AJCN 19th International Congress of Nutrition
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American Journal of Clinical Nutrition, Vol. 84, No. 2, 414-418, August 2006
© 2006 American Society for Nutrition

ORIGINAL RESEARCH COMMUNICATION

Calcium retention in adolescent boys on a range of controlled calcium intakes1,2,3

Michelle Braun, Berdine R Martin, Mark Kern, George P McCabe, Munro Peacock, Zhen Jiang and Connie M Weaver

1 From Purdue University, West Lafayette, IN (MB, BRM, GPM, ZJ, and CMW); San Diego State University, San Diego, CA (MK); and the Indiana University School of Medicine, Indianapolis, IN (MP)

2 Supported by the National Institutes of Health (AR 40553).

3 Address reprint requests to CM Weaver, Purdue University, Foods and Nutrition, 1264 Stone Hall, 700 West State Street, West Lafayette, IN 47907-2059. E-mail: weavercm{at}purdue.edu.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: National calcium requirements in the United States for boys are based on data from girls. On average, boys develop larger skeletons than do girls, yet it is unknown whether the additional skeletal accretion in boys requires additional dietary calcium intake.

Objective: The objective was to determine calcium retention in adolescent boys in response to a range of controlled intakes and to compare the intake needed for maximal retention in boys with that needed in adolescent girls studied under the same conditions.

Design: Thirty-one boys aged 12–15 y participated in 3-wk metabolic balance studies testing a range (700–2100 mg/d) of calcium intakes in a crossover study design with a 2-wk washout period. Calcium intake was varied by using a beverage fortified with calcium citrate malate. After a 1-wk equilibration period, calcium retention was calculated as dietary calcium intake minus the calcium excreted in the feces and urine over the following 2 wk. The dietary intake at which maximal calcium retention occurred was determined by using a nonlinear regression model. The results in boys were compared with those obtained in 35 adolescent girls previously studied under the same protocol.

Results: Maximal calcium retention in boys was achieved at an intake of 1140 mg/d. Calcium retention was higher (by 171 ± 38 mg/d) in boys than in girls at all calcium intakes studied.

Conclusion: The higher calcium retention in boys than in girls was attained through higher net calcium absorption and lower urinary excretion than in girls.

Key Words: Dietary calcium requirement • calcium retention • adolescents • boys • metabolic balance


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Calcium requirements vary throughout life. The greatest needs for calcium are at times of rapid growth, the most dramatic of which—in absolute terms—is the pubertal growth spurt. Adolescent dietary calcium recommendations in North America are based on intakes aimed at optimizing skeletal calcium retention (1). The adolescent period of rapid growth requires high accretion rates of calcium, which are achieved by a high retention efficiency of dietary calcium.

In adolescents, sex differences exist in both the age at which peak calcium accretion in the skeleton occurs and in the amount of calcium accrued. On the basis of a longitudinal study of total bone mineral density measured by dual-energy X-ray absorptiometry (DXA) throughout puberty in a cohort of boys and girls, peak bone accrual rates were 407 g/y in boys and 322 g/y in girls (2). In boys, the peak bone accrual rate occurred 18 mo later than in girls (2). By the end of adolescence, boys have a higher total-body bone mineral content than do girls (3, 4). It is unknown, however, whether the development of a larger skeleton in boys requires more dietary calcium intake to optimize calcium retention or whether boys utilize dietary calcium more efficiently than do girls.

We set out to establish the dietary calcium requirements of boys by using the same approach that we previously used in girls (5). The relation between dietary calcium intake and calcium retention was studied in adolescent boys in a 21-d metabolic balance study of 2 calcium intakes ranging between 700 and 2000 mg/d in a crossover design.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Subjects
Healthy white adolescent boys were recruited from local schools. Recruitment targeted boys aged 13–15 y. A screening questionnaire was completed by all interested participants. Health status was determined by medical history questionnaire, physical examination, and blood biochemistry.

Self-assessed pubertal status was determined by Tanner stage (6) with the use of a questionnaire administered by a research coordinator. Total-body bone mineral density and bone mineral content were measured by DXA (Lunar Corp, Madison, WI). The subjects' heights and weights were measured at the time of DXA scanning with a wall stadiometer and a calibrated electronic scale, respectively, while the subjects were wearing light clothing and no shoes. Weight was measured daily throughout the study to monitor health. The study was approved by the Institutional Review Boards of Purdue University and Indiana University School of Medicine and Clarian.

Study design
The subjects lived on the Purdue University campus in university housing for two 3-wk periods of the summer (June to August) in a camp environment. An established set of protocols was used for conducting metabolic balance studies in adolescent children at research camps, including menus, activities, and laboratory procedures. Because the methods used for the boys in the current study were the same as those used for the girls in a previous study (5), data from both sexes were compared.

The subjects were studied twice: once during a relatively low dietary calcium intake and once during a relatively high calcium intake. The 3-wk balance studies were performed in a randomized order, separated by a washout period of 2 wk. The subjects were randomly assigned to receive 1 of 5 dietary calcium intakes such that the 10 dietary intakes from the lowest to the highest spanned from 693 to 1986 mg/d (Table 1Go) to bracket the threshold intake of the girls in the previous study (5).


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  		TABLE 1. Dietary calcium intakes in adolescent boys by randomly assigned group1

 
Dietary intake and analysis
Dietary intake was controlled and subjects ingested only foods prepared by the staff. A 4-d cycle menu was developed, and a composite of meals for each day was saved for analysis. All foods and beverages were prepared with deionized water and weighed to the nearest 0.1 g. The different caloric needs of the subjects were met by providing calcium-free ad libitum products, such as beverages reconstituted with deionized water and calcium-free flavored frozen treats. The subjects were not allowed to use discretionary flavor enhancers, such as salt.

The calcium intakes were varied by using a beverage fortified with calcium citrate malate at different calcium concentrations. Orange drinks fortified or unfortified with calcium citrate malate were a gift from Proctor & Gamble (Cincinnati, OH) and blended by the study staff to achieve equal volumes of appropriate calcium content. Fortified beverages were served with breakfast, lunch, and dinner. Beverage glasses containing calcium-rich fluids such as milk and juice were rinsed with deionized water, and the rinse was also consumed. A daily meal composite was frozen for the analysis of mineral content. The meal composite was prepared at the same time and to the same specifications as the meals. Diet composites were thawed, homogenized, and freeze-dried (Dura-Dry Freeze-Dryer model PAC-TC-44; FTS Systems Inc, Stone Ridge, NY) for composition analysis.

Sample collection and analysis
Subjects collected all urine and feces for the duration of each 3-wk study period. Urine was collected in acid-washed containers and pooled as 24-h collections, which ended with the collection taken on rising on the morning of each day. Urine samples were processed daily, and total urine volume was measured. The urine was acidified with concentrated hydrochloric acid (1%, by vol) and frozen at –10 °C. Acidified duplicate urine samples were thawed and diluted with 3% HNO3 for the measurement of calcium content. Fecal samples were collected in preweighed containers and immediately frozen. Fecal samples were also pooled as 24-h collections. Fecal samples pooled by 24-h collections were diluted with concentrated hydrochloric acid and ultrahigh purity water (resistivity: >16 M{Omega}) and homogenized with a stomacher (Lab-Blender 3500; Tekmar, Cincinnati, OH). Aliquots were sampled in triplicate, dried at 48 °C, ashed at 600 °C, and diluted with 3% HNO3 for the measurement of calcium. Diet and fecal samples were prepared similarly. The calcium contents in the diet and fecal and urine samples were measured by inductively coupled plasma spectrophotometry (Optical Emission Spectrometer, Optima 4300DV; Perkin-Elmer, Shelton, CT).

Compliance measures
Creatinine was used both to assess urine collection compliance based on a constant daily urinary creatinine excretion and to adjust for incomplete and overcomplete 24-h collections. Urinary creatinine was measured according to a colorimetric procedure on a Cobas-Mira Plus (Roche Diagnostic Systems, Branchburg, NJ). Corrected urinary calcium was calculated as

Formula 1(1)
Polyethylene glycol (PEG; E3350 Dow Chemical Co, Midland, MI) was used to assess fecal collection compliance. Each subject ingested 6 gelatin capsules (2 capsules with each meal) to equal 3 g PEG/d. Capsules were assembled by hand; each gelatin capsule contained 500 ± 5 mg PEG. PEG was analyzed by using a turbidimetric assay according to the method of Allen et al (7). All samples were analyzed in duplicate.

Retention calculation
Calcium retention was calculated by subtracting the sum of urinary and fecal calcium excretion from dietary calcium intake. The first week of each 3-wk study was regarded as an equilibration period to the diet. A balance period began and ended on a day on which a fecal sample was collected and included all days in between each. The sum of intake minus the sum of excretion was averaged over the time period of compliance.

Statistical analysis
Analysis of variance and regression were used to examine the effects of calcium intake, study period, and order on calcium retention, urinary calcium, and fecal calcium. These variables were modeled as a function of calcium intake by using nonlinear regression. Model building methods were used to determine an appropriate functional form to describe the nonlinear relation between calcium intake and calcium retention (8). We examined a variety of models, including some that allowed for the possibility of negative estimates of retention. This process led to a model of the form

Formula 2(2)
where Y is the mean calcium retention for a given intake, L = ß1 (1 + ß2x), and x is the calcium intake. The parameters of the model are ß0, ß1, ß2, and the SD of variation about the mean. Multiple observations of the same subjects were assumed to be correlated. This is the model that was used to analyze the girls' data (5). Details regarding the methodology for taking into account the correlation are given by Jiang (9). Model building techniques, including nonparametric regression and the analysis of residuals, were used to determine appropriate models for the inclusion of additional explanatory variables, such as sex and body size. This analytic approach led to models that included the additional variables as additive terms. The SAS mixed procedure (SAS Institute Inc, Cary, NC) was used to analyze the fecal and urinary excretion data.

For the comparison of boys and girls, models with distinct parameters were examined. An analysis of these models indicated that there were no statistically significant sex differences in the parameters ß0, ß1, and ß2. This led to a model with a linear term, g, to describe sex differences:

Formula 3(3)
where g is the sex of the subject, coded as 0 for girls and 1 for boys. Weight, height, and BMI were examined as possible variables that would explain a sex effect. To deal with the complications arising from the fact that there are several candidate variables for inclusion, a model selection algorithm, based on the residuals from the basic model and taking into account the correlation between observations from an individual, was developed (9). Statistical significance was set at P < 0.05. All statistical analyses were done by using the Statistical Analysis System (version 9.1; SAS Institute).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Thirty-one boys completed at least one 3-wk study period and 26 boys completed 2 periods (Table 1Go). The characteristics of the subjects are shown in Table 2Go. Subjects were in steady state after a 1-wk equilibration period, as evidenced by constant calcium to PEG ratios of excretion in the feces. Neither the month in which the balance study was conducted nor the treatment order of the high- and low-calcium treatments had a significant effect on calcium retention. No significant difference (P > 0.05) between creatinine-corrected and -uncorrected urinary calcium excretion was found, which indicated good compliance of the subjects with the urine collections and consistent timing of the 24-h pools.


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  		TABLE 2. Characteristics of subjects1

 
Smoothed curves describing the dependence of urinary calcium and fecal calcium excretion on calcium intake are shown in Figure 1Go. The relation for urinary calcium is approximately constant (P > 0.05 for the test of zero slope). The relation between fecal calcium and intake depicted in Figure 1Go is approximately linear (b = 0.47 ± 0.11, P < 0.001) up to an intake of 1500 mg/d. Above this value, the relation is also approximately linear with a greater slope (b = 1.34 ± 0.29, P < 0.001). The difference between the slopes is statistically significant (t = 2.36, P = 0.027). The 95% CI for the slope for intakes >1500 mg/d is (0.76, 1.91). The data, therefore, are compatible with a slope of 1, which implies that an increase in calcium intake of 1 mg/d is associated with an increase in fecal calcium excretion of 1 mg/d. The sharp increase in fecal calcium excretion at higher calcium intakes led to a plateau in calcium retention. This is illustrated in the plot of the relation between calcium intake and percentage maximal calcium retention (Figure 2Go).


Figure 1
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  		FIGURE 1.. Relation between urinary and fecal calcium excretion and dietary calcium intake in adolescent boys. The relation for fecal calcium was approximately linear (b = 0.47 ± 0.11, P < 0.001) up to an intake of 1500 mg/d. Above this value the relation was also approximately linear with a greater slope (b = 1.34 ± 0.29, P < 0.001). The difference between the slopes was statistically significant (t = 2.36, P = 0.027).

 

Figure 2
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  		FIGURE 2.. Maximal calcium retention as a function of calcium intake (mean and 95% CI) in adolescent boys.

 
Thirty-five previously studied girls completed at least one 3-wk study period under the same conditions as in the current study (5). Differences in measures of body size were observed between the boys and the girls. Boys weighed more than girls (64.9 ± 18.8 and 53.3 ± 9.9 kg, respectively; P < 0.002) and boys were taller (165.7 ± 7.8 and 157.4 ± 5.7 cm; P < 0.001). The mean Tanner stage of the girls was 3.8 ± 0.8 and that of the boys was 3.5 ± 1.1 (P > 0.05). The boys were 13.2 ± 0.7 y of age, and the girls were 13.6 ± 0.8 y of age.

The shapes of the curves describing the relation between calcium retention and calcium intake for boys and girls were not distinguishable, but the level of the curves varied with sex. The fitted model for the sex difference in calcium retention was as follows:

Formula 4(4)
where x is calcium intake.

Calcium retention was higher in the boys than in the girls, by an average of 171 ± 38 mg Ca/d, and the difference was consistent across intakes (Figure 3Go). The addition of measures of body size to the model did not eliminate the sex differences.


Figure 3
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  		FIGURE 3.. Scatterplot and predicted curves of calcium retention as a function of calcium intake in boys and girls.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Data from balance studies suggest that maximal net calcium retention is reached with calcium intakes between 1200 and 1500 mg/d for most healthy girls aged 9–18 y (5, 10–15). The calcium intake at which maximal skeletal calcium retention occurs is the basis for dietary calcium intake recommendations. No statistically significant increase in calcium retention at calcium intakes >1300 mg/d was previously reported in pubertal girls studied under the same conditions as used in the present study (5). In the present study of pubertal boys matched for sexual maturity to these girls, the lowest intake that permitted achievement of the maximal calcium accretion of 628.9 mg/d within the 95% CI of the estimate was 1140 mg/d. The calcium intakes for maximal retention were not significantly different between sexes. However, calcium retention was higher in the boys than in the girls, and the difference was consistent across intakes. Maximal retention curves for boys and girls were parallel. Therefore, the calcium recommendation set by the Institute of Medicine (1) for North American adolescents aged 9–18 y, which is based primarily on data from girls, can also be applied to boys.

The usual mean intake of adolescent boys and girls is 1000 and 900 mg Ca/d, respectively, according to published dietary surveys (16, 17). Application of the nonlinear model developed in the present study allowed us to predict calcium retention at different calcium intakes for each sex. Calcium retention in girls is predicted to double, from 158 to 316 mg Ca/d, if the usual intake of 900 mg Ca/d is increased to the recommended intake of 1300 mg Ca/d (1). The increase in calcium retention in boys is also predicted to be 158 mg/d if the calcium intake is increased from 900 to 1300 mg /d, but this represents only a 32% increase because of the higher calcium retention efficiency at an intake of 900 mg Ca/d in boys.

Bailey et al (2) estimated calcium accretion using longitudinal bone densitometry measurements. Daily calcium retention during the adolescent growth spurt was estimated to be 359 mg/d for boys (199–574 mg/d) and 284 mg/d for girls (171–459 mg/d). Mean (±SD) calcium intakes, estimated by dietary recall, were 1140 ± 392 mg/d for boys and 1113 ± 378 mg/d for girls. These estimates of calcium retention are lower than those measured in the present study, which was conducted under controlled conditions and using optimal calcium intakes. Also, the sex difference of 75 mg Ca/d was less than our estimate of 177 mg Ca/d.

Urinary calcium excretion was higher in the girls than in the boys at the same calcium intake. Abrams et al (18) also reported that urinary calcium excretion was greater in girls (93.9 ± 43.8 mg/d) than in boys (66.9 ± 26.2 mg/d). Calcium intake accounted for 0.2% of the variance in urinary calcium excretion in boys, in contrast with 6% of the variance in urinary calcium in girls (5).

Compared with the girls, who were studied during pubertal growth, the boys had higher calcium retention at all intakes. The addition of measures of body size into the model did not eliminate the sex differences observed in the current study. This higher calcium retention was achieved through lower urinary output and higher net calcium absorption in the boys. Ongoing stable-isotope kinetic and biochemical analyses in boys will provide further insight into sex differences in calcium metabolism. Sex steroid hormones, but not calciotropic hormones, were different by sex in a large cohort of Indiana children (3), which makes them more likely candidates of regulators of calcium and bone metabolism. The calcium retention curve for boys, as a function of calcium intake, was higher but parallel to the curve for girls. Thus, boys utilize calcium more efficiently than do girls and do not require higher calcium intakes to achieve their larger skeletons.


   ACKNOWLEDGMENTS
 
CMW, GPM, BRM, and MP were responsible for the study design. MB, BRM, MK, and CMW were responsible for conducting the study and the data collection. MB, GPM, and ZJ were responsible the for data analysis. All authors were responsible for preparing the manuscript. None of the authors had a personal or financial conflict of interest.

We thank the staff of Camp Calcium and the study subjects.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Institute of Medicine. DRI: Dietary Reference Intakes for calcium, phosphorus, magnesium, vitamin D, and fluoride. Washington, DC: National Academy Press, 1997.
  2. Bailey DA, Martin AD, McKay HA, Whiting S, Mirwald R. Calcium accretion in girls and boys during puberty: a longitudinal analysis. J Bone Miner Res 2000; 15: 2245–50.[Medline]
  3. Hui SL, DiMeglio LA, Longcope C, et al. Difference in bone mass between black and white American children: attributable to body build, sex hormone levels, or bone turnover? J Clin Endocrin Metab 2003; 88: 642–9.[Abstract/Free Full Text]
  4. Horlick M, Thornton J, Wang J, Levine LS, Fedun B, Pierson RN Jr. Bone mineral in prepubertal children: gender and ethnicity. J Bone Miner Res 2000; 15: 1393–7.[Medline]
  5. Jackman LA, Millane SS, Martin BR, et al. Calcium retention in relation to calcium intake and postmenarcheal age in adolescent females. Am J Clin Nutr 1997; 66: 327–33.[Abstract/Free Full Text]
  6. Tanner J. Growth at adolescence. 2nd ed. Oxford, United Kingdom: Blackwell, 1962.
  7. Allen LH, Raynolds WL, Margen S. Polyethylene glycol as a quantitative fecal marker in human nutrition experiments. Am J Clin Nutr 1979; 32: 427–40.[Abstract/Free Full Text]
  8. Neter J, Kutner M, Nachtsheim CJ, Wasserman W. Applied linear statistical models. 4th ed. Chicago, IL: Richard Irwin, 1996.
  9. Jiang Z. Estimation of parameters in non-linear models with dependent data Statistics. West Lafayette, IN: Purdue University, 2004.
  10. Matkovic V, Fontana D, Tominac C, Goel P, Chesnut CH III. Factors that influence peak bone mass formation: a study of calcium balance and the inheritance of bone mass in adolescent females. Am J Clin Nutr 1990; 52: 878–88.[Abstract/Free Full Text]
  11. Weaver CM, Martin BR, Plawecki KL, Peacock M, Wood OB, Smith DL, Wastney ME. Differences in calcium-metabolism between adolescent and adult females. Am J Clin Nutr 1995; 61: 577–81.[Abstract]
  12. Weaver CM, Peacock M, Martin BR, Plawecki KL, McCabe G. Calcium retention estimated from indicators of skeletal status in adolescent girls and young women. Am J Clin Nutr 1996; 64: 67–70.[Abstract/Free Full Text]
  13. Wastney M, Ng J, Smith D, Martin B, Peacock M, Weaver C. Differences in calcium kinetics between adolescent girls and young women. Am J Physiol 1996; 271: R208–16.
  14. Matkovic V, Heaney R. Calcium balance during human growth: evidence for threshold behavior. Am J Clin Nutr 1992; 55: 992–6.[Abstract/Free Full Text]
  15. Abrams S, Stuff J. Calcium metabolism in girls: current dietary intakes lead to low rates of calcium absorption and retention during puberty. Am J Clin Nutr 1994; 60: 739–43.[Abstract/Free Full Text]
  16. Bialostosky K, Wright JD, Kennedy-Stephenson J, McDowell M, Johnson CL. Dietary intake of macronutrients, micronutrients, and other dietary constituents and other dietary constituents: United States, 1988-1994. Vital Health Stat 11 2002.
  17. Ervin R, Wang CY, Wright JD, Kennedy-Stephenson J. Dietary intake of selected minerals for the United States population: 1999–2000. Advance Data from Vital and Health Statistics. Hyattsville, MD: National Center for Health Statistics, 2004: 341.
  18. Abrams SA, Grusak MA, Stuff J, Obrien KO. Calcium and magnesium balance in 9–14-y-old children. Am J Clin Nutr 1997; 66: 1172–77.[Abstract/Free Full Text]
Received for publication November 2, 2005. Accepted for publication March 30, 2006.




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