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diet13
Connie M Weaver, William R Proulx, and Robert Heaney
ABSTRACT To achieve adequate dietary calcium intake, of calcium. In this review, the choice of the calcium food source
several choices are available that accommodate a variety of and the influence of salt, protein, and caffeine on calcium reten-
lifestyles and tastes. Liberal consumption of dairy products in the tion, and ultimately calcium requirements, are discussed.
diet is the approach of most Americans. Some plants provide
absorbable calcium, but the quantity of vegetables required to
Am J Clin Nutr 1999;70(suppl):543S8S. Printed in USA. 1999 American Society for Clinical Nutrition 543S
544S WEAVER ET AL
TABLE 2
Comparison of sources of absorbable calcium with milk
Estimated Servings
Serving Calcium Fractional absorbable needed to equal
Food size1 content2 absorption3 calcium4 240 mL milk
g mg % mg n
Milk 240 300 32.1 96.3 1.0
Beans
Pinto 86 44.7 26.7 11.9 8.1
Red 172 40.5 24.4 9.9 9.7
White 110 113 21.8 24.7 3.9
Bok choy 85 79 53.8 42.5 2.3
Broccoli 71 35 61.3 21.5 4.5
Cheddar cheese 42 303 32.1 97.2 1.0
Cheese food 42 241 32.1 77.4 1.2
Chinese cabbage flower leaves 85 239 39.6 94.7 1.0
Chinese mustard greens 85 212 40.2 85.3 1.1
Chinese spinach 85 347 8.36 29 3.3
Fruit punch with calcium citrate malate 240 300 52.0 156 0.62
Kale 85 61 49.3 30.1 3.2
Spinach 85 115 5.1 5.9 16.3
(0.506 and 4.094 g) for 2-wk periods on subjects with either low industrialized nations. By using urinary calcium values for known
(<1554 mg) or high (<1876 mg) daily calcium intakes were stud- protein intakes from Zemel (29), dietary calcium intakes required
ied (26). Although this was a small sample size (n = 3 per group), to offset protein-induced urinary calcium losses were calculated
sodium intake significantly affected urinary calcium (P < 0.05). (Table 3). Each additional gram of dietary protein results in an
A longitudinal study in postmenopausal women showed a additional loss of 1.75 mg Ca/d. With an average absorption
negative correlation between urinary sodium excretion and bone efficiency of 30%, this requires an additional 5.83 mg dietary
density of the hip. Because no bone loss occurred at the total hip Ca/d to offset the loss. When protein that is high in phosphorus is
with an intake of 1768 mg Ca/d or with a urinary excretion of ingested, as is the case for meat, cereals, beans, and dairy prod-
2110 mg Na/d, it was suggested that bone loss could have been ucts, the hypercalciuric effect of protein is offset by the hypocal-
prevented by either a dietary increase of 891 mg Ca/d or by halv- ciuric effect of phosphorus (28). However, increasing phosphorus
ing the daily sodium excretion (27). Because neither of these increases endogenous fecal calcium to about the same extent as
diets is common, it may be more realistic for some to reduce their does decreasing urinary calcium. Thus, the effect of protein on
sodium intake by a modest amount and increase their calcium altering calcium requirements is similar whether the loss occurs
intake by a modest amount (eg, 1198 mg Ca/d and 2.3 g Na/d) through the urine or feces.
than to focus on either nutrient exclusively. The specific amino acid profileespecially of amino acids
containing sulfurdetermines the calciuretic effect of protein
(29). Sulfate generated from the metabolism of these amino
REDUCING DIETARY PROTEIN VERSUS INCREASING acids increases the acidity of the urine, causing greater amounts
DIETARY CALCIUM of calcium to be excreted in the urine. The proteins of many
The effect of dietary protein on calcium balance is a well-doc- plants, especially legumes, have lower amounts of methionine
umented phenomenon. As the intake of dietary protein increases, and cysteine than do animal proteins. Young and Pallett (30)
the urinary excretion of calcium increases as a result of decreased summarized the amino acid content of various protein sources
fractional tubular reabsorption, such that doubling protein intake based on data from the Food and Agriculture Organization and
results in a 50% increase in urinary calcium excretion (28). As a the US Department of Agriculture (Table 4). The concentration
result, recommended intakes of dietary calcium are influenced by of sulfur-containing amino acids in cereals is similar to that in
the protein intake of the population for which they are set. This animal foods, whereas nuts and seeds have the highest concen-
largely explains why recommended calcium intakes for the US tration at 46 mg/g protein. Using US Department of Agriculture
population are higher than those for populations in other, less- food-consumption data, Young and Pellett (30) calculated the
546S WEAVER ET AL
TABLE 3 following a vegetarian diet does not guarantee that urinary cal-
Calcium intakes required to offset urinary losses in adults consuming cium will be lower than that of omnivores. Kunkel and Beauch-
various amounts of dietary protein ene (35) studied the protein intake and urinary excretion of pro-
Urinary Required dietary tein metabolites of 125 vegetarian and nonvegetarian women.
Protein intake calcium loss1 calcium intake2 Although the total protein intake of the vegetarians was signifi-
g/d mmol/d mg/d
cantly lower than that of the nonvegetarians (53.6 and 66.5 g/d,
respectively) and significant differences in the intake of animal
48 4.2 970 and plant protein existed between the 2 groups, the excretion of
54 4.4 1006
sulfate in the urine was not significantly different between the 2
60 4.7 1043
66 5 1079
groups. Therefore, some vegetarians may be living under a false
72 5.3 1112 sense of security with regard to their calcium balance if their
78 5.5 1149 protein intakes are similar to those of nonvegetarians or if their
84 5.8 1185 diet provides a significant sulfur-containing amino acid load.
90 6 1219 Additional research is needed to understand the quantitative rela-
96 6.3 1255 tion between the sulfur-containing amino acid content in the diet,
1
When protein sources are rich in phosphorus, the calcium loss is whether from plant or animal sources, and urinary calcium.
shifted from urine to feces (28). Urinary calcium values per protein load Two strategies exist for minimizing the impact of dietary pro-
were obtained from data provided in reference 29. These values, corre- tein on calcium balance while consuming a plant-based diet. The
sponding to a range in protein intakes, were determined by using an intake first is to consume a diet with a low protein content, a low sul-
of 500 mg Ca/d. At the high calcium intakes suggested here, the associated fur-containing amino acid content, or both. This would effec-
absorptive hypercalcemia would result in additional calcium loss in the
TABLE 5
Protein and calcium intakes of female lactoovovegetarians and omnivores1
Lactoovovegetarians Omnivores
Study Calcium Protein Ca:Pro Calcium Protein Ca:Pro
mg/d g/d mg/d g/d
Tylvasky and Anderson (36) (n = 20) 898 56.0 16.0 712 68.0 10.5
Tesar et al (37) (n = 366) 823 442 54.6 2.1 15.1 902 21 69.9 1.1 12.9
Marsh et al (38) (n = 28) 820.7 351 62.6 23.7 13.1 863 199 76.5 20.0 11.3
Janelle and Barr (39) (n = 37) 875 255 57.1 10.8 15.3 950 437 77.1 19.7 12.3
Nieman et al (40) (n = 37) 628 328 46.8 3.0 13.4 633 73 55.0 3.1 11.5
Shultz and Leklem (41) (n = 37) 782 311 60.0 14 13.0 841 246 62.0 10 13.6
1
Ca:Pro, calcium-to-protein ratio.
2
x SD.
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