars enhance calcium absorption (Kerstetter et al., 2005; Norman et al., 1980). Dietary sodium, protein, and net endogenous noncarbonic acid production can increase calcium excretion in the urine (Lutz, 1984). In general, diets that provide lower levels of xed acid production favor calcium retention (Frassetto et al., 1998). With all of these factors related to calcium economy, it seems that at least some of them should be taken into account when deciding if a food should be considered as a good source of calcium. Many of these factors are a result of the overall diet. However, the fractional absorption of calcium is primarily a function of the amount of calcium present in a food, the chemical and physical form of the calcium, and various components in a food that may inhibit or enhance calcium absorption (Weaver and Heaney, 1999). Fractional absorption of calcium from various food sources has been assessed in a variety of ways and reasonable data currently exist for many foods. The objective of this study is to utilize published values for fractional absorption of calcium from foods to develop a logical system to determine if a food should be considered to be a good source of calcium.

Table 1 Foods that meet both criteria for a good calcium sourcea C.A. Titchenal, J. Dobbs / Journal of Food Composition and Analysis 20 (2007) 717724 Food Serving volumeb (mL) Serving weight (g) Calcium per serving (mg) Calcium fractional absorptionc (%) 32 32 32 32 32 24 32 32 32 30 20 31 31 31 40 40 52 54 27 27 27 Calcium absorbed per serving (mg) 144 108 101 91 89 88 100 98 39 90 60 135 43 78 95 85 51 43 88 64 51 Energy per serving (kJ (kcal)) 644 1016 380 510 610 410 543 715 523 468 468 393 318 368 46 46 67 42 740 485 589 (154) (243) (91) (122) (146) (98) (130) (171) (125) (112) (112) (94) (76) (88) (11) (11) (16) (10) (177) (116) (141) Calcium per 418 kJ (100 kcal) (mg) 291 139 347 234 189 376 238 179 98 268 268 462 182 288 2173 1927 619 790 183 203 133 Calcium absorbed per 418 kJ (100 kcal) (mg) 93 45 111 75 61 90 77 57 31 80 54 143 56 89 860 775 319 425 50 55 36

Yogurt, plain lowfat Yogurt, fruit avors, lowfat Milk (nonfat with added milk solids) Milk (2% reduced fat) Milk (whole) Soy milk (calcium fortied)d Cheese, Mozz, part skim, low moist Cheese, Cheddar Ice cream, vanilla, light (4.8% fat) Orange juice (calcium fortied CCM)d Orange juice (calcium fortied TCP/CL)d Tofu, regular (calcium sulfate)d Tofu, soft (calcium sulfate and nigari)d Tofu, rm (nigari)d Choy Sum (cabbage ower leaves) Kai Choy (Chinese mustard greens) Turnip greens Bok Choy (Chinese cabbage) Sardines, canned in oile Salmon, pink, canned, drainede Salmon, sockeye, canned, drainede
a b

237 237 237 237 237 237

118.5 237 237 118.5 118.5 118.5 118.5 118.5 118.5 118.5

245 245 245 245 244 245 42 42 76 249 249 126 124 126 85 85 72 85 85 85 85

448 338 316 285 276 368 310 306 122 300 300 434 138 253 239 212 99 79 324 235 188

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Provides at least 30 mg of absorbable calcium per serving and per 418 kJ (100 kcal) of the food. Serving sizes commonly used in food guidance systems such as the United States Dietary Guidelines; 1 cup 237 mL. c Percent of ingested calcium in a food that is typically absorbed; varies with the amount of calcium ingested. Fractional absorption values are from Weaver et al., 1999 and other sources. d Calcium content can vary greatly depending on the brand. CCM, calcium citrate-malate; TCP/CL, tricalcium phosphate/calcium lactate. e Fractional absorption is assumed to be similar to bone meal (Heaney et al., 1990a).

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3. Results and discussion Table 1 presents the assessment data for foods that meet both criteria for a good food source of calcium (430 mg absorbable calcium per serving and per 418 kJ (100 kcal) of the food). Most milk products meet both criteria. However, among the types of ice cream, only light ice cream (less than 5% fat) qualies as a good calcium source. Due to higher energy content, the higher fat ice creams do not meet the criterion for 30 mg of absorbable calcium per 418 kJ (100 kcal) (Table 2). Cottage cheese does not meet either criterion for a good calcium source (Table 3). Calcium fortied soymilk and orange juice can both provide signicant amounts of calcium and some types of tofu meet both criteria (Table 1). However, none of the varieties of silken tofu evaluated meet either criterion (Table 3). Some dark green leafy cabbage family vegetables and turnip greens meet the good calcium source criteria (Table 1); however, other vegetables presented in Table 2 do not contain enough absorbable calcium per serving to provide signicant amounts of calcium. Because of their low-energy content, however, when these vegetables are consumed in large amounts, some can provide a signicant amount of absorbable calcium. For example, the absorbable calcium in 500 mL of cooked kale or broccoli is comparable to that in 240 mL of cows milk. However, more than 2 L of cooked spinach are needed to provide comparable amounts of absorbable calcium. Canned sh, such as salmon and sardines that include bones, provide a signicant amount of absorbable calcium. This is based on the assumption that bioavailability of calcium in canned sh is similar to bone meal (Heaney et al., 1990a). However, calcium fractional absorption values were unavailable for other types of seafood prepared by other methods (Table 4). This approach to assessing food sources of calcium requires data on the fractional absorption of calcium for each food. If calcium fractional absorption is not known for a food (or a very similar food), it is generally inappropriate to list it as a good source of calcium. Table 4 presents a speculative assessment of foods sometimes listed as good calcium sources for which data on bioavailability were unavailable. As described in the table, a speculative value for calcium fractional absorption (based on various assumptions described in the table footnote) is assigned to each food to see how these foods are likely to fare in this two-pronged system of assessing food sources of calcium. Only fortied ready-to-eat cereals

Table 2 Foods that meet only one of the two criteria for a good calcium sourcea

Ice cream, vanilla, rich (16.2% fat) Ice cream, vanilla (11% fat) Rutabagad Kaled Broccolid Brussel sproutsd Cabbage, greend Kohlrabid Watercress (fresh) Chinese spinach, amaranthd Cauliowerd Spinachd

Food

Food either contains at least 30 mg of absorbable calcium per serving or per 418 kJ (100 kcal) of the food. Serving sizes commonly used in food guidance systems such as the United States Dietary Guidelines; 1 cup 237 mL. c Percent of ingested calcium in a food that is typically absorbed; varies with the amount of calcium ingested. Fractional absorption values are from Weaver et al., 1999 and other sources. d Cooked by boiling or steaming.
b

published for a particular food. When more than one fractional absorption value was available for a food, the value selected was the one associated with a calcium load similar to what would be commonly consumed in a typical serving of that food. Food serving sizes are those commonly used in food guidance systems such as the United States Dietary Guidelines.

Calcium per 418 kJ (100 kcal) (mg) Energy per serving (kJ (kcal)) Calcium absorbed per serving (mg) Calcium fractional absorptionc (%) Calcium per serving (mg) Serving weight (g) Serving volumeb (mL)

118.5 118.5 118.5 118.5 118.5 118.5 118.5 118.5 118.5 118.5 118.5 118.5

107 72 85 85 78 78 75 82 17 85 62 85

125 92 41 47 31 28 23 21 20 138 10 122

32 32 61 49 61 64 65 67 67 8 69 5

40 30 25 23 19 18 15 14 13 12 7 6

1112 606 100 46 113 138 100 84 125 46 63 88

(266) (145) (24) (11) (27) (33) (24) (20) (30) (11) (15) (21)

47 63 171 448 115 85 97 105 66 1314 69 595

15 20 105 221 70 54 63 70 44 110 47 30

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Table 3 Foods that do not meet either of the two criteria for a good calcium sourcea Food Serving volumeb (mL) 118.5 118.5 118.5 118.5 237 118.5 118.5 118.5 118.5 118.5 118.5 118.5 118.5 118.5 Serving weight (g) 113 113 113 113 245 90 86 90 90 126 126 86 127 89 28 28 Calcium per serving (mg) 69 69 78 68 93 106 88 81 65 39 39 41 41 25 75 37 Calcium fractional absorptionc (%) 32 32 32 32 31 22 24 22 22 31 31 27 24 24 21 21 Calcium absorbed per serving (mg) 22 22 25 22 29 23 21 18 14 12 12 11 10 6 16 8 Energy per serving (kJ (kcal)) 401 339 426 485 531 334 623 523 531 288 288 489 456 472 706 698 (96) (81) (102) (116) (127) (80) (149) (125) (127) (69) (69) (117) (109) (113) (169) (167) Calcium per 418 kJ (100 kcal) (mg) 72 85 76 59 73 133 59 65 51 57 57 35 37 22 44 22 Calcium absorbed per 418 kJ (100 kcal) (mg) 23 27 25 19 23 29 14 14 11 18 18 9 9 5 9 5

Cottage cheese, nonfat Cottage cheese, lowfat (1% fat) Cottage cheese, lowfat (2% fat) Cottage cheese, creamed Soy milk Beans, cowpeas (cooked) Soybeans (cooked) Beans, white (cooked) Beans, small white (cooked) Tofu, silken, soft Tofu, silken, extra rm Beans, Pinto (cooked) Beans, red (cooked) Beans, red kidney (cooked) Almonds, dry roasted Sesame seeds, no hulls
a b

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Food contains at least 30 mg of absorbable calcium per serving and per 100 kcal of the food. Serving sizes commonly used in food guidance systems such as the United States Dietary Guidelines; 1 cup 237 mL. c Percent of ingested calcium in a food that is typically absorbed; varies with the amount of calcium ingested. Fractional absorption values are from Weaver et al., 1999 and other sources.

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Table 4 Speculative assessment of some calcium-containing foods with unknown bioavailability Food Serving volumea (mL) Serving weight (g) Calcium per serving (mg) Possible fractional absorptionb (%) 20 30 30 30 30 30 20 30 30 20 10 10 30 Estimated calcium absorbed per serving (mg) 50200 35 26 26 23 22 20 18 12 12 8 6 6 Energy per serving (kJ (kcal)) 100 431 109 351 527 602 431 67 242 389 79 75 50 Calcium per 418 kJ (100 kcal) (mg) 2501000 113 338 102 62 51 97 375 71 65 432 350 158 Estimated calcium absorbed per 418 kJ (100 kcal) (mg) 50200 34 102 31 19 15 19 113 21 13 43 35 48

Fortied ready-to-eat cereals Ocean perch, Atlantic, dry cooked Okra, cooked from frozen Blue crab, canned Clams, canned Rainbow trout, farmed, cooked Oatmeal, plain, instant, fortied Seaweed, wakame, raw Molasses Figs, dried Beet greens, cooked Taro leaf, cooked Winged beans, immature, cooked
a b

118.5

118.5 15 59 118.5 118.5 118.5

28 85 85 85 85 85 28 40 20 37 85 73 31

2501000 116 88 86 78 73 100 60 41 60 82 63 19

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(103) (26) (84) (126) (144) (103) (16) (58) (93) (19) (18) (12)

Serving sizes commonly used in food guidance systems such as the United States Dietary Guidelines; 1 cup 237 mL. Speculative values based on the following assumptions: Most values are arbitrarily set at 30%. Fortied ready-to-eat cereals and oatmeal are set at 20% to allow for some inhibition of calcium absorption by the ber and phytate in whole grain cereals. Figures are set at 20% because much of the calcium may be in the seeds which may limit calcium bioavailability. Beet greens and taro are set at 10% because they both contain a signicant amount of oxalate.

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and Atlantic Ocean perch meet both criteria. This variety of perch appears to contain much greater amounts of calcium than most nsh (USDA/ARS, 2005). The bioavailability of calcium in fortied cereals may be quite variable and dependent upon the form of calcium used in fortication as well as the ber and phytate content of the grains used to make the cereal. The remaining foods in Table 4 are unlikely to meet the criterion of 430 mg absorbable calcium per serving. In combination, these foods can contribute to overall intake of absorbable calcium, albeit in limited amounts. Most current nutrition textbooks provide calcium food lists that include poor calcium sources (Table 3). These lists are misleading when calcium values are listed without qualication as to bioavailability or other limitations. Simple calculations using Table 3 data illustrate that these foods contribute little absorbable calcium in comparison to the 300 mg of absorbable calcium needed daily by the average adult. To put this into perspective, absorbing 300 mg of calcium requires consuming about 7200 kJ (1725 kcal) of silken tofu (3 L or 12.5 cups), 8700 kJ (2080 kcal) of cooked white beans (2 L or 8.3 cups), or 12 500 kJ (3000 kcal) of almonds (525 g). In the amounts commonly and reasonably consumed, these foods contribute little to total calcium needs and should not be considered good sources of calcium. Perhaps the most basic example of the inappropriate use of data on the calcium content of foods is illustrated by spinach. The calcium content is similar in equal volumes of cooked spinach and milk. However, it would require approximately 6 L of cooked spinach (or 700 mL of milk) to obtain 300 mg of absorbable calcium. Although the concept of calcium bioavailability is almost always discussed in nutrition textbooks, their calcium food source tables commonly include foods like spinach with no indication of the extremely limited bioavailability. Understandably, nutrition education materials also ignore bioavailability. For example, the United States Department of Agricultures MyPyramid website (USDA/CNPP, 2005) links to a table in the United States Dietary Guidelines that lists white beans, spinach and beet greens among food sources of calcium. Although a footnote to the table states that bioavailability should be considered in selecting dietary calcium sources, there is no indication that specic foods in the table have low bioavailability. Consumers of nutrition information should not need to become experts in nutrient bioavailability to properly use nutrition education materials. Because information on the bioavailability of calcium in foods is relatively extensive, it seems that it is time to incorporate this knowledge into applied nutrition. 4. Conclusion The criteria that a good food source of calcium should provide at least 30 mg of absorbable calcium per standard serving and per 418 kJ (100 kcal) of food can facilitate the

evaluation of calcium food sources. Based on these criteria, most of the foods listed in Tables 2 and 4 and all of the foods in Table 3 should not be included in lists of good food sources of calcium. Using a systematic approach such as that proposed here could facilitate decisions about what foods to include in lists of recommended calcium food sources. This will help to prevent the misuse of nutrient data based upon oversimplied listing of foods merely by calcium content. Acknowledgments The authors would like to thank many researchers who published the data on calcium bioavailability that made this paper possible. We also would like to acknowledge the University of Hawaii Research Council for its contribution to the nancial support of this work. References
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724 C.A. Titchenal, J. Dobbs / Journal of Food Composition and Analysis 20 (2007) 717724 U.S. Department of Agriculture, Center for Nutrition Policy and Promotion, 2005. MyPyramid USDA Food Guidance System. Retrieved April 22, 2006 from /http://www.mypyramid.gov/ pyramid/milk_tips.html#nomilkS. Weaver, C.M., Heaney, R.P., 1999. Calcium. In: Shils, M.E., Olson, J.A., Shike, M., Ross, A.C. (Eds.), Modern Nutrition in Health and Disease. Williams & Wilkins, Baltimore, pp. 141155. Weaver, C.M., Heaney, R.P., Proulx, W.R., Hinders, S.M., Packard, P.T., 1993. Absorbability of calcium from common beans. Journal of Food Science 58, 14011403. Weaver, C.M., Heaney, R.P., Nickel, K.P., Packard, P.I., 1997. Calcium bioavailability from high oxalate vegetables: Chinese vegetables, sweet potatoes and rhubarb. Journal of Food Science 62, 524525. Weaver, C.M., Proulx, W.R., Heaney, R.P., 1999. Choices for achieving adequate dietary calcium with a vegetarian diet. American Journal of Clinical Nutrition 70, 543S548S. Weaver, C.M., Heaney, R.P., Connor, L., Martin, B.R., Smith, D.L., Nielsen, S., 2002. Bioavailability of calcium from tofu as compared with milk in premenopausal women. Journal of Food Science 67, 31443147. Larsen, T., Thilsted, S.H., Biswas, S.K., Tetens, I., 2003. The leafy vegetable amaranth (Amaranthus gangeticus) is a potent inhibitor of calcium availability and retention in rice-based diets. British Journal of Nutrition 90, 521527. Lutz, J., 1984. Calcium balance and acidbase status of women as affected by increased protein intake and by sodium bicarbonate ingestion. American Journal of Clinical Nutrition 39, 281288. Norman, D.A., Morawski, S.G., Fordtran, J.S., 1980. Inuence of glucose, fructose, and water movement on calcium absorption in the jejunum. Gastroenterology 78, 2225. Siener, R., Heynck, H., Hesse, A., 2001. Calcium-binding capacities of different brans under simulated gastrointestinal pH conditions. Journal of Agricultural and Food Chemistry 49, 43974401. U.S. Code of Federal Regulations, 2005. Specic requirements for nutrient content claims. Title 21, part 101, section 54. U.S. Department of Agriculture, Agricultural Research Service, 2005. USDA Nutrient Database for Standard Reference, Release 18. Retrieved June 130, 2005 from the Nutrient Data Laboratory Home Page, /http://www.ars.usda.gov/ba/bhnrc/ndlS.

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