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The Journal of Clinical Endocrinology & Metabolism Vol. 85, No. 12 4470-4475
Copyright © 2000 by The Endocrine Society

From the Clinical Research Centers

Changes in Calcium Kinetics in Adolescent Girls Induced by High Calcium Intake1

M. E. Wastney, B. R. Martin, M. Peacock, D. Smith, X.-Y. Jiang, L. A. Jackman and C. M. Weaver

Division of Neonatology (M.E.W.), Georgetown University Medical Center, Washington, DC 20007; Department of Foods and Nutrition (B.R.M., L.A.J., C.M.W.), Purdue University, West Lafayette, Indiana; Indiana University School of Medicine (M.P.), Indianapolis, Indiana; and Department of Chemistry (D.S., X.-Y.J.), University of Nebraska, Lincoln, Nebraska

Address all correspondence and requests for reprints to: Meryl E. Wastney, Ph.D., DRC, Private Bag 3123, Hamilton, New Zealand. E-mail: wastneym{at}drc.co.nz


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
To identify the mechanism/s whereby calcium retention is increased by calcium intake in adolescent girls, kinetic studies were performed using stable calcium isotope tracers. Girls (n = 10; 12 ± 1 yr old, mean ± SD) were studied while on a controlled diet containing a low (21.2 mmol/day) and a high (47.4 mmol/day) calcium intake, in randomized order, using a cross-over design. Studies were separated by 1 month. Calcium tracers were administered after 1 week on the study diet, orally and iv; and serum, urine, and feces were collected for the following 14 days. Tracers were measured using fast atom bombardment mass spectrometry, and kinetic data were analyzed by compartmental modeling. Biochemical markers of bone turnover were measured in serum and urine samples. On high (compared with low) calcium intake, fractional absorption did not differ, absorbed calcium increased (19.6 ± 7.5 vs. 8.0 ± 2.5 mmol/day, mean ± SD, P < 0.001), calcium excreted in urine increased (2.8 ± 1.7 vs. 2.1 ± 1.1 mmol/day, P < 0.01), calcium retained in bone increased (14.5 ± 8.9 vs. 3.2 ± 3.6 mmol/day, P < 0.001), bone formation did not change, and bone resorption decreased by 32%. These changes, measured by kinetics, were corroborated by changes in markers of bone turnover. We conclude that increased bone retention of calcium, with high calcium intake in adolescent girls, is attributable to an increase in absorption and a decrease in bone resorption.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
IN ADOLESCENTS, CALCIUM retention increases linearly with calcium intake (1, 2), up to about 37 mmol/day. Calcium intakes above this level, up to 57 mmol/day, result in relatively small additional accumulation (2). Controlled trials in children have confirmed that bone mass increases when calcium intake is supplemented (3, 4, 5, 6, 7).

The mechanisms involved in the increase in bone retention have not been identified, although both suppression (8) and stimulation (9) of bone remodeling have been proposed. Serum osteocalcin (OC) a marker of bone formation, was decreased by 15% in 7- to 10-yr-old twins given a 25 mmol/day calcium supplement for 3 yr, which increased bone mass, compared with those given placebo (10). However, no changes were observed in serum OC and bone specific alkaline phosphatase (markers of bone formation) or urinary cross-links (bone resorption markers) in adolescent girls whose bone density increased with milk supplementation (4).

Kinetic studies, using calcium tracers, provide a more quantitative measure of bone turnover than bone markers. The purpose of this study was to identify the mechanisms whereby calcium intake increases calcium retention in adolescents, by measuring calcium kinetics, biochemical markers of bone turnover, and serum levels of calcium-regulating hormones in the same girls, on a low and high intake of calcium.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Subjects

Healthy, white girls, 11–14 yr old (12 ± 1 yr, mean ± SD, n = 10) participated in a study to determine the relationship between calcium intake and retention, under a controlled living environment, as described previously (2). Subject characteristics are given in Table 1Go. Exclusion criteria included daily calcium intakes of greater than 20 mmol, disease affecting calcium metabolism, use of sex steroid contraceptives, smoking, and weight outside 85–120% of the ideal for age and height. The protocol was approved by Purdue University and Indiana University School of Medicine Use of Human Subjects Research Committees. Informed consent was obtained from subjects and their guardians.


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  		Table 1. Age, sexual maturity, and anthropometrics of adolescent girls (n = 10)

 
Calcium kinetics

Subjects were studied while on a high (47.4 ± 1.2 mmol/day) or low (21.2 ± 2.0 mmol/day) calcium intake, during two 21-day study periods that were separated by 1 month, in randomized order, using a cross-over design. No sequence effect of calcium intake on calcium retention was detected, as discussed previously in detail (2). The high intake was achieved by fruit-flavored beverages containing calcium citrate malate (Proctor & Gamble, Cincinnati, OH), as described previously (2). After a 1-week adaptation to the assigned diet, subjects were administered stable calcium isotope orally (1 mmol of 44Ca as CaCO3) with a breakfast containing one-third of their daily calcium intake, and 1h after the oral dose, iv (0.9 mmol of 42Ca as CaCl2). All urine and feces and 28 blood samples were collected during the 14 days after tracer administration. Compliance of urine and fecal collections was determined by creatinine and PEG recovery, as described previously (2). Calcium was determined in the samples by atomic absorption spectroscopy (5100 PC, Perkin-Elmer Corp., Norwalk, CT), and isotope ratios were determined by fast atom-bombardment mass spectrometry (11).

Biochemical markers of bone turnover

At the end of each 21-day metabolic period, blood was drawn, after an 8-h overnight fast, and left to clot for 30 min. Serum was removed immediately and stored at -70 C. Twenty-four-hour urine collections, at the end of each balance period, were aliquoted and stored at -70 C. Biochemical markers of bone formation (serum OC and serum bone alkaline phosphatase) and biochemical markers of bone resorption [serum tartrate-resistant acid phosphatase, urinary hydroxyproline/creatinine (OHP:Cr), and urinary cross-linked N- teleopeptides of type I collagen] were measured as described previously (12). Pyridinoline (PYR) and total deoxypyridinoline (DPX) were measured by high-performance liquid chromatography (13). Vitamin D metabolites were measured as previously described (14). Creatinine was measured by a Multichannel Analyzer (Roche). Serum PTH 1–84 was measured by two-site RIA (Nichols Institute Diagnostics, San Juan Capistrano, CA). Insulin-like growth factor 1 (IGF-1) was analyzed by using kits from DSL (Webster, TX).

Data analysis

Tracer data (oral and iv) from serum, urine, and feces were fitted simultaneously by a three-compartmental model, described previously (15), using the WinSAAM modeling program (16). The model (Fig 1Go) consists of compartments representing calcium pools within the body that turn over at distinct rates. Transfer of calcium between compartments, L(I, J), was defined as the fraction of compartment J moving into compartment I per unit time. The mass of calcium transferred per day, or transport rate, R(I, J), was calculated as the product of fractional transfer and compartment mass, M(J): R(I, J) = L(I, J) x M(J). Bone turnover parameters were determined as described previously (15), including rates of calcium deposition in bone or bone formation (Vo+), resorption of calcium from bone (Vo-), and calcium retention or bone balance (Vbal) calculated as Vo+ - Vo-. Rates of calcium absorption (Va), calcium excretion in urine (Vu), fecal calcium excretion (VF), and endogenous fecal calcium excretion (Vf) were also calculated. Absorption was calculated as the fraction of calcium in the gut (compartment 8) that entered serum (compartment 1): absorption = L(1, 8)/[L(1, 8) + L(9, 8)].



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  		Figure 1. A model of calcium metabolism in adolescent girls. Circles, Compartments; numbers in circles, compartment number; arrows, movement between compartments; thick arrows, entry of calcium via the diet (Vi) or bone resorption (Vo-). Asterisks indicate entry of tracer, and triangles identify sampled compartments. Compartment 1 contains blood; compartment 2, soft tissue; and compartment 3, exchangeable calcium on bone. Values next to arrows are transfer coefficients (fraction/day, mean ± SD) for girls (n = 9); while on low (upper value) and high (lower value), calcium intakes of 21.5 mmol/day and 47.4 mmol/day, respectively. Urinary excretion, L(6 1 ), was significantly different (paired t test, P < 0.05) on low vs. high calcium intake. Absorption, calculated as L(1 8 )/[L(1 8 )+L(9 8 )], also differed (P < 0.05) with intake. L(3 2 ) was allowed to vary during fitting of the model to the data, but the value did not differ significantly between low and high calcium intake.

 
Assumptions in fitting the data were: that kinetics were identical for the tracer administered orally and tracer administered iv; and that subjects were in steady-state during the 14 days after the administration of tracers. As reported previously, a 7-day period was adequate to achieve a constant fecal Ca/PEG ratio on these calcium intakes (2), an indicator of steady-state. The amount of tracer remaining from the first study, at the start of the second study, was determined by simulation, by solving the model for 35 days beyond the first study (i.e. from day 14 to day 49), to determine the amount of tracer remaining in each compartment.

Data were fitted for each subject while on the low calcium intake. Then, the minimum number of parameters necessary to fit data, obtained while the subjects were on high calcium intake, were changed. One subject was excluded from analysis of kinetic data, because she was not compliant in collecting urine and fecal samples (PEG recovery < 80%).

Population values for kinetic parameters were determined using the multiple studies feature of the SAAM program (17). Paired t tests were used to compare the effect of calcium intake on biochemical measures. Significant differences were determined to be P < 0.05.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Kinetic data are shown for serum, urine, and feces for a representative girl on low and high calcium intake (Fig. 2Go). After iv tracer administration, there was little difference in tracer decrease from serum on the high vs. low calcium diet (Fig. 2AGo); tracer excreted in urine was higher on the higher intake (Fig. 2BGo), whereas similar amounts were excreted in feces (Fig. 2CGo). After oral tracer administration, appearance of tracer in serum was similar on both low and high intake (Fig. 2DGo), indicating that fractional absorption did not differ between the low and high calcium intake. Tracer excretion in urine was higher on the high intake (Fig. 2EGo), and appearance of tracer in feces was similar, although (in this subject) tracer was excreted faster on the high calcium intake (Fig. 2FGo). These differences are confirmed by the parameter values calculated using the model where all, except for urinary excretion, are the same for low and high intake (Fig 1Go).



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  		Figure 2. Observed (symbol) and calculated (lines, using the model in Fig. 1Go) values for one subject while on low [20 mmol/day (triangles, solid line)] and high [46 mmol/day (squares, dotted line)] calcium intake. Values are shown for tracer in serum, urine, and feces after iv (A, B, and C) and oral (D, E, and F) tracer administration and for calcium excretion in urine (G) and feces (H).

 
The fraction absorbed did not differ on the high vs. low intake (Table 2Go). The fraction absorbed (calculated from tracer, administered with breakfast containing one-third of the daily calcium) was higher than the fraction calculated from the diet (or calcium intake over the whole day). The amount of calcium absorbed was significantly higher (P < 0.001) on the high calcium intake. Urinary excretion increased by 0.7 mmol/day, and calcium balance increased by 11.2 mmol/day on high calcium intake (Table 2Go). The increase in the amount of calcium absorbed was similar in magnitude to the amount decreased by resorption, indicating that absorbed calcium spared bone calcium on the higher calcium intake. On the low intake, 40% of calcium absorbed was retained; whereas on the higher intake, 74% of the absorbed calcium was retained.


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  		Table 2. Calcium kinetics derived from multicompartmental analysis in adolescent girls (n = 9) at two levels of calcium intake

 
Pool sizes, except for those in the intestine (compartments 8 and 9), were similar on low and high calcium intake (Fig 3Go). Bone deposition did not differ; but resorption was significantly lower, by 32%, on high calcium intake (Table 2Go). The increases in calcium retention were highest in subjects who were within 6 months of menarche and lowest in subjects more than 20 months post menarche or -10 months menarche (Fig 4Go).



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  		Figure 3. Rates of calcium metabolism (mmol/day) and pool sizes (mmol calcium) calculated by using the average parameter values shown in Fig. 1Go. The upper values are for low calcium intake and the lower values are for high intake. Note: rates differ slightly from those determined by averaging the rates calculated for each subject shown in Table 2Go.

 


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  		Figure 4. Increase in calcium balance (calculated as Vo+ minus Vo-) with higher calcium intake, for each subject shown, as a function of postmenarcheal age.

 
Biochemical measures on low and high calcium intakes are given in Table 3Go. No changes were observed in PTH, vitamin D metabolites, or IGF-1. Serum calcium decreased by 8% on high calcium intake. No changes were detected in markers of bone formation. Urinary calcium:Cr increased on high calcium intake, and there was a significant decrease in OHP:Cr, a marker of bone resorption. The other markers of bone resorption decreased, but the changes were not significant.


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  		Table 3. Effect of calcium intake on calcium retention and related biochemical measures in adolescent girls (n - 10)1

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Calcium retention in adolescents is strongly impacted by dietary calcium intake (2, 18). Few studies have investigated changes in calcium kinetics with calcium intake in adolescents, to understand how the additional intake leads to increased retention. The calcium kinetic studies reported here show that the increased retention resulted from an increase in absorbed calcium and suppression of bone resorption. These results differ from young adults in whom an increase in calcium intake from 20 to 50 mmol/day did not change bone retention, because fractional absorption decreased and endogenous excretion increased (19). However, in osteoporotic women fed 12.5 mmol calcium/day and then supplemented by 50 mmol calcium/day, bone retention increased through decreased bone resorption (20), similar to the changes observed here in young girls.

Mechanisms

The large increase in amount of calcium absorbed on the high calcium intake occurred because fractional absorption did not decrease with higher calcium intake. Net absorption in a larger sample of adolescent girls (n = 35, 12.7 ± 1.2 yr) (2) are in agreement with these results, in showing only a small change (from 0.32 to 0.28) in fractional absorption at 21.2 vs. 47.4 mmol/day intake. This result is contrary to the significant decrease in absorption with calcium intake observed in subjects 3–5 yr old (21), 8–16 yr old (22), 21–24 yr old (19), or 35–45 yr old (23). Thus, the inverse relationship between fractional absorption and intake may not hold in rapidly growing adolescents undergoing the pubertal growth phase. Also, the relationship may function only at lower calcium intakes, because a strong negative relationship was reported between fractional absorption and calcium intake less than 25 mmol/day in white girls but not at intakes greater than 25 mmol/day (24). The higher absorption reported here and previously (15) from breakfast, compared with the whole day, is probably related to the overnight fast. Birge et al. (25) reported that absorption from a 8.2-mmol calcium load was 54% after an overnight fast but was reduced to 33% when a meal was given 2.5 h before the measurement. Fractional absorption was also inversely related to the amount of calcium in the previous meal (25).

Our studies on 12 yr olds, studied on controlled intakes in a cross-over design, showed that retention was increased through suppression of bone resorption. These results differ from a cross-sectional study in girls 5–18 yr old, which showed that bone turnover increased with absorbed calcium (up to 16.2 mmol/day), with deposition increasing faster than resorption (9). The lack of change in bone formation markers and the decrease in a marker of resorption support our results, showing that bone formation does not change and that resorption suppresses with high calcium intake. O’Brien et al. (22) also reported that urinary telopeptides were lower in girls on a calcium intake of 35 mmol/day than 7 mmol/day. Two other markers of bone resorption, urinary PYR:Cr and urinary DPX:Cr, were reduced significantly in a larger sample (n = 25;12–15. yr) while on high (42–52 mmol/day), compared with low (21–34 mmol/day), calcium intakes (unpublished data).

Bone turnover and retention are known to decrease with postmenarcheal age (14, 15, 26); and as shown here and previously (2), the largest impact of calcium intake on calcium retention occurs within the first 6 months of onset of menarche. Therefore, as adolescents approach adulthood, their response to calcium intake will change, such that retention will increase less with calcium intake.

Relationship of kinetic and biochemical changes

Biochemical markers of bone turnover are predictive of Vo+ and Vo- (27). Resorption markers are sensitive to bone loss and decreases are measured over 6 h, after a 25-mmol oral calcium load (28), and increases are measured within days of initiation of bed rest or space flight (29). Changes in the diurnal rhythm of resorption markers have also been observed after 2 wk of calcium administration (30). By contrast, after 1 yr of calcium administration to older women, only bone formation markers were changed (31). We found that, in young girls, changes in markers of bone resorption were variable, ranging from -11 to -23% and were lower than the calculated change of -32% in bone resorption on the higher calcium intake. The most predictive marker of bone resorption was hydroxyproline, which decreased by 23%, which was still quite short of the 32% change in resorption measured by kinetics. Thus, biochemical markers of bone resorption were not quantitatively in agreement with each other but also underestimated changes in bone resorption in response to diet and, in most cases, were unable to show a statistically significant effect. Similarly, markers were not changed after prolonged (18 mo) dairy supplementation to girls, although bone mass increased (4). Because marker levels change significantly with stage of sexual maturity (32), some changes in markers caused by calcium intake may be masked by stage of maturity. However, the effect of stage of maturity is minimized in our study by use of within-subject comparisons over a relatively brief study period of 2 months.

We found no changes in serum PTH, vitamin D metabolites, or IGF-1. Dietary calcium influenced the amount of absorbed calcium without influencing these mediators of absorption, but the effect was to suppress bone resorption. Osteoclasts respond directly to extracellular calcium in vitro (33). Whether delivery of calcium to bone is a factor acting locally is not clear. We found decreases in total serum calcium, but this does not preclude an increase in local free calcium.

In summary, calcium intake can profoundly increase bone balance, especially close to onset of menarche. This enhanced bone retention of calcium with calcium intake in adolescent girls is attributable to increased absorption of calcium, combined with decreased bone resorption. At this period in a woman’s life, when bone turnover is at its maximum, the sum of bony resorption and dietary calcium absorption is essentially constant. Therefore, what does not come from the diet comes from the skeleton. This study lends further support to the importance of achieving adequate dietary calcium during this life stage.


   Footnotes
 
1 Funded by NIH Grants R01-AR-40553 and M01-RR-00750. Back

Received March 11, 2000.

Revised June 6, 2000.

Revised August 8, 2000.

Accepted August 20, 2000.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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B. Dibba, A. Prentice, M. Ceesay, M. Mendy, S. Darboe, D. M Stirling, T. J Cole, and E. M. Poskitt
Bone mineral contents and plasma osteocalcin concentrations of Gambian children 12 and 24 mo after the withdrawal of a calcium supplement
Am. J. Clinical Nutrition, September 1, 2002; 76(3): 681 - 686.
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