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Calciuric Effects of Short-Term Dietary Loading of Protein, Sodium Chloride and Potassium Citrate in Prepubescent Girls

College of Pharmacy and Nutrition, University of Saskatchewan, Saskatoon, Saskatchewan, CANADA

Address reprint requests to: Susan J. Whiting, PhD, College of Pharmacy and Nutrition, 110 Science Place, University of Saskatchewan, Saskatoon, SK, CANADA S7N 5C9

	ABSTRACT

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Objective: Studies using adult human subjects indicate that dietary protein and sodium chloride have negative effects on the retention of calcium by increasing urinary calcium excretion, while alkaline potassium improves calcium retention along with decreasing urinary calcium losses. This study investigated the effect of these dietary factors on acute urinary calcium excretion in 14 prepubescent girls age 6.7 to 10.0 years.

Methods: Subjects provided a fasting urine sample then consumed a meal containing one of five treatments: moderate protein (MP) providing 11.8 g protein, moderate protein plus 26 mmol sodium chloride (MP+Na), high protein (HP) providing 28.8 g protein, high protein plus 26 mmol sodium chloride (HP+Na), or high protein plus 32 mmol potassium as tripotassium citrate (HP+K). Urine was collected at 1.5 and 3.0 hours after the meal. Supplemental protein was given as 80:20 casein:lactalbumin. Test meals were isocaloric, and unless intentionally altered, components of interest except phosphate were equal between treatments. Each subject completed all five treatments.

Results: Urinary calcium excretion rose after the meal, peaking at 1.5 hours. There were no significant differences in calcium excretion between treatments at any time point. The high protein treatments did not result in a significant increase in either net acid or sulfate excretion at 1.5 hours compared to moderate protein. Dietary sodium chloride had no effect on urinary sodium or calcium excretion over the 3 hours. After the potassium treatment, sodium excretion increased (p0.002) and net acid excretion decreased (p<0.001) compared to other treatments at 1.5 hours.

Conclusions: In children, a simultaneous increase in protein and phosphorus due to increased milk protein intake did not increase acute urinary calcium excretion. An effect of dietary sodium chloride on acute urinary calcium excretion was not observed. Both these findings were similar to those of adult studies previously conducted in the same laboratory using similar format and treatments. Potassium citrate was not hypocalciuric in children, a response differing from that for adults, who have shown a decrease in acute urinary calcium excretion in response to alkaline potassium treatment. Further characterization of calciuric responses to dietary factors is required for children, who may differ from adults in many respects.

Key words: calcium, urine, children, potassium, sodium, milk protein

	INTRODUCTION

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Researchers have found that bone mass at critical skeletal sites, such as the spine and proximal femur, reaches its peak by the late teens [1,2]. Low bone mass is a factor leading to osteoporotic fractures, and childhood may be the best time to ensure that the genetic potential for bone mass is achieved in order to reduce the risk of developing osteoporosis [3]. Urinary excretion of calcium is an important, regulated component of calcium metabolism. Increases in urinary calcium excretion lead to a less positive calcium balance if absorption is not correspondingly increased. Isolated protein, especially that with a high sulfur-amino acid content such as animal protein, has been shown to increase 24-hour urinary calcium excretion in adults [4]. Effects of natural sources of protein on urinary calcium excretion is less clear, as the high phosphorus content of food proteins appears to reduce urinary calcium excretion and counter the hypercalciuric effect of protein [5,6]. However, in epidemiological studies, a positive relationship between incidence of hip fracture and level of animal protein intake has been observed [7] and subjects consuming animal-based foods excrete more calcium than subjects ingesting plant-based foods at comparable calcium intakes [8]. A high intake of sodium chloride, which increases urinary calcium losses in adults [9] and adolescents [10], is associated with reduced bone density [11]. Alkaline potassium, which decreases urinary calcium excretion in adult men [12,13] and postmenopausal women [14], has been shown to improve calcium retention [14,15].

The impact of protein, sodium chloride, and alkaline potassium on urinary calcium excretion in children has not been adequately studied. It is necessary to determine the calciuric responses of children to these dietary factors in order to make dietary recommendations which will result in optimal accumulation of bone mineral. To investigate the effects of these dietary components on urinary calcium excretion in children, we used a short-term model similar to that developed by Allen and coworkers for testing the calciuric effect of protein in adults [16]. Similar acute load-tests have been performed in our laboratory using adult subjects [17] and it is therefore possible to compare the calciuric responses to diet between children and adults.

	METHODS

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Subjects
Study procedures were approved by the University of Saskatchewan Advisory Committee on Ethics in Human Experimentation, and subjects and their parents or guardians gave informed consent. Twenty subjects began the study and 14 subjects who met our criteria of healthy Caucasian girls completed all five treatments. Reasons for attrition included subjects dropping out, not completing all treatments within the time frame of the study, or being on medication. A questionnaire concerning the children’s health was administered to the parents prior to the start of the load tests. On days preceding the load tests, subjects filled in a food record for that day. Subject data are given in Table 1. Results are based on these 14 girls unless otherwise stated.

Treatments
The base meal alone provided 3.2 g of protein, and the test meals were made by adding to the base meal one of the following: 8.6 g milk protein as casein and lactalbumin, moderate protein (MP); 8.6 g milk protein plus 26 mmol sodium chloride (MP+Na); 26 g milk protein, high protein (HP); 25.6 g milk protein plus 26 mmol sodium chloride (HP+Na); 25.6 g milk protein plus 32 mmol of potassium as tripotassium citrate (HP+K). The added milk protein was a mixture of 80% casein (Alacid 710, New Zealand Milk Products Inc., Santa Rosa, CA) and 20% lactalbumin (Alatal 812, New Zealand Milk Products Inc., Santa Rosa, CA) which simulated the protein composition of cow’s milk. The milk protein mixture contained 0.2 mmol of phosphorus per g of protein. Therefore, the high protein treatments contained higher levels of phosphorus. The total protein intake, including that from the base meal, was 11.8 g for MP and 28.8 g for HP. Table 1 gives the energy, protein, calcium, phosphorus, sodium, potassium and sulfur content of each meal.

To keep the treatments isocaloric, the sugar in the moderate protein treatments was replaced with the artificial sweetener sucralose (Splenda®, McNeil Consumer Products Company, Saint John, NB). During the HP+K treatment, subjects received 250 mL sugar-free soda (Fresca®) with the HP+K treatment, as half of the potassium citrate was dissolved in this drink. There were at least 48 hours between treatments.

Dietary Analysis
Food records for days preceding the acute load tests were analyzed using NUTS nutrient analysis software (Version 3.7, Quilchena Consulting Ltd., Victoria, BC). Nutrient composition of the base meal ingredients were also determined this way. The nitrogen, calcium, phosphorus, sodium, potassium, and sulfur concentrations of the casein and lactalbumin were analyzed by Plains Innovative Laboratory Services (PILS, Saskatoon, SK).

Chemical Analyses
Urine was acidified using 1 mL of 6 mol/L HCl for every 25 mL of urine. Urine was analyzed for calcium by flame atomic absorption spectrophotometry (Perkin-Elmer 4000, Perkin Elmer Corporation, Norwalk, CT) after dilution in lanthanum chloride, sodium and potassium by flame emission spectrophotometry (Corning Flame Photometer 410, Corning Medical and Scientific, Corning, NY), phosphate by the method of Fiske and SubBarow [18], creatinine by a modified Jaffe method [18], and sulfate turbidometrically [19]. All of the above analyses were done in duplicate. Net acid excretion (NAE) was measured in unacidified urine by titration [20]. Only 13 subject samples were available for NAE analysis.

Statistical Analysis
Urine excretion data is expressed per mmol of creatinine, except for creatinine, which is expressed per 1.5 hours. Statistical analysis was performed using the computer program Primer of Biostatistics^TM (version 3.0, McGraw-Hill, Inc., NY). At each time point, the results were analyzed by repeated measures ANOVA to detect treatment effects. If there were differences between treatments at p<0.05, the Student-Newman-Keuls test was used to detect differences between individual treatment means. Correlation analyses were also performed using the same statistical program.

	RESULTS

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Subjects were healthy as determined by the responses to the health questionnaire. One subject was reported to be lactose intolerant but she tolerated all treatments. Another subject had a mean fasting urinary calcium excretion of 0.56 mmol/mmol creatinine, which was below the 95th percentile for fasting urinary calcium found in British children 2 to 15 years old [21] so she was not excluded from the study. The average of complete food records from the 5 days before each study day was used to obtain intakes of protein, calcium, phosphorus, sodium and potassium, given in Table 1. The pre-study food records indicated a significant correlation between protein and phosphorus intake (r=0.89, p<0.001). There was also a significant correlation between calcium intake and protein intake (r=0.75, p<0.001).

There were no significant differences in mean fasting urinary calcium excretion between treatment days (Fig. 1). The average of subjects’ fasting urinary calcium excretion was 0.25 mmol/mmol creatinine, and mean fasting urinary calcium excretion ranged between 0.06 and 0.56 mmol/mmol creatinine. There was no correlation between fasting urinary calcium excretion and pre-study intake of calcium (data not shown). There were no significant differences in 1.5 or 3.0 hour calcium excretion between treatments (Fig. 1). Urinary calcium excretion peaked at 1.5 hours after all treatments.

View larger version (33K): [in this window] [in a new window]   Fig. 1. Effect of test meals fed to children containing moderate protein (MP), MP plus sodium chloride (MP+Na), high protein (HP), HP plus sodium chloride (HP+Na) or HP plus potassium citrate (HP+K) on urinary excretion of electrolytes (expressed per mmol creatinine, Cr). * Significantly different from all other treatment means at same time point (p<0.002). # Significantly different from 3.0 hour phosphate excretion for MP and MP+Na (p<0.05).

There were no significant differences in fasting sodium excretion between treatments (Fig. 1) and no correlation between pre-study sodium intake and fasting urinary sodium (data not shown). In response to the potassium treatment only, there was a significantly higher urinary sodium excretion at 1.5 hours. The average amount of sodium excreted by 3 hours after the administration of HP+K treatment was 10.8 mmol in excess of the amount excreted after the HP treatment. There were no differences in sodium excretion between the other treatments. There was, however, a significant correlation between fasting urinary sodium and fasting urinary calcium (r=0.53, p<0.001), using all the fasting samples from each of the 14 subjects, for a total of 70 samples.

There were no significant differences in fasting phosphate excretion between treatments (Fig. 1) and there was no correlation between pre-study phosphorus intake and fasting phosphate excretion (data not shown). The phosphate excretion at 1.5 hours was significantly higher during the HP+K treatment compared to the other treatments. At 3 hours, the phosphate excretion during the HP+Na treatment was significantly higher than that during the MP and MP+Na treatments.

Net acid excretion (NAE) results for 13 subjects are shown in Table 3. There were no significant differences in fasting NAE between treatments. There was a large drop in NAE at 1.5 hours when the children were given HP+K. It should be noted that when given either of the other HP treatments, the girls did not show a protein-induced increase in net acid excretion at 1.5 hours. Fasting and 1.5 hour urinary sulfate excretion (Table 3) was measured after administration of treatments MP, MP+Na, HP, and HP+Na, to determine if there was any change in sulfate excretion indicating that the high protein treatments were providing excess sulfur amino acids for these children. There were no significant differences in fasting sulfate excretion between treatments. Despite differences in sulfur intake between MP and HP diets (Table 2), our data indicated that an increase in protein load from 11.8 g to 28.8 g did not result in a significantly increased sulfate excretion (p=0.091) in the children.

Results for creatinine, given in Table 3, indicate that there were no significant differences in creatinine excretion between treatments at any time point. There was no significant correlation between pre-study protein intake and fasting creatinine excretion. Fasting creatinine excretion is highly variable because the fasting urine was not from a controlled period of time as were the 1.5 and 3.0 hour collections. There was a significant correlation between average 1.5 hour creatinine excretion and body weight (r=0.81, p<0.001) and between average 3.0 hour creatinine excretion and body weight (r=0.79, p<0.001).

	DISCUSSION

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The use of an acute test to study the effect of dietary factors on calcium excretion in children was demonstrated in this study. Each subject was able to consume all of the treatments. In acute studies involving adults in which urine was collected for 4.5 hours after a meal similar to that given to the children, urinary calcium excretion peaked at 3.0 hours and decreased by 4.5 hours [17]. In our children, urinary calcium excretion peaked earlier, at 1.5 hours, and decreased by 3.0 hours. Therefore, 3.0 hours seemed to be more than adequate as a collection time for children.

In adults, a simultaneous increase in protein and phosphorus intake (as would occur when eating high-protein foods), does not result in a significant increase in urinary calcium excretion over the long-term [6,22] or short-term [16,17]. In the children, an increase in protein intake from approximately 12 g (0.43 g per kg body weight) to approximately 29 g (1.0 g per kg body weight) similarly did not increase urinary calcium excretion. In a corresponding study of adult males [17] we found that an increase in total protein from 23 g (0.32 g per kg body weight) to 53 g (0.75 g per kg body weight) had no effect on urinary calcium excretion in spite of an increase in sulfate and net acid excretion. The finding that an increase in food-derived protein intake, with an accompanying increase in phosphorus, does not increase urinary calcium excretion in children is in agreement with the finding that protein intake did not affect 24-hour urinary calcium excretion or bone density in a group of adolescent girls whose diets were being monitored [10]. An increase in food-derived protein from 0.5 to 1.5 g per kg, as dairy, eggs and meat, did increase urinary calcium excretion in a sample of adolescent renal patients; however, in this study, dietary calcium, phosphate and potassium were not controlled [23].

The girls in our study did not show an increase in urinary excretion of sulfate or net acid in response to the added dietary protein. The subjects appeared to utilize the sulfur amino acids provided by the high protein load. This suggests that after an overnight fast, there was an apparent utilization of all the protein provided by the HP meal although it was equal to the total average daily recommended protein intake for children 7 to 9 years (1.0 g protein per kg) [24]. In the study of adolescent renal patients, Nakano and colleagues [23] compared 1.5 and 0.5 g protein per kg body weight, and found after 4 days of feeding that urinary sulfate as well as net acid excretion rose significantly with the higher protein diet. Thus, it would appear that a much higher intake of protein than that used in our study is necessary to see aciduria and sulfaturia in children.

Studies involving 24-hour urine collections indicate that sodium chloride ingestion increases urinary calcium excretion in adults [13,25,26]. However, the children did not show a change in acute urinary calcium excretion in response to an increase in sodium chloride intake. In the 3 hours of the acute test there was no increase in urinary sodium after a load of NaCl, indicating retention of the ingested sodium. From the results of this study and a similar lack of calciuric response to acute sodium chloride ingestion in adult women [27], it appears that a short-term load test is not useful for studying the effects of sodium chloride intake on urinary calcium excretion. The correlation between fasting urinary sodium/creatinine and fasting urinary calcium/creatinine was significant for the girls in this study (r=0.53, p<0.001, n=70). We found that for 10 adult women who provided six fasting samples each, there was a significant correlation between urinary calcium and sodium excretion (r=0.56, p<0.001) [27]. Thus children show a hypercalciuric response to increased chronic sodium intake as do adults. Matkovic et al [10] found that in early pubertal girls, 24-hour urinary sodium excretion was an important determinant of 24-hour urinary calcium excretion, and that a higher urinary calcium excretion was accompanied by lower bone density. The significance of excess sodium chloride on bone was demonstrated in a prospective study of postmenopausal women in which a negative association between urinary sodium excretion and bone mass was found [11].

In adults, dietary alkaline potassium such as potassium bicarbonate [12–14] or potassium citrate [28] reduces 24-hour urinary calcium excretion and promotes a more positive calcium balance [14,15]. In short-term studies, administration of 50 mmol potassium bicarbonate decreases acute urinary calcium excretion in adults [17]. Children in this study were given potassium citrate providing 32 mmol of potassium (1.2 mmol K per kg body weight) but there was no change in urinary calcium excretion. In contrast, we previously gave adults 50 mmol of potassium bicarbonate (0.7 mmol K per kg) acutely [17] and found significant hypocalciuria. In both the children in this study and adults in our previous study, the acute alkaline potassium treatment resulted in a decrease in net acid excretion and an increase in sodium excretion. Notably, rats also do not respond to a load of alkaline potassium with a decrease in urinary calcium excretion [29,30]. The differences in bone metabolism between children and adults (i.e., bone modelling vs. remodelling) may be involved in the difference in calciuric response between adults and children to alkaline potassium.

An increase in urine volume during the HP+K treatment was observed in the children. In our previous studies in adults, there was no change in urine volume between treatments [17,27]. The increase in volume in the children treated with potassium may have been due to an increase in fluid intake with this treatment. There is the possibility that any hypocalciuric effect of alkaline potassium may have been countered by an increase in calcium excretion caused by the large increase in urine volume at 1.5 hours with the HP+K. Calcium excretion does not vary with changes in free water excretion [31]. The additional solute and volume load of the HP+K treatment may have altered intravascular expansion, triggering atrial natriuretic peptide to promote solute diuresis [32]. Possibly hypocalciuria was not observed as calcium reabsorption was inhibited. However, the natriuresis occurring with HP+K given to adults did not inhibit a K-induced hypocalciuria. We have observed that rats given potassium bicarbonate also showed an increase in urine volume together with no change in calcium excretion [30]. The large urine volume at this time period likely accounts for the simultaneous increase in phosphate excretion. Studies in both humans [33] and rats [30] show a trend for phosphate excretion but not calcium excretion to parallel urine volume. The parallel responses between the responses of children and rats to alkaline potassium warrants further study.

	CONCLUSIONS

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A short-term model for testing the calciuric effect of dietary factors, similar to acute load-tests we have performed using adult subjects, was tested in prepubescent girls. A simultaneous increase in protein and phosphorus intake did not increase urinary calcium excretion in children measured acutely. The girls did not show an increase in net acid excretion with the high protein intake, and seemed to utilize the additional sulfur-containing amino acids provided by the high protein treatment. The short term load test did not show an expected hypercalciuria after an acute load of sodium chloride. The alkaline potassium did result in an increase in urinary sodium excretion and a decrease in net acid excretion, but did not affect urinary calcium excretion as has been observed in adults. Determination of calciuric responses by children to dietary factors which affect calcium metabolism are necessary in order to make specific dietary recommendations for children to optimize accumulation of bone mineral.

	ACKNOWLEDGMENTS

 
This work was supported by the Dairy Farmers of Canada. The participation of the subjects was greatly appreciated as was the technical assistance of Virginia Guiboche, Celeste Meyer, and Darin Anderson.

Received January 1, 1997. Accepted October 1, 1997.

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