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Original Research Communications |
1 From MRC Keneba, The Gambia, and MRC Human Nutrition Research (formerly MRC Dunn Nutritional Laboratory), Cambridge, United Kingdom.
2 Shire Pharmaceuticals and Nycomed Pharma donated the calcium and placebo tablets.
3 Address reprint requests to A Prentice, MRC Human Nutrition Research, Downham's Lane, Milton Road, Cambridge CB4 1XJ, United Kingdom. E-mail: ann.prentice{at}mrc-hnr.cam.ac.uk.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Objective: We investigated the effect of a calcium supplement on bone mineral accretion in rural Gambian children.
Design: A randomized, double-blind, placebo-controlled study was conducted in 160 children (80 boys, 80 girls) aged 8.3–11.9 y. Bone mineral content (BMC), bone mineral density (BMD), and BMC adjusted for bone width, body weight, and height (size-adjusted BMC) were measured at the midshaft and distal radius. Each child received either 1000 mg Ca/d (as calcium carbonate) or a placebo 5 d/wk for 12 mo. Supplementation increased calcium intake from 342 to 1056 mg/d (8.6 to 26.4 mmol/d).
Results: Calcium supplementation resulted in a higher BMC, BMD, and size-adjusted BMC (
difference ± SE): midshaft radius—BMC (3.0 ± 1.4%; P = 0.034), BMD (4.5 ± 0.9%; P 
0.0001), and size-adjusted BMC (4.6 ± 0.9%; P 0.0001); distal radius—BMC (8.4 ± 3.2%; P = 0.009), BMD (7.0 ± 2.7%; P = 0.011), and size-adjusted BMC (5.5 ± 2.7%; P = 0.042). Supplementation had no significant effect on height, weight, or bone width at the midshaft radius or distal radius. At the end of the study, the calcium group had a significantly lower mean plasma osteocalcin concentration than the placebo group after adjustment for baseline concentration, sex, and pubertal status (-21.9 ± 6.5%; P = 0.001).
Conclusions: Increased calcium intake resulted in increased bone mineral status, possibly in association with a decreased bone remodeling space. Further studies are needed to determine whether an increased calcium intake has long-term benefits in Gambian children.
Key Words: Bone mineral accretion • calcium • children • Gambia • osteocalcin • single-photon absorptiometry
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The mean dietary calcium intake of Gambian children is 
300 mg/d (9), about one-fourth to one-third of US (10) and British (11) recommendations. Children in rural areas of The Gambia have poor growth, delayed puberty, and a low bone mineral status compared with British and American children (9, 12). An intake of 300 mg Ca/d is close to the theoretical peak rate for bone mineral accretion during childhood and adolescence, even without accounting for incomplete absorption (9). Therefore, it is plausible that the low calcium supply in Gambian children may contribute to their poor growth performance and bone mineralization.
The aim of this study was to examine whether an increase in calcium intake to close to recommended amounts would improve bone mineral acquisition in 8–12-y-old Gambian children. This age group was chosen because most would not have reached puberty and some studies have indicated that the effect of calcium supplementation is confined to prepubertal children, although this finding is not universal (2–4, 6, 7). Bone width and body size were monitored and plasma osteocalcin concentrations, a marker of bone formation rate, were quantified to provide an insight into the mechanism of action and to investigate whether calcium supplementation would decrease bone remodeling space, resulting in a reversible increase in bone mineral at skeletal surfaces, rather than promote bone growth (2, 13–15).
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Calcium supplementation
Subjects were stratified by sex and randomly assigned to receive a calcium supplement or placebo. The randomization procedure was conducted by a member of the staff in Cambridge who was otherwise not involved in the study. The subjects and the field and laboratory staff remained unaware of the assignments throughout the study. Four children started the study each week to allow recruitment to be spread over one calendar year. All measurements in each subject were completed within a 7-d period. Assignment to group was by a randomized permuted block of 4 to ensure that an equal number of subjects was allocated to the calcium and placebo groups each week, to minimize the potential for seasonal confounding.
The calcium supplement consisted of 2 chewable calcium carbonate tablets (Calcichew; Shire Pharmaceuticals Ltd, Andover, United Kingdom and Nycomed Pharma AS, Oslo) containing 500 mg (12.5 mmol) elemental Ca/tablet. The placebo consisted of 2 tablets of similar shape, taste, and texture, produced by the manufacturer of the calcium tablets. Each subject received either the calcium supplement or the placebo for 5 d each week for 12 mo, starting the week after baseline measurements were taken. The tablets were dispensed to the subjects at a centrally located building in the village and were consumed under strict supervision. To achieve regular attendance, a youth club was organized every weekday evening. For children who were unable to attend the youth club for any reason, tablets were dispensed at the children's homes by the fieldworkers on the same day.
The supplement was consumed in the early evening, between 1700 and 1900. This allowed the tablets to be administered between lunch (generally between 1400 and 1500) and dinner (2030) to minimize possible interference with absorption of other minerals, such as iron and zinc. During the fasting month of Ramadan, tablets were consumed later in the evening, immediately after the subjects had broken fast but before the main meal was eaten. Tablets that were missed because of illness or absence from the village were consumed on weekends; the dose remained at 1000 mg/d. The tablets were well accepted, there were no reports of adverse side effects, and the overall compliance for each child was 100%. Thus, by the end of the 12-mo supplementation period, every child had consumed all the tablets that had been assigned to him or her at the start of the study.
Bone mineral status
Measurements of bone mineral content (BMC; g/cm), bone width (BW; cm), and bone mineral density (BMD; g/cm2) at the midshaft and distal radius of the left arm were made by using single-photon absorptiometry (Lunar SP2 scanner; Lunar Radiation Corporation, Madison, WI). Baseline measurements were conducted during the week before supplementation began. Outcome measurements were made after 12 mo ( ± SD: 385 ± 41 d), during the week before the supplement was withdrawn. The duration of this period was similar in the 2 groups (calcium group: 387 ± 28 d; placebo group: 388 ± 28 d).
The midshaft radius on the ulna was located by measuring the distance between the midpoint of the ulnar styloid process and the proximal edge of the olecranon and marking the position that was one-third of this length from the ulnar styloid process. Three transverse scans were made at the same position and the mean was recorded. The wrist measurement was made at the 5-mm distal site, defined as the site where the distance between the radius and ulna is 5 mm. This site was located by performing a rectilinear scan with a step distance of 1.5 mm and using the value for which the interosseous distance was closest to 5 mm but between 4 and 6 mm.
The instrument was calibrated daily, and long-term stability was assessed regularly by using phantoms. The CVs over the study period for BMC, BW, and BMD were 1.11%, 0.94%, and 0.82%, respectively, for the small phantom (BMC = 0.374 g/cm) and 0.52%, 0.41%, and 0.53%, respectively, for the large phantom (BMC = 1.196 g/cm), indicating satisfactory instrument stability with no sign of drift.
Dietary calcium intake
Dietary calcium intake was measured during the week of baseline measurements. The assessment was made by using a direct-weighing method over 2 d (16). Each subject was visited by a fieldworker before and after each meal and on several other occasions during the measurement period. All food items consumed and any leftovers were weighed and recipes for all dishes were recorded. Consumption of snacks during and between meals was determined by recall at the next visit. Computation of nutrient intakes was carried out using GAMBIAN DIDO and MW1N4 software programs (17) based on McCance and Widdowson's food composition data (18), supplemented by information on the composition of Gambian foods (19). This additional information had been obtained by analyzing raw ingredients and cooked dishes and accounting for food items that were rich in calcium but were either eaten in small quantities or infrequently, such as certain vegetables and small fish bones (19). Calcium from drinking water was not quantified because the calcium concentration of Keneba water is low (<0.25 mmol/L, or <10 mg/L) (19).
The diet in Keneba is based on groundnuts, cereals, fish, and vegetables and is known to be deficient in many nutrients (9, 20). There were no significant differences in dietary patterns or nutrient intakes between the calcium and placebo groups.
Anthropometry and pubertal status
Anthropometry and pubertal stage assessments were conducted at the beginning and end of the study. Each subject was weighed to the nearest 0.1 kg while wearing light clothing and no shoes. Standing height of subjects without shoes was recorded to the nearest 0.1 cm. Pubertal status was assessed according to Tanner staging (21). The pubertal status of the girls was based on breast and pubic hair development and the assessment was conducted by a female pediatric consultant physician (EMEP). The pubertal status of the boys was assessed by the principal investigator (BD) and was based on genital and pubic hair development.
Plasma osteocalcin
Blood was collected after an overnight fast in the week before and 12 mo after supplementation began, before the supplement was withdrawn. The sample was anticoagulated with lithium heparin, kept cool, separated, frozen within 45 min, and transported on dry ice to Cambridge. An unavoidable delay during transportation resulted in the thawing of samples from 62 subjects, precluding their analysis. Results are presented here only for those subjects who had osteocalcin measurements made at both baseline and at the end of the 12-mo supplementation period (n = 49 in the calcium group and n = 49 in the placebo group). Intact osteocalcin was quantified by using an immunoradiometric assay (N-TACT Osteocalcin; INCStar Corporation, Stillwater, MN) that had a between-run precision of 6% during the study period for a control sample, measured in duplicate, with a concentration of 26 µg/L. The vitamin D status of all subjects was within the normal range, as indicated by a plasma 25-hydroxyvitamin D concentration >25 nmol/L.
Statistical analysis
Descriptive statistics are reported as means ± SDs and differences ± SEs for all variables, unless otherwise stated. Statistical analysis was performed by using analysis of variance, analysis of covariance, and multiple regression analysis (LINEAR MODEL SOFTWARE, DATADESK 4.1; Data Description Inc, Ithaca, NY). All continuous variables were converted to natural logarithms to facilitate examination of power relations between continuous variables and to investigate proportional effects of discrete variables (22, 23). In all cases, the distribution of the logged variables approximated normality. When the dependent variable is expressed as a natural logarithm, the regression coefficient for a discrete variable corresponds closely to the percentage effect: (difference/mean) x 100 (22, 23).
To examine the influence of the calcium supplement and other variables on bone mineral status independently of bone and body size, BMC was adjusted for BW, body weight, and height by using simultaneous multiple regression analysis with backwards elimination (22). A similar approach was used to adjust plasma osteocalcin for sex and pubertal status. The baseline value was entered as an independent variable in all regression analyses to minimize regression toward the mean. The basic model used to examine the effect of the calcium supplement was as follows:
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Subject characteristics and bone variables were similar in boys and girls at baseline, except that girls had significantly greater triceps skinfold thickness [by 1.6 ± 0.3 mm ( ± SE); P 0.0001]. Similar results were obtained when the analyses were conducted in boys and girls separately. Consequently, the characteristics of the 2 groups and the effect of the calcium supplement were examined with the sexes combined.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). The children in both groups were small for their age and puberty was delayed compared with British reference children (21, 24). The mean (±SD) z scores of the whole group relative to the British reference were as follows: height-for-age z score = -1.17 ± 0.86 and weight-for-age z score = -1.76 ± 0.85. Most subjects were prepubertal throughout the study (Table 1). No girl had reached menarche at the start of the study and 2 started menstruating during the intervention. The number of children who had entered puberty at the start or who moved into Tanner stages 2–5 during the study did not differ significantly between the 2 groups. Dietary calcium intake averaged 338 ± 142 mg/d (8.45 ± 3.55 mmol/d) and was not significantly different between the 2 groups (calcium group: 342 ± 129 mg/d, or 8.55 ± 3.28 mmol/d; placebo group: 334 ± 153 mg/d, or 8.35 ± 3.83 mmol/d). Calcium supplementation raised the calcium intake of the children in the calcium group by 714 mg/d (17.85 mmol/d), to a total intake of 1056 mg/d (26.4 mmol/d).
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). The incremental gains in BMC and BMD at both the midshaft and distal radius were greater in the calcium than in the placebo group, significantly so after adjustment for baseline values (Table 3). These incremental gains were not correlated with age, sex, pubertal status, or dietary calcium intake, and no significant interactions with the supplement group were observed, indicating that the response to the supplement was not influenced by any of these variables. The significant differences in BMC at the midshaft and distal radius at the end of the study between the calcium and placebo groups remained after further adjustment for BW, weight, and height by using regression analysis. There was a trend toward a smaller BW at the midshaft radius in the calcium group at the end of the study, after adjustment for baseline values, but it was not significant. There were no significant effects of the calcium supplement on weight, height, or distal radius BW.
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). At the end of the study, the calcium group had experienced a decrease in plasma osteocalcin during the 12-mo study period and had significantly lower concentrations than the placebo group (Table 3). The plasma osteocalcin concentration of the placebo group at the end of the study was not significantly different from that at baseline (Table 3). After adjustment for the baseline value, plasma osteocalcin concentrations at the end of the study were not influenced by age but were significantly greater in girls than in boys ( difference ± SE 17.8 ± 7.1%; P = 0.015) and in those who were at Tanner stages 2–5 (n = 39) than in those at Tanner stage 1 (n = 59): by 15.8 ± 7.2% (P = 0.031). After adjustment for the baseline value, sex, and pubertal status, the calcium group had significantly lower plasma osteocalcin concentrations than the placebo group (22%; Table 3). There was no evidence of any interaction between the supplement effect on plasma osteocalcin and age, sex, pubertal status, or dietary calcium intake. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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5% at both sites. This represents a shift of 0.3–0.4 of the population SD for this age group, which in adults would represent a significant reduction in fracture risk (25). Therefore, the study supports the findings of calcium supplementation studies in other groups of children, which suggest that an increase in calcium intake, if sustained throughout childhood, can positively modify peak bone mass and, thereby, reduce osteoporotic fracture risk in later life (2–7). The results of the present study were necessarily limited by the use of single-photon absorptiometry, which was able to monitor the effects of calcium supplementation only on the bones of the forearm and not at other skeletal sites. However, at the time of the study, there were no facilities for dual-energy X-ray absorptiometry in The Gambia and more comprehensive measurements of bone mineral status were not possible. The observed increases in bone mineral were similar whether expressed as BMC, BMD, or size-adjusted BMC. In contrast, there was no evidence of a positive effect of the supplement on the size of the growing skeleton, either in terms of increased statural height or in bone width, in fact, there was a trend toward a smaller increase in bone width at the midshaft radius in the calcium group. This suggests that the effect of the higher calcium intake was to increase the amount of mineral present within a given bone volume rather than to promote bone growth. Other intervention studies using calcium salts have shown similar effects, with an increase in bone mineral but no effect on size (2, 3, 5, 6). This contrasts with the results of studies using milk and dairy products (26) or calcium salts extracted from milk (8), in which anabolic effects on the skeleton were also indicated. The lack of an effect on height in this group of growth-retarded children also parallels the results of earlier studies in which an increase in height velocity in older children from disadvantaged backgrounds was observed in studies using milk but not in those using calcium salts (9, 27–29). It is possible, however, that deficiencies of other nutrients in the diet of the Gambian children may have limited any potential effect of the calcium supplement on growth.
The increased bone mineral in the calcium group was accompanied by a marked decrease in plasma osteocalcin concentration, a marker of bone formation rate. Interestingly, the one other study using calcium salts that investigated alterations in plasma osteocalcin also showed a decrease in plasma osteocalcin concentrations in the group of children who responded to the supplement (2). This contrasts with the lack of an effect on the bone formation marker in children supplemented with milk (26), suggesting that the mechanism of action of these 2 sources of calcium on the skeleton may differ.
The decrease in plasma osteocalcin observed in this study suggests that the effect of the supplement on bone mineral status may have been due to a phenomenon known as the bone remodeling transient (30–32), in which an increase in calcium supply leads to a decrease in the activation frequency of osteoclasts at the start of the remodeling process. This produces a decrease in bone resorption and, because of coupling within each bone remodeling cycle, ultimately reduces the bone formation rate. This decreases the proportion of skeletal surfaces that are actively undergoing bone remodeling at any one time, resulting in an increase in the mineral present per unit volume of bone. The increase in bone mineral reaches an upper threshold with the completion of resorption cycles initiated before the change in calcium supply and is reversed if the calcium supply returns to its original level. These alterations in bone mineral can be sufficiently large to be detected by absorptiometry (33). The phenomenon of the bone remodeling transient is well recognized in adults and is the basis for the antiresorptive action of calcium used as a therapy for postmenopausal bone loss (33). However, whether a reduced rate of skeletal remodeling, or specifically of bone formation, represents a benefit for the growing skeleton is unknown and requires further study. Although it has been suggested that the lower rates of bone remodeling observed in American black children than in white children may underpin the differences in peak bone mass and osteoporotic fracture rates between these ethnic groups (14), more research is required to determine the long-term outcome of a reduction in the bone formation rate in growing individuals as a result of dietary manipulation.
The children in the present study had a low customary calcium intake, averaging 350 mg/d, which increased 3-fold with the calcium supplement. Despite this, the magnitude of the observed calcium effect was similar to the 2–6% increase reported from studies in children with a considerably higher customary calcium intake or in which lower amounts of supplemental calcium were used (2, 3, 5, 6). Our study, therefore, provides no evidence to support the possibility that children with a very low calcium intake have a greater response to calcium supplementation than do children with high intakes (8). Therefore, it is difficult to equate the results in these Gambian children with a correction of calcium deficiency because analogous effects have been noted in children with a customary calcium intake before supplementation similar to that of the Gambian children after receiving extra calcium (2–4, 7). Instead, our results suggest that the bone remodeling space decreases with increasing calcium intake in an approximately linear fashion over a wide range of intakes. This parallels the findings from the mathematical modeling of data from balance studies in children in which calcium retention appeared to rise with increasing calcium intakes up to a maximum threshold at high intakes (10). If this interpretation proves correct, it raises questions about the relation of the bone remodeling rate to bone health and about what level of bone remodeling should be regarded as optimal for the growing skeleton.
In summary, this randomized, controlled study in The Gambia showed that supplementation with calcium carbonate increased bone mineral status, decreased the bone formation rate, but did not alter growth in prepubertal and peripubertal children with a low customary calcium intake and who were lighter, shorter, and less mature than reference children of the same age. Calcium supplementation may benefit Gambian children by increasing bone mineralization and, ultimately, peak bone mass. Alternatively, these results may indicate an alteration in bone remodeling, the consequences of which for bone health are unknown. Follow-up studies of the Gambian children are currently in progress to resolve some of these issues.
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ACKNOWLEDGMENTS |
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