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* Department of Allied Health, University of Connecticut, Storrs, CT; Yale University, School of Internal Medicine, New Haven, CT; ** Division of Nutritional Sciences, Cornell University, Ithaca, NY; and Yale New Haven Hospital, New Haven, CT
3 To whom correspondence should be addressed. E-mail: jane.kerstetter{at}uconn.edu.
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ABSTRACT |
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 TOP ABSTRACT METHODS AND MATERIALSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • dietary protein • calcium metabolism • soy • meat • parathyroid hormone
Dietary protein is an important regulator of calcium homeostasis. Previous studies in healthy adults showed that 4 d of consumption of a low-protein omnivore diet (0.7 g protein/kg) induces a significant decline in intestinal calcium absorption with an accompanying fall in urinary calcium and a rise in parathyroid hormone (PTH).4 Conversely, during consumption of high-protein omnivore diets (2.1 g protein/kg), intestinal calcium absorption is normal or high, urinary calcium increases, and PTH is suppressed (1,2). Consumption of a high-protein diet for 1 wk induced little change in kinetic measures of rates of bone resorption or formation (3). In another kinetic study, ingestion of a high-protein meat diet for 4 wk did not increase bone resorption (4). The current study was designed to examine the effect of substituting soy protein for meat protein on calcium homeostasis during a 1-wk dietary intervention study in humans.
Soy is a complex food; it contains a variety of compounds that can influence calcium homeostasis and skeletal balance. The estrogen-like effects of isoflavones found naturally in soy have raised considerable interest. Although supportive data exist (5–7), it remains uncertain whether the amount of isoflavones contained in a soy diet can have a clinically significant, bone-sparing effect (8–10).
Few studies have evaluated the effects of soy protein alone on mineral homeostasis, without the potential confounding effect of isoflavones. Determining the effect of soy protein itself on skeletal homeostasis is important because not all soy foods are a rich source of isoflavones. In fact, soy foods vary considerably in their isoflavone content. Traditional soy foods (e.g., tofu, soy milk, tempeh, and miso) provide 
30–40 mg of isoflavones per serving, whereas second-generation soy foods (e.g., soy hot dogs, burgers, cheeses, ice cream) often contain substantially fewer isoflavones, depending on how the soy beans are processed. For example, the isoflavone concentrations of soy foods can range from 0.04 mg/g in soy sausage, to 0.1 mg/g in soymilk, and 2.5 mg/g in soy protein isolate (11).
Because they are relatively low in the sulfur-containing amino acids, soy proteins are thought to be potentially beneficial to the calcium economy and the skeleton because they generate less endogenous acid than animal proteins. Consistent with this, Massey (12) calculated the acidogenic capacity of soy protein (40 mEq potential acid as sulfate/100 g protein) to be considerably lower than that of meat, fish, and poultry (59–73 mEq/100 g protein). Because lower dietary sulfur amino acids mean lower urinary calcium (13), it was assumed that the fall in urinary calcium reflected less calcium wasting. Together, these data suggest that the inclusion of soy foods in a diet will improve calcium economy and bone health because the reduced endogenous acid load will require less buffering in bone, leading to less bone loss. There are, however, a limited number of human intervention studies that evaluated the effect of soy protein alone (low or void in isoflavones) on bone metabolism (6,9).
Because many of the studies evaluating the effects of soy foods on the skeleton employed soy that contained isoflavones (7,8,14,15), it is difficult to determine whether any of the changes were due to the soy protein per se, the isoflavone, or some interaction between them. The purpose of this study therefore, was to explore the acute effects of soy protein alone (vs. meat protein) on calcium economy in healthy adults.
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METHODS AND MATERIALS |
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TOPABSTRACTMETHODS AND MATERIALSRESULTSDISCUSSIONLITERATURE CITED |
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Subjects. Healthy women (n = 20) were recruited to participate in the study; 12 of the women were young (mean age 29.2 ± 1.8, range 20–38 y) and 8 were postmenopausal (mean age 58.9 ± 1.6, range 53–66 y). The body weights of the young and older women were 62.4 ± 2.2 and 68.1 ± 3.2 kg, respectively. The BMI (kg/m2) in the young and older women was 22.6 ± 0.8 and 25.1 ± 0.9, respectively. Exclusion criteria included use of medications known to affect calcium metabolism (e.g., glucocorticoids, nonsteroidal anti-inflammatory medications, vitamin D, birth control pills, and hormone replacement therapy). Subjects with amenorrhea, who were pregnant, who smoked, or who had an eating disorder, diabetes, renal disease, gastrointestinal disease, bone disease, or nephrolithiasis were excluded. Individuals with an intense daily physical exercise routine were excluded. Subjects were asked to suspend any vitamin or mineral supplementation during the entire study. The racial background of the subjects was either Caucasian or Asian. Subjects continued their usual activities at home, school, and work during the study. Light-to-moderate exercise was permitted as long as it did not change during the study. Informed consent was obtained from each participant. Intestinal calcium absorption was measured in the 6 women using dual stable calcium isotopes as previously reported (1). Titratable acid and net acid excretion (NAE) were measured in 12 women (6 young and 6 postmenopausal). Subjects were chosen for the absorption and titratable acid/NAE studies based on their willingness to participate; however, there is no reason to suspect that the findings in these individuals would differ from the findings in the entire group.
Diets.
The design of the experimental and adjustment diets was similar to those in a previous report (2). Under the guidance of a research dietitian, study subjects selected their adjustment diets to contain 1 g protein/kg (from omnivore sources), 20 mmol calcium, and 100 mmol sodium. Subjects consumed sufficient energy for weight maintenance. Caffeine-containing beverages were limited to 1/d and alcohol was not permitted.
During the 4-d experimental period, subjects reported daily to the GCRC to receive their meals and record their body weight. Mean energy intake was 0.14 MJ/kg (33 kcal/kg) and was adjusted with simple sugars and fats to maintain body weight. Mean body weight of the subjects fluctuated <2% throughout the study.
All experimental diets were individually calculated to contain 1 of 2 levels of protein (0.7 and 2.1 g/kg) and 1 of 2 major types of protein (meat or soy). Other nutrients in the experimental diets were controlled [mean calcium intake (range) 19.5–20.1 mmol, sodium 102–103 mmol and phosphorus 35–49 mmol]. Normally, a tripling of dietary protein results in a tripling of phosphorus intake because the 2 nutrients are found together in foods. The difference in the phosphorus intake between the low- and high-protein diets was minimized by selecting foods with a higher phosphorus content during the low-protein diet period and foods with a lower phosphorus content during the high-protein diet period. Subjects consumed low-sodium herbs, spices, condiments, seltzer water, and distilled drinking water ad libitum. Oxalate-rich vegetables and chocolate were excluded from both the adjustment and experimental diets.
An alcohol-washed, low-isoflavone soy protein isolate (Pro Fam 930) was obtained from Archer Daniels Midland. This soy isolate is 90% protein by weight and contains negligible isoflavone (0.2 mg/g). The second soy product used in the experimental diets was Harvest Burgers Recipe Crumbles, a commercially available product distributed by Worthington Foods. Recipe Crumbles is a second-generation soy product; as such, it is low in isoflavones. These 2 products were the only sources of soy used in the experimental soy-based diets. They were independently analyzed for isoflavone content using published methods (16). Beef, poultry, fish and dairy foods were not served during consumption of the soy diets, but they were the primary sources of protein served for the meat diets. A commercially available, chewable form of calcium carbonate (Tums; Smith Kline Beecham) was used in both the meat- and soy-based diets to ensure a total calcium intake of 20 mmol in every subject. The nutrient content of each experimental diet was calculated using the Food Processor Plus nutrient analysis program (ESHA Research), the USDA Handbook no. 8, and manufacturer's information. The phytic acid content of the experimental diet was calculated using published values (17).
Sample collection and analyses. Blood and urine collections were obtained at the beginning and end of each 4-d experimental period. Timed 24-h urine collections on d-1 and 3 were analyzed for calcium, phosphorus, sodium, and creatinine content. In 12 subjects, NAE and titratable acid were measured on d 3 in 24-h urine samples that were collected into mineral oil. Two-hour urine samples from fasting subjects were obtained on d 0 and 4 for measurement of cAMP and creatinine. Blood was drawn at the midpoint of the 2-h period for measurement of mid-molecule PTH, serum cAMP, calcitriol, total and ionized calcium, phosphorus, and creatinine.
Analyses. All assays were performed as previously reported (2). Briefly, serum and urinary creatinine and sodium were measured in the Clinical Chemistry Laboratories of the Yale-New Haven Hospital. Serum total and urinary calcium were measured by flame atomic absorptiometer (Model 2380, Perkin Elmer). Blood ionized calcium was determined on an undiluted sample using a Beckman Lablyte 820, with an ion-selective electrode (Beckman). Mid-molecule PTH was determined with antiserum to the mid-region of human PTH, using 125 iodine-labeled human PTH (37–84) as a radioactive trace, and standards from a human PTH adenoma extract. The method of Reinhardt et al. (18) was used to measure serum calcitriol. Plasma and urinary cAMP were measured as previously reported (19). Nephrogenous cAMP (NcAMP; a bioindex of parathyroid function) was calculated from plasma and urinary cAMP measurements (19). Urinary titratable acid and NAE were measured in triplicate using the method of Chan (20) in which NAE is the sum of the titratable acid plus ammonium minus bicarbonate. Intestinal calcium absorption was measured using dual stable calcium isotopes following the procedure we reported previously (1).
Statistical analysis. All values are presented as means ± SEM. Initial comparisons of the important outcome variables (e.g., PTH, urinary calcium and NAE) were made between the 2 age groups using a t test. The age groups did not differ; thus, they were combined for subsequent analyses.
Repeated measures ANOVA was used to evaluate differences among the 4 levels of protein at baseline (d 0). All dietary intake data and d 4 data were evaluated using a 2-way repeated-measures ANOVA evaluating the type of protein, the level of protein, and their interaction. Once a significant protein level x protein type interaction was identified, multiple paired t tests were conducted and a Bonferroni correction was applied. Pearson's correlation was used to evaluate the relation between urinary calcium, NAE, and N-telopeptide cross-links (NTX). SPSS version 12.0 was used in the statistical analysis of the data. Differences of P < 0.05 were considered significant, whereas a P-value between 0.05 and 0.10 was suggestive of a trend.
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RESULTS |
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TOPABSTRACTMETHODS AND MATERIALSRESULTSDISCUSSIONLITERATURE CITED |
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Urinary titratable acid and NAE were lower when the subjects consumed the soy-based vs. the meat-based diets (P 
0.01; Table 2). When they consumed the high-protein diets, their urinary NAE was higher than when they consumed the low-protein diets (P = 0.03; Table 2). Titratable acid excretion also tended to be higher during the high-protein interventions (P = 0.09). NAE and titratable acid excretion did not differ between the young and postmenopausal women in response to the 4 diets. There was no correlation between 24-h urinary calcium, NTX, and NAE.
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At d 4, NcAMP was significantly influenced by the level and type of dietary protein. The interaction of protein level and protein type was significant for NcAMP (P = 0.03; Table 2). Thus, NcAMP levels were significantly higher during the soy interventions than during the meat interventions. This was particularly evident when subjects consumed the low-protein diets: NcAMP levels were 13% higher during the low-protein soy intervention than during the low-protein meat intervention. A similar but less striking change was observed in serum calcitriol levels at d 4. The serum calcitriol concentration on d 4 of the soy diet periods was higher than at d 4 of the meat diet periods. Urine NTX excretion on d 4 was not affected by the type or level of dietary protein, although the interaction tended to be significant (P = 0.06).
Because of the large interindividual variability in intestinal calcium absorption and the small number of women studied, fractional calcium absorption did not differ significantly when the women consumed the 4 diets. There were 11 occasions on which we measured intestinal calcium absorption during the soy vs. meat diet periods within the same level of protein (6 times during the low-protein and 5 times during the high-protein diet because one subject did not complete the final high-protein study). On 8 of these 11 occasions, intestinal calcium absorption was lower during the soy diet intervention than during the meat diet intervention (P = 0.1, paired t test). Although not significant, the tendency for lower intestinal calcium absorption during the soy protein diet periods (Fig. 1), may be nutritionally relevant.
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DISCUSSION |
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TOPABSTRACTMETHODS AND MATERIALSRESULTSDISCUSSIONLITERATURE CITED |
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There are surprisingly few studies that have investigated the effects of soy protein alone, (e.g., without isoflavones) on calcium and bone metabolism. Three human dietary intervention studies found that soy protein induced less of an increase in urinary calcium than did meat protein (22–24). In another study, the addition of soy protein to a moderately low-protein diet in humans did not induce the rise in urinary calcium that occurred when a comparable amount of meat protein was added to the diet (25). Most recently, Spence et al (9). found that the inclusion of an alcohol-washed soy protein isolate (devoid of isoflavones) in the diet of postmenopausal women resulted in a lower urinary calcium excretion compared with a casein-whey protein.
The variability in urine calcium values in our study was unusually large, which explains in part why the trend toward reduced calcium excretion during the high-meat vs. high-soy protein diet periods was not significant. However, it is worth noting that in 75% of the subjects, urinary calcium values were lower when they consumed the soy protein than when they consumed the meat protein diet. The decline in urine calcium between the high-protein meat and high-protein soy interventions was 0.76 mmol, or 30 mg. Our results are consistent with other studies that generally found that soy protein-based diets are associated with relative hypocalciuria (albeit modest), compared with meat protein diets. What remains unclear is the mechanism underlying this observation.
Because soy protein generates less fixed acid when metabolized than meat protein, it could potentially require less buffering in bone and therefore lead to less skeletal resorption. This would suggest that the reduction in calcium excretion during the soy-based diet could be due to reduced bone loss. Consistent with the notion that soy-based diets generate less fixed acid, in the current study we found that the soy-based diets generated less urinary titratable acid and NAE compared with the meat-based diets. A decrease in titratable acid was also observed by other investigators (8,25) when soy was substituted for meat protein.
However, despite soy's consistent effect on net acid and titratable acid excretion, most studies have not reported beneficial effects of soy on skeletal homeostasis (10). In our study, we found no change in urinary NTX excretion, a marker of bone resorption when the 4 diets were compared. Furthermore, there was no association between NAE and NTX excretion in our subjects. There are at least 4 other recent intervention trials in which soy protein either alone or with isoflavones, did not affect bone balance or turnover (8,9,26,27). In a comprehensive evaluation of skeletal metabolism using calcium isotopes and a panel of indirect markers of bone turnover, Spence et al. (9) found that neither soy protein alone or soy and isoflavone induced changes in bone deposition, resorption, or balance in postmenopausal women. Roughead et al. (8) reported that, in a 7-wk crossover diet study using 47calcium retention as the primary outcome measure, substituting soy (containing isoflavones) for meat protein had no measurable effect on bone homeostasis in 13 postmenopausal women. In a double-blind, randomized, placebo-controlled trial, 202 healthy postmenopausal women who consumed 26 g of soy protein (containing isoflavone) or placebo for 12 mo showed no change in bone mineral density (BMD) (26). Gallagher et al. (27) also found no effect of a soy protein isolate (containing isoflavones) on BMD in postmenopausal women. In these 4 studies, both isoflavones and soy protein were administered together. Because no changes occurred, it is unlikely that either food component had an effect alone. However, there are some human intervention trials in which the addition of soy had a beneficial skeletal effect (5,6,15). Nonetheless, taken together, the majority of data suggest that the effect of soy-based diets on urinary calcium is not likely due to an effect on skeletal balance.
Intestinal calcium absorption, when measured directly with dual stable calcium isotopes did not differ between the diets in our subset of 6 women although, as noted, there was a trend toward lower intestinal calcium absorption during consumption of the soy-based diets. Nonetheless, it seems plausible that a decline in intestinal calcium absorption during the soy diet periods explains the more exaggerated rise in the calcitropic hormones. Contrary to this formulation, Spence et al. (9) did not see a difference in intestinal calcium absorption when subjects consumed soy and control protein diets. One potential explanation is that Spence and co-workers routinely supplemented their subjects with vitamin D, whereas we did not. It is possible that vitamin D supplementation protected these subjects from a soy protein–induced decline in intestinal calcium absorption.
If, in fact, intestinal calcium absorption is impaired during consumption of a soy-based diet, the high phytic acid content of the soy foods may play a role. Phytic acid, inositol hexaphosphate, is a phosphorus-rich compound that occurs naturally at very high levels in soy foods. Phytic acid strongly chelates multivalent metal ions, particularly zinc, calcium, and iron, resulting in the formation of insoluble salts that are poorly absorbed in the gastrointestinal tract (28). Several investigations showed that phytic acid interferes with iron (29–31), zinc (32,33), and probably calcium absorption (34,35).
In summary, in our acute experimental model, a soy-based diet decreased NAE and caused an increase in calcitropic hormones, whereas markers of bone turnover and urinary calcium excretion were unaffected. In a small subset of subjects, intestinal calcium absorption, as measured with dual stable calcium isotopes, tended to be lower during consumption of the soy-based diets. Overall, our data are consistent with the conclusion that soy protein causes a slight decline in intestinal calcium absorption compared with meat protein. Should this indeed be the case, then the substitution of soy proteins for meat proteins may require an increase in dietary calcium and/or vitamin D to compensate for reduced calcium bioavailability.
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FOOTNOTES |
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2 Supported by grants from the U.S. Department of Agriculture (U.S. Department of Agriculture Agreement 97-35200-4420), the NIH (DK 52128), NCRR General Clinical Research Center (Grant number RR00125) and The Ethel F. Donaghue Women's Health Investigator Program at Yale University.
4 Abbreviations used: BMD, bone mineral density; NAE, net acid excretion; NcAMP, nephrogenous cAMP; NTX, N-telopeptide cross-links; PTH, parathyroid hormone; GCRC, General Clinical Research Center.
Manuscript received 10 December 2005. Initial review completed 26 January 2006. Revision accepted 6 April 2006.
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