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American Journal of Clinical Nutrition, Vol. 80, No. 5, 1422-1427, November 2004
© 2004 American Society for Clinical Nutrition

ORIGINAL RESEARCH COMMUNICATION

Effect of habitual dietary calcium intake on calcium supplementation in 12–14-y-old girls1,2,3

Christian Mølgaard, Birthe L Thomsen and Kim F Michaelsen

1 From the Department of Human Nutrition and Centre for Advanced Food Studies, The Royal Veterinary and Agricultural University, Frederiksberg, Denmark (CM and KFM), and the Department of Biostatistics, University of Copenhagen, Denmark (now the Department of Cancer Epidemiology, Danish Cancer Society) (BLT)

2 Supported by FØTEK (Food Technology Research and Development Programme) and the Danish Dairy Research Foundation.

3 Reprints not available. Address correspondence to C Mølgaard, Department of Human Nutrition, Rolighedsvej 30, DK-1958 Frederiksberg C, Denmark. E-mail: cm{at}kvl.dk.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: There is no agreement on how much calcium young girls need for optimal bone mineralization.

Objective: We evaluated whether the effect of calcium supplementation on whole-body bone mineral accretion depends on habitual calcium intake.

Design: This was a randomized, double-blind, placebo-controlled, 1-y calcium intervention study of girls aged 12–14 y selected from a larger group according to habitual calcium intake: subgroup A (n = 60) habitually consumed 1000–1307 mg/d (40th–60th percentile), and subgroup B (n = 53) habitually consumed <713 mg/d (<20th percentile). The girls from each subgroup were randomly assigned to receive either 500 mg Ca/d or placebo. Whole-body bone mineral content (BMC), bone area (BA), bone mineral density (BMD), and BMC adjusted for BA, height, and weight (size-adjusted BMC) were measured at baseline and after 1 y.

Results: There was no significant effect modification of baseline habitual calcium intake on the relation between calcium supplementation and height, weight, BMC, size-adjusted BMC, BA, BMD, or alkaline phosphatase. Calcium supplementation had an effect on BMD (0.8%; P = 0.049) and tended to show signs of an effect on size-adjusted BMC (0.5%; P = 0.08).

Conclusion: A modest effect of calcium supplementation on BMD was shown. However, the effect was independent of habitual calcium intake.

Key Words: Young girls • bone mineral content • calcium intervention • habitual calcium intake


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Prevention of osteoporosis in the elderly should start early in life because peak bone mass is a major determinant of bone mass later in life (1, 2). Genetic influence accounts for 70–80% of the variation in bone mass (3, 4); still, ≥20% may be due to environmental factors such as nutrition and physical activity. Lifestyle factors during growth are potentially important for fracture risk later in life (5), because a reduction of 10% in bone mass in the elderly is associated with at least a doubling of fracture risk (6).

The results of observational studies of the association between calcium intake and bone mass during growth are conflicting (7-14). However, several calcium intervention studies have shown an effect on bone mineral accretion during childhood and adolescence (15-18). The effect of calcium supplementation on bone accretion may depend on habitual dietary calcium intake, so that supplementation mainly affects individuals with low habitual intakes (19). To our knowledge, however, no published intervention studies in which the participants were selected according to their habitual calcium intake have analyzed the relation between habitual calcium intake and the effect of calcium supplementation on bone accretion. The present randomized double-blinded intervention study of young girls aged 12–14 y was designed to evaluate the hypothesis that the effect of a relatively small supplement of calcium (500 mg/d) on bone accretion would depend on habitual calcium intake.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Subjects
All girls (n = 1213) aged 12 y ± 6 mo from the Frederiksberg and Copenhagen municipalities with Danish names according to lists from the National Central Person Register were mailed a food-frequency questionnaire (FFQ) for recording of dietary calcium intake (20). The FFQ was identical to that used later during the intervention. The respondents were asked to fill in the FFQ and return it together with information on their health, weight, and height. Six hundred eight girls (50%) returned the FFQ. Calcium intake was estimated from the FFQ. A few girls did not report weight and height. Median (10th, 90th percentile) calcium intake was 1161 (543, 2129) mg/d.

Two groups (A and B) were then selected according to dietary calcium intake. Group A had intakes between the 40th and 60th percentiles of the group of girls (1000–1304 mg/d; n = 121), and group B had intakes below the 20th percentile (<713 mg/d; n = 120). Self-reported median (10th, 90th percentile) weight and height were 45.0 (36.0, 56.0) kg and 159.0 (148.0, 167.0) cm, respectively, for group A (n = 113) and 44.0 (34.0, 56.0) kg and 158.0 (146.0, 165.0) cm, respectively, for group B (n = 109). After exclusion because of nonwhite ethnic origin, abnormal weight-for-height [less than the third or greater than the 97th percentile (21)], or diseases or intake of drugs with a potential effect on bones, 105 (A) and 83 (B) girls were eligible for the present study. From groups A and B, 60 and 53 girls, respectively, agreed to participate. Self-reported median (10th, 90th percentile) weight and height for the final groups were 45.0 (36.0, 57.0) kg and 159.0 (149.8, 167.0) cm, respectively, for group A (n = 57) and 45.0 (35.0, 56.1) kg and 158.0 (145.9, 167.1) cm, respectively, for group B (n = 48). The study was approved by the Ethics Committee for Copenhagen and Frederiksberg [J.nr. (KF) 01–033/95].

Design
Girls from each of the 2 groups (A and B) were randomly assigned to receive either a daily calcium supplement of 500 mg given as calcium carbonate salt (group C) or a placebo tablet containing microcrystalline cellulose (group P) during the first year. In the second year, the data for which are not reported here, all participants received a supplement of 500 mg Ca/d. Both the calcium supplement containing 250 mg Ca per tablet and the placebo were chewable (both manufactured by Almega A/S, Ringsted, Denmark). The girls were asked to consume 2 tablets daily together with their evening meal. The tablets were delivered to the subject's private address every third month, and uningested tablets from the previous period were collected. Random assignment of the 113 girls gave the following numbers in each group at the start: group AC, 30; group AP, 30; group BC, 26; and group BP, 27. One hundred eleven completed the first year.

At baseline and after 1 y, the following measurements were made: height, weight, evaluation of pubertal development, dual-energy X-ray absorptiometry (DXA) scan, serum alkaline phosphatase, serum 25-hydroxyvitamin D, calcium intake by FFQ, and physical activity by questionnaire. The girls were enrolled in the study during November to June. Compliance was evaluated by tablet counting and was expressed as a percentage: (number of tablets eaten/number of tablets that should have been eaten) x 100.

Anthropometry and puberty
Height and weight were measured before each DXA scan. Height was determined to the nearest 1 mm by using a stadiometer. Weight was measured to the nearest 0.1 kg by using a digital electronic scale. Subjects wore only underpants and a cotton T-shirt when weighed. Pubertal development was evaluated as menarcheal status by recording whether the girl had had menarche or not. Menarcheal status (+/–) was recorded at both examinations. Most of the girls had had menarche before the 1-y examination, so we used menarcheal status at baseline as the indicator of pubertal development in the analyses.

Bone mineral assessment
Whole-body bone mineral content (BMC) measured in grams hydroxyapatite, whole-body bone size expressed as anterior-posterior projected bone area (BA) measured in cm2, and bone mineral density (BMD = BMC/BA, in g/cm2) were determined by DXA with a Hologic 1000/W scanner (Hologic Inc, Waltham, MA). For analysis, software version 5.61 was used. The subjects wore only underpants and a cotton T-shirt during the scan. For quality control, a spine phantom was scanned daily. The CVs for these BMC and BA measurements on the spine phantom over a period of 2 y (n = 358) were 0.37% and 0.28%, respectively. In adults examined over an 8-wk interval, reproducibility expressed as CV% was 1.6%, 2.2%, and 0.9% for whole-body BMC, BA, and BMD, respectively (D Hansen, A Astrup, unpublished observations, 1998). The entrance radiation dose was 15 µSv, with an effective dose per DXA scan not >10 µSv, equal to about one day's background radiation in Denmark.

Calcium intake and physical activity
Calcium intake was estimated by using an FFQ with 88 items that queried about usual daily intake (in mg/d) during the past month. The FFQ was previously validated against food records, and its reproducibility and validity have previously been described in detail (20).

Physical activity was recorded by using a 24-h recall questionnaire (habitual activity estimation scale; 22) as described previously (14). In short, the scale records the hours per day spent at each of 4 activity levels: supine position (I), sitting (II), walking (III), and running (IV). Hours per day spent on high activity (level IV) was used as a measurement for activity level, as described earlier (14).

Blood analyses
Blood samples were collected at baseline and after 1 y. Total alkaline phosphatase (in U/L) was measured by COBAS MIRA (Boehringer Mannheim, Mannheim, Germany). 25-Hydroxyvitamin D (in nmol/L) was analyzed by radioimmunoassay (25-hydroxyvitamin D 125I RIA kit; DiaSorin, Stillwater, MN).

Statistical methods
Statistical analyses were performed by using the statistical software package SAS 6.12 for PC (SAS Institute Inc, Cary, NC). Descriptive measurements are reported as medians (10th, 90th percentile) unless stated otherwise. Statistical analyses were performed by analysis of covariance. All continuous variables except age were converted to the natural logarithm before analyses. Log transformation facilitates exploration of power relations between continuous variables and multiplicative effects of discrete variables (18, 23, 24). The baseline value was included as a covariate in all of the analyses so that all results relate to accretion in the response variables. The chosen model estimates multiplicative associations. However, the comparisons of the 2 treatment groups are presented as percentage differences, as used by Dibba et al (18). Thus, the effect of 1 y of calcium supplementation is presented in the table as the back-transformed expected value with calcium supplementation after 1 y subtracted by the back-transformed expected value under placebo treatment after 1 y. This difference measured in percent of the back-transformed expected value under placebo treatment may be obtained by subtraction of 1 from the exponential transformation of the parameter, followed by multiplication by 100. For small values, this transformed value is close to the untransformed value multiplied by 100.

To examine the influence of the calcium supplement on BMC adjusted for bone and body size (size-adjusted BMC), BA, height, and weight were included as independent variables in the analyses as recommended by Prentice and others (18, 23, 24). That is, we included the mean and difference of baseline and first-year values after conversion to the natural logarithm (18).

Interaction between prestudy calcium intake and the intervention was tested to evaluate whether the effect of 1 y of calcium supplementation depended on prestudy habitual calcium intake. To analyze whether the effect of calcium supplementation was related to menarcheal status, we tested an interaction term between the intervention group and menarcheal status at baseline. P values < 0.05 were considered significant and values < 0.1 as indicating a tendency. Significance was assessed by the F test statistic.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The subjects' characteristics at baseline and after 1 y according to habitual calcium intake group (A, B) and intervention group (P, C) are shown in Table 1Go. There were no significant differences between the intervention groups at baseline. The subjects' calcium intake, numbers of hours per day of high activity level (IV), serum 25-hydroxyvitamin D concentrations, and serum alkaline phosphatase concentrations at baseline and after 1 y according to habitual calcium intake group (A, B) and intervention group (P, C) are shown in Table 2Go. There were no significant differences between the P and C groups at baseline.


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  		TABLE 1. Clinical characteristics at baseline and after 1 y in the average habitual calcium intake group (A) and the low habitual calcium intake group (B)1

 

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  		TABLE 2. Dietary calcium intake, total calcium intake including the supplement, hours per day performing a high level of physical activity, serum 25-hydroxyvitamin D, and serum alkaline phosphatase at baseline and after 1 y in the average habitual calcium intake group (A) and the low habitual calcium intake group (B) 1

 
Median compliance was 86% for the first year (430 mg Ca/d for the calcium-supplemented groups), and there were no significant differences among the 4 groups (one-way ANOVA, P = 0.44). The changes in height, weight, BMC, BA, BMD, alkaline phosphatase, and size-adjusted BMC are shown in Table 3Go. There was no significant interaction between habitual calcium intake (A-B) and the intervention (C-P) in the analyses of height, weight, BMC, size-adjusted BMC, BA, BMD, or alkaline phosphatase (all P > 0.15). When groups A and B were analyzed together, there was a significant effect of the intervention on BMD (0.8%; 95% CI: 0.01%, 1.54%; P = 0.049) and a tendency toward an effect on size-adjusted BMC (0.5%; 95% CI: –0.06%, 1.15%; P = 0.08).


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  		TABLE 3. Change in height, weight, bone measurements, and alkaline phosphatase during the first year of intervention in the average habitual calcium intake group (A) and the low habitual calcium intake group (B)1

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In the present study, we found no clear evidence that baseline habitual calcium intake influences the effect of calcium supplementation on bone accretion. When the low and average habitual intake groups were combined, we found a moderate (0.8%) effect of 1 y of calcium supplementation on whole-body BMD and a tendency toward a moderate effect (0.5%) on size-adjusted BMC.

As in other studies (16, 25), the present study had relatively few participants. Thus, although the study was specifically designed to obtain a clear difference in habitual calcium intake between the 2 groups, it had limited statistical power. To increase the power to detect a possible relation between habitual calcium intake and the effect of calcium supplementation, a larger sample size and a larger difference in habitual calcium intake could be relevant.

Calcium intake and bone status
The results of observational studies have been inconsistent: some studies have shown a positive association between calcium intake and BMD or BMC (7, 8), but most studies have found no relation (9-12, 26). A few longitudinal studies examined the relation between habitual dietary calcium intake and BMC accretion. Gunnes and Lehmann (27) found that at high activity levels a concomitantly high calcium intake is likely to additionally increase trabecular BMD gain in children <11 y of age. A longitudinal study with children <18 mo of age also found an association between calcium intake and BMC accretion (28). In a study of children aged 5–19 y, an association between size-adjusted BMC and an increase in habitual calcium intake was seen, but only in boys (14).

Calcium intervention studies have shown an effect on bone mineral accretion during the intervention (15-19, 29). The intervention studies used different calcium salts, such as carbonate (18, 29), citrate malate (15, 16), or a combination of salts (17), with no obvious differences in effects between the different calcium salts. Two studies using milk (25) or calcium phosphate extracted from milk (19) showed an effect on BMC, BMD, and bone size, but this could have been due to milk components other than calcium.

When we combined the average and low habitual calcium intake groups in our study, we found a greater increase in BMD and a tendency toward a greater increase in size-adjusted BMC in the supplementation group during the 1 y of intervention. The modest effect may have been due to the relatively low supplementation dose (median of 430 mg/d) in our study compared with that used in other studies (15, 17-19). However, 2 other studies with a low supplementation dose also found an effect (16, 29). Lloyd et al (16) found a significant effect of 354 mg Ca/d on both lumbar and whole-body BMD and BMC in a group of 12-y-old girls with an average habitual calcium intake of {approx}1000 mg/d.

Effect of habitual calcium intake
The present study was designed to analyze whether habitual calcium intake influences the effect of calcium supplementation on bone accretion. We found no clear evidence of a significant relation between habitual calcium intake and the effect of supplementation. However, the difference between the supplemented group and the placebo group was larger in the group with low habitual calcium intake (group B) than in the group with average habitual calcium intake (group A) for BMC, BA, and BMD (Table 3Go), which agrees with a higher effect of extra calcium in persons with low habitual calcium intakes. The lack of relation between habitual calcium intake and the effect of supplementation agrees with the results of other studies that did not find an association between baseline calcium intake and the effect of calcium supplementation on bone accretion despite higher calcium supplementation doses (15, 18). However, one study found that the effect of milk calcium phosphate supplementation was highest in the group with a habitual calcium intake below the median (<855 mg/d) (19).

We were surprised to find that the effect of extra calcium in the group with low habitual calcium intake (mean intake of 631 mg/d) was not larger. The reason for this may be that average dietary calcium intake in this group was not very low, and average 25-hydroxyvitamin D was close to 30 nmol/L, indicating no serious vitamin D deficiency in these children (30). Dibba et al (18) did not find a higher response to a large calcium supplementation dose (714 mg/d) in Gambian children with a low customary calcium intake ({approx}350 mg/d) than in children in other studies with higher habitual calcium intakes. An explanation could be that the effect on BMD or BMC of an increase in calcium intake through a supplement is mainly due to a reduction in the remodeling space in response to a reduction in bone turnover (31). The larger absolute fall in total alkaline phosphatase in the supplemented group BC than in the placebo group BP during the first year (t test, P = 0.01) may indicate a larger fall in bone turnover in the supplemented group despite no significant difference in percentage change (Table 3Go).

Conclusion
The modest response to extra calcium in our study may indicate that the level of calcium intake is not a major determinant of bone status among healthy Danish girls with normal vitamin D status. Thus, the results of the present study do not indicate a need for change in the Nordic recommendation of 900 mg Ca/d for girls during puberty. However, whether a calcium supplement during childhood results in a higher peak bone mass can only be shown in longitudinal studies in which extra calcium is given over many years.


   ACKNOWLEDGMENTS
 
We are grateful to Birgitte Hermansen for carrying out most of the practical work in the study.

CM and KFM designed the study. CM was responsible for the collection of data, analysis of data, and writing of the manuscript. BLT supervised the statistical analysis. All authors participated in the discussion of the results and commented on the manuscript. None of the authors had any financial or personal interest in the company sponsoring the research project.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Received for publication April 8, 2003. Accepted for publication June 21, 2004.




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