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Factors affecting calcium balance in Chinese adolescents
Bone 46 (2010) 162–166
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Bone j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / b o n e
Factors affecting calcium balance in Chinese adolescents Jing Yin, Qian Zhang, Ailing Liu, Weijing Du, Xiaoyan Wang, Xiaoqi Hu, Guansheng Ma ⁎ National Institute for Nutrition and Food Safety, Chinese Center for Disease Control and Prevention, 7 Pan Jia Yuan Nan Li, Beijing 100021, China
a r t i c l e
i n f o
Article history: Received 3 February 2009 Revised 21 September 2009 Accepted 21 September 2009 Available online 29 September 2009 Edited by: R. Baron Keywords: Calcium Retention Absorption efficiency Adolescence
a b s t r a c t Chinese dietary reference intakes (DRIs) for calcium were developed mainly from studies conducted amongst Caucasians, yet a recent review showed that reference calcium intakes for Asians are likely to be different from those of Caucasians (Lee and Jiang, 2008). In order to develop calcium DRIs for Chinese adolescents, it is necessary to explore the characteristics and potential influencing factors of calcium metabolic balance in Chinese adolescents. A total of 80 students (15.1 ± 0.8 years) were recruited stratified by gender from a 1-year calcium supplementation study. Subjects were randomly designed to four groups and supplemented with calcium carbonate tablets providing elemental calcium at 63, 354, 660, and 966 mg/ day, respectively. Subjects consumed food from a 3-day cycle menu prepared by staff for 10 days. Elemental calcium in samples of foods, feces, and urine was determined in duplicates by inductively coupled plasma atomic emission spectrometry. The total calcium intake ranged from 352 to 1323 mg/day. The calcium apparent absorption efficiency and retention in boys were significantly higher than that in girls (68.7% vs. 46.4%, 480 mg/day vs. 204 mg/day, P b 0.05). Calcium retention increased with calcium intakes, but did not reach a plateau. Calcium absorption efficiency in boys increased with calcium intake up to 665 mg/day, and decreased after that. In girls, calcium absorption efficiency decreased with calcium intake. Calcium absorption efficiency increased within 1 year after first spermatorrhea in boys, but decreased with pubertal development in girls. Sex, calcium intake, age, and pubertal development were the most important determinants of calcium absorption (R2 = 0.508, P b 0.01) and retention (R2 = 0.745, P b 0.05). This study indicates that sex, calcium intake, age, and pubertal development are important factors for calcium retention and absorption during growth, which should be considered for the development of calcium DRIs for Chinese adolescents. © 2009 Elsevier Inc. All rights reserved.
Introduction Calcium is responsible for maintaining the stiffness of the skeleton, and is also important in soft tissue and in cellular metabolism. The integrity of the skeleton would be at risk if calcium supply falls short of requirements [2]. Obtaining adequate calcium intake during childhood through early adulthood is crucial to osteoporosis prevention, as almost 40% of adult peak bone mass is acquired during those years [3,4]. Impaired acquisition of bone during puberty is an important risk factor for the development of osteoporosis in later life [5]. Dietary calcium reference intakes (DRIs) in China were developed by Chinese Nutrition Society in 2000, mainly using data obtained from studies conducted in other countries. However, ethnic differences in bone mass and its accretion rate are evident among Asian, Black, Caucasian, and Hispanic adolescents in the US [1]. The smaller bone size of Asians was assumed to be one of the main reasons for differences in bone mineral between Asians and Caucasians [6], and
⁎ Corresponding author. Fax: +86 10 67711813. E-mail address: [email protected] (G. Ma). 8756-3282/$ – see front matter © 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.bone.2009.09.022
hip axis length was found to be shorter in mature Asians and Blacks than Whites [7]. Calcium requirements might vary between cultures for dietary, genetic, lifestyle, and geographical reasons [2]. There is some evidence for associations between polymorphism of the vitamin D receptor (VDR) gene and Ca absorption in adolescents [8,9]. Black adolescents retained more calcium than their White counterparts with the same calcium intake [10,11]. Furthermore, Asian adults have lower average body weight and bone mass than Caucasians of the same age [1]. Hip fractures for Asian people were lower than those for Caucasians living in Northern Europe and North America [12]. Another study found that Asian women had lower incidence of hip fracture over 1 year of follow-up than White and Black women, although Asian women had the lowest BMD [13]. However, it also reported that there is no significant interethnic differences with BMAD (bone mineral apparent density (BMAD, g/cm3) correcting the values for height [14]. The 2002 China National Nutrition and Health Survey (CNNHS) found that the average calcium intake was 376 mg/day for boys and 343 mg/day for girls aged 14–17 years [15], which was only about 30% of calcium adequate intake (AI, 1000 mg/day). The gap between recommended AI and actual calcium intake, as well as the factors that potentially affect calcium balance, varied widely in a group of Chinese
J. Yin et al. / Bone 46 (2010) 162–166
163
Material and methods
water of all subjects were collected and processed daily for 10 days. Urine samples were 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. The urine was acidified using concentrated hydrochloric acid (1%, by vol.). Fecal samples were collected in preweighed containers and pooled as 24-h collections, diluted with concentrated hydrochloric acid and double distilled water, and homogenized with a blender. All samples were frozen at −20 °C. Aliquots were sampled. Samples and calcium carbonate tablets were digested using the wet method [16]. Calcium in samples was measured with inductively coupled plasma atomic emission spectrometry (Optima 3000, Perkin Elmer).
Study population
Anthropometric measurement
A total of 337 healthy adolescents (average 13.5 years old) were recruited from two junior middle schools in Beijing, China (172 boys, 165 girls). Students were randomly assigned to four groups stratified by gender, each group included about 40 students. Each participant ate three pieces of chewable calcium carbonate tablets each day. Supplementation doses of calcium in the four groups were 63, 354, 660, and 966 mg/day, respectively. All subjects completed questionnaires about medical and family fracture history. Those with any family history of bone or arthritic diseases, intake of medicine that could affect bone or cartilage or calcium metabolism, were excluded. Compliance of calcium supplementation was estimated 1 year later with an interview about recalling intakes of calcium tablets during holidays and study terms. After 1 year, 10 boys and 10 girls (aged 12–17 years) were randomly selected from each group to participate in a 10-day balance study. These 80 students were asked to live in schools and during a 3-day adaptation period and 7-day metabolism period. The study protocol and questionnaires used were approved by the Ethical Committee of National Institute for Nutrition and Food Safety, Chinese Center for Disease Control and Prevention. A written consent form was obtained from each participant and his/her guardian.
Height and weight were measured in a standing position wearing indoor clothing following a standardized procedure by trained interviewers. Body mass index (BMI) was calculated as weight in kilograms divided by height in meters squared (kg/m2). Information on past illnesses and date of first spermatorrhea in boys or menarche in girls was obtained using interview-administrated questionnaires.
adolescents. Therefore, the body of evidence required to formulate recommendations for calcium intake in this population is currently insufficient and requires additional metabolic studies. Calcium balance studies provide one of the most important lines of evidence for the development of calcium DRIs. In this paper we discuss characteristics of calcium metabolism and some potential influencing factors in Chinese adolescents undergoing calcium balance assessment. These results may provide the basis for developing calcium DRIs to guide adolescents on calcium intake, which is of great importance for the prevention of osteoporosis.
Food preparation and intakes A 3-day cycle menu was developed referring to local dietary habits and vegetables supplied by market. Actual food intakes were recorded in every meal by weighing each food before and after meals were consumed. Subjects were asked to only consume foods prepared by the staff during the adaptation period and metabolism period, and were asked to eat a calcium carbonate tablet under the supervision of staff before each meal. We supplied similar foods to every student and encouraged them to eat as during the prior 12 months. Collection and measurement of metabolic samples Samples of cooked foods were collected and homogenized using a blender with blades of stainless steel. Samples of feces, urine, and
Dietary intake Dietary intake during the calcium supplementation study was assessed with a 24-h dietary recall method for 3 consecutive days (two weekdays and one weekend day) by trained interviewers. The Chinese Food Composition Tables were used to calculate nutrient intakes [17]. Statistical analysis Calcium retention was determined by calcium intake minus urinary and fecal calcium excretion during balance period. Calcium apparent absorption efficiency was determined by calcium intake minus fecal calcium excretion, and then divided by calcium intakes. One-way ANOVA was used for analyzing differences in age, height, body weight, BMI, pubertal development, calcium intake, and retention among the four groups. The Kruskal–Wallis test was used for analyzing calcium apparent absorption efficiency. P values less than 0.05 were considered significant. The factors which might be related to calcium absorption and retention potentially were analyzed using multivariable stepwise regression. Pubertal development was classified as the first spermatorrhea or menarche, 12 months for boys and 24 months for girls. Pubertal development entered in the models as a categorical variable. P values for entry and removal of terms into and out of the model were 0.10. Curve estimations of calcium apparent absorption efficiency and calcium retention were done with calcium intake as the independent variable. All statistical analysis was done with the SAS Statistical Package (SAS 8.2e for Windows, SAS Institute, Inc.).
Table 1 Comparison on characteristics of subjects among four groups. Boys
n (n1) Age (years) Height (cm) Weight (kg) BMI (kg/m2) Period (mo)a
Girls
Group 1
Group 2
Group 3
Group 4
Group 1
Group 2
Group 3
Group 4
9 (8) 15.3 ± 0.7 167.3 ± 8.6 63.6 ± 18.6 22.6 ± 6.1 14 ± 6
10 (8) 15.5 ± 0.5 169.0 ± 5.2 57.7 ± 9.2 20.2 ± 2.4 13 ± 6
9 (7) 15.3 ± 0.5 170.4 ± 9.8 59.8 ± 6.2 20.7 ± 2.5 22 ± 15
7 (5) 15.2 ± 0.7 166.4 ± 5.1 56.8 ± 13.4 20.3 ± 3.5 15 ± 11
10 (10) 14.6 ± 1.1 159.0 ± 5.6 53.3 ± 12.1 20.9 ± 3.6 29 ± 16
8 (8) 14.9 ± 0.8 157.9 ± 6.5 52.7 ± 10.7 21.0 ± 3.1 34 ± 22
10 (10) 15.0 ± 1.1 159.0 ± 6.0 52.5 ± 6.3 20.7 ± 2.1 32 ± 10
10 (10) 14.7 ± 0.8 159.9 ± 6.1 51.1 ± 6.7 19.9 ± 1.7 30 ± 9
One-way ANOVA test among four groups, P N 0.05. n1, number after first spermatorrhea or menarche. a Months since spermatorrhea for boys, or months since menarche for girls.
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Table 2 Comparison on Ca metabolic balance among four groups ðx F sÞ.
Boys (n = 37) Ca intake from dietary and water (mg/day) Total Ca intake (mg/day) Urine Ca (mg/day) Feces Ca (mg/day) Ca retention (mg/day) Ca apparent absorption efficiency (%) Girls (n = 38) Ca intake from dietary and water (mg/day) Total Ca intake (mg/day) Urine Ca (mg/day) Feces Ca (mg/day) Ca retention (mg/day) Ca apparent absorption efficiency (%)
Group 1
Group 2
Group 3
Group 4
P
352.0 ± 56.4 427.1 ± 48.2a 55.0 ± 31.9 129.0 ± 28.0a 243.1 ± 82.1a 69.3
369.6 ± 64.6 723.6 ± 64.6b 74.1 ± 37.3 177.1 ± 83.8a,b 472.4 ± 109.2b 75.3
308.2 ± 81.2 1002.0 ± 46.2c 115.0 ± 57.5 291.8 ± 139.2b 595.5 ± 153.9b,c 71.0
345.1 ± 100.5 1323.0 ± 85.1d 94.2 ± 78.5 582.7 ± 180.9c 645.7 ± 196.0c 55.6
0.368 0.000 0.128 0.000 0.000 0.057
289.4 ± 51.3 352.4 ± 51.3a 110.3 ± 64.6 161.8 ± 69.9a 80.3 ± 60.1a 55.0
265.9 ± 40.9 619.9 ± 40.9b 156.0 ± 66.7 326.9 ± 117.8b 137.0 ± 102.0a,b 47.6
305.6 ± 39.1 965.6 ± 39.1c 186.3 ± 53.6 550.0 ± 91.8c 229.3 ± 103.1b 43.0
294.2 ± 40.8 1260.0 ± 40.8d 154.4 ± 59.2 750.8 ± 120.6d 355.0 ± 127.9c 40.4
0.296 0.000 0.065 0.000 0.000 0.136
One-way ANOVA. Kruskal–Wallis Test for rate comparison. a,b,c,d Different letter means there were significant difference between groups.
A total of 73 of 80 students completed the 10-day metabolic balance study. The characteristics of the subjects appear in Table 1. The average age of subjects was 15.1 ± 0.8 years. There were no significant differences in age, height, and body weight among the four groups (P N 0.05). First spermatorrhea occurred in the past 12 months for 13 boys, and menarche occurred 24 months ago for 27 girls. The total calcium intakes (from dietary, water, and calcium carbonate tablets) of boys were 427, 724, 1002, and 1323 mg/day for four groups, respectively, while that of girls were 352, 620, 966, and 1260 mg/day. Calcium retention as well as calcium excreted in feces increased significantly with total calcium intake among the four groups (P b 0.05), but there were no significant differences among the four groups on calcium intake from dietary and water, calcium apparent absorption efficiency, and calcium excreted in urine (Table 2). The average calcium intake was similar between boys and girls (839 mg/day vs. 809 mg/day), but calcium apparent absorption efficiency as well as retention differed significantly between boys and girls (46.4% vs. 68.7%, 480 mg/day vs. 204 mg/day) (P b 0.05)
(Table 2). Calcium intake, retention, and apparent absorption efficiency of boys were significantly higher than that of their girl counterparts in respective groups (P b 0.05). Using curve estimation, calcium retention increased with calcium intake, but did not reach a plateau in both boys and girls. Trends of Ca absorption efficiency differed between boys and girls. Calcium absorption efficiency increased to 78.6% in boys when their calcium intakes reached 665 mg/day, but then decreased with more calcium intakes. However, in girls, calcium absorption efficiency decreased with calcium intake, and the plateau of calcium apparent absorption efficiency approached 45.0% when calcium intake was 650 mg/day (Figs. 1 and 2). Using multivariable stepwise regression, we found that sex and calcium intake were the two most important contributors for calcium balance in Chinese adolescents, explaining about 50% of the variability in calcium absorption, with pubertal development also playing a role. Calcium apparent absorption efficiency increased in boys with time after first spermatorrhea, peaking at 12 months and decreasing thereafter. Calcium apparent absorption efficiency decreased in girls with time after menarche up to 24 months, and steadied after that. Sex, calcium intake, and age were the most important determinants for calcium retention, explaining 74.5% of variability in calcium retention (Table 3, Fig. 3).
Fig. 1. Relationship between Ca intake and Ca metabolism balance in boys.
Fig. 2. Relationship between Ca intake and Ca metabolism balance in girls.
Results
J. Yin et al. / Bone 46 (2010) 162–166 Table 3 Multivariable stepwise regression analysis with Ca apparent absorption efficiency or Ca retention as a dependent variable and age, sex, weight, height, Ca intake, and pubertal development as independent variables. β
SE
Standard β P
Ca apparent absorption efficiency 0.508 Sex 21.044 3.217 0.593 Ca intake −0.015 0.004 −0.294 Pubertal development −5.953 3.229 −0.167 Ca retention Sex 291.457 28.714 0.66 Ca intake 0.367 0.04 0.567 Age −51.734 17.918 −0.188
0.000 0.001 0.07 0.745 0.000 0.000 0.005
R2 0.394 0.089 0.025 0.404 0.309 0.032
Both standard of enter model and remove model were 0.10. Pubertal development was classified by periods between Ca balance experiment and first spermatorrhea or menarche: 12 months for boys and 24 months for girls.
Discussion This study represents the first attempt to evaluate calcium balance among Chinese adolescents over 1-year period and to evaluate characteristics and potential influencing factors of calcium metabolism and calcium balance in Chinese adolescents, including sex, age, calcium intake, and pubertal development in order to develop calcium DRIs based on characteristics of calcium balance in Chinese adolescents. It was recommended to use gender- and ethnic-specific standards for interpreting pediatric bone densitometry data [18]. There were significant differences in calcium absorption and retention between boys and girls in this study, which probably reflected differences in stage of pubertal development between boys and girls. At the time of this study, first spermatorrhea or menarche had been experienced by most subjects, and girls were more mature in pubertal development than boys. Bachrach et al. reported that Black and Asian females and Asian males tended to reach a plateau in BMD earlier than the other ethnic groups [18]. Martin et al. found BMC velocity peak at 13.3 years of age for boys and 11.4 years for girls in Canada. Within 3 years on either side of peak BMC velocity peak, boys had consistently higher BMC and BMC velocity compared with girls and the discrepancy increased steadily through puberty [19]. The rates of bone calcium deposition reached a maximum in girls shortly before menarche, which was approximately five times that of adulthood, and the decline in bone calcium deposition rate is gradual after menarche [20]. Girls in this study were in the stage of slower BMC velocity, but boys were at the peak in BMC velocity, which could contribute to observed differences in calcium absorption and retention. In this study, we found that pubertal development explained only 2.5% of the variability in calcium absorption. Calcium absorption of girls in this study was 46.4%, which was 52–55% in Chinese girls in 9–11.5 years before menarche [21], but 34% in Chinese young women aged 18–23 years [22]. Calcium absorption of girls in this study was shown in Fig. 3, which indicated calcium absorption decreased with pubertal development in Chinese girls. Calcium absorption of Chinese girls in this study was similar to postmenarcheal girls who were Black (44%), but not those who were White (25%) [23]. Calcium absorption of Chinese boys in this study was higher than true fractional calcium absorption (61%) in 7-year-old Chinese children [24], and was significantly higher than that in pubertal Caucasian boys (30%) [25]. Sex and calcium intake were found to be the most important contributions to calcium balance in Chinese adolescents, which explained more than 70% of variability in calcium retention. Of these, calcium intake explained about 30% of variation. A recent metabolic study in White American boys aged 13–15 years found that calcium intake explained 21.7% of the variability in calcium retention, suggesting that calcium intake is the greatest predictor of calcium retention in adolescent boys [26]. Weaver reviewed that dietary calcium could predict 10–15% of skeletal calcium retention during
165
adolescence with race and sexual maturity in the model [27]. These studies support the notion that adequate calcium intake during adolescence is important for calcium retention and bone accrual during skeletal growth. We did not achieve a plateau of calcium retention in this study, but we tried to calculate calcium requirement for Chinese adolescents using the results of other studies, such as studies on daily calcium retention in bone. Martin found that PBMCV was 320 g/year in boys and 240 g/year in girls. Assuming that calcium comprises 40% of bone mineral [28], Zhai et al. found that maximal daily calcium retention was 338 mg in Chinese boys and 261 mg in girls with a cross-sectional study [29]. To maintain these values for the skeleton, taking into account 100 mg for urinary calcium, and 40 mg for other losses not accounted for elsewhere, the net absorbed calcium during this period needs to be 478 mg/day for boys and 401 mg/day for girls. This requires an intake of 625 mg/day for boys and 872 mg/day for girls. To meet the needs of pubertal development, we presumed that recommended adequate intakes of calcium were more than 600 mg/ day in 12- to 17-year-old boys and 900–1000 mg/day in girls during the phase of peak growth, values that differ greatly from recommended intakes for American boys. Braun found that maximal calcium retention in 12- to 15-year boys was achieved at an intake of 1140 mg/day. Calcium retention was higher (by 171 ± 38 mg/day) in boys than in girls at all calcium intakes studied [30]. This difference could be the result of ethnic variability in calcium absorption and retention. Blacks had 185 mg/day greater mean skeletal calcium retention than did Whites as a result of significantly greater net calcium absorption and lower calcium excretion [31].There are several limitations in our results. Firstly, subjects in this study had taken part in the intervention study of calcium supplementation for 1 year, but only 60% complied with calcium supplementation when they recalled actual tablet intakes after the study. This might be one explanation of the observed high absorption efficiency, although we included a 3-day adaptation period. Longer balance equilibration periods may be helpful in future studies. Secondly, we did not document the progression of pubertal development by Tanner stage in this study. Pubertal information was collected prior to initiating the supplementation program, which precluded stratifying study results by Tanner stage. We analyzed pubertal development with date of first spermatorrhea in boys or menarche in girls, which might be difficult to evaluate in boys and might cause recall bias. Lastly, no fecal markers were used in this study; therefore, we could only estimate true
Fig. 3. Trends of Ca absorption with pubertal development. Ca absorption efficiency decreased with pubertal development in girls, but increased in boys within 1 year after first spermatorrhea.
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calcium absorption and excretion compliance. Based on these results, we suggest that adequate intakes of calcium for Chinese adolescents exceed 600 mg/day in 12- to 17-year-old boys and 900–1000 mg/day in girls during the peak growth phase. Further metabolic balance studies with biochemical markers are needed to confirm these results. In conclusion, sex, calcium intake, age, and pubertal development are important contributors for calcium retention and absorption during skeletal growth. These factors should be taken into consideration for the development of calcium DRIs in Chinese adolescents. Acknowledgments The authors wish to thank all subjects for their participation in this study. A special thanks to Dr. Laura Laslett for assistance on English reviewing. This study was supported by China National Natural Science Foundation (Project No. 30471453). References [1] Lee WT, Jiang J. Calcium requirements for Asian children and adolescents. Asia Pac J Clin Nutr 2008;17(Suppl 1):33. [2] Report of a Joint FAO/WHO Expert Consultation. Human vitamin and mineral requirements; 2002. [3] Weaver CM. The growing years and prevention of osteoporosis in later life. Proc Nutr Soc 2000;59:303–6. [4] Matkovic V, Jelic T, Wardlaw GM, et al. Timing of peak bone mass in Caucasian females and its implication for the prevention of osteoporosis. Inference from a cross-sectional model. J Clin Invest 1994;93:799–808. [5] Suuriniemi M, Mahonen A, Kovanen V, et al. Association between exercise and pubertal BMD is modulated by estrogen receptor alpha genotype. J Bone Miner Res 2004;19:1758–65. [6] Bhudhikanok GS, Wang MC, Eckert K, Matkin C, Marcus R, Bachrach LK. Differences in bone mineral in young Asian and Caucasian Americans may reflect differences in bone size. J Bone Miner Res 1996;11:1545–56. [7] Wang MC, Aguirre M, Bhudhikanok GS, Kendall CG, Kirsch S, Marcus R, Bachrach LK. Bone mass and hip axis length in healthy Asian, black, Hispanic, and white American youths. J Bone Miner Res 1997;12:1922–35. [8] Abrams SA, Griffin IJ, Hawthorne KM, et al. Vitamin D receptor Fok1 polymorphisms affect calcium absorption, kinetics, and bone mineralization rates during puberty. J Bone Miner Res 2005;20:945–53. [9] Ames SK, Ellis KJ, Gunn SK, Copeland KC, Abrams SA. Vitamin D receptor gene Fok1 polymorphism predicts calcium absorption and bone mineral density in children. J Bone Miner Res 1999;14:740–6.
[10] Bryant RJ, Wastney ME, Martin BR, et al. Racial differences in bone turnover and calcium metabolism in adolescent females. J Clin Endocrinol Metab 2003;88: 1043–50. [11] Wigertz K, Palacios C, Jackman LA, et al. Racial differences in calcium retention in response to dietary salt in adolescent girls. Am J Clin Nutr 2005;81:845–50. [12] Hagino H. Epidemiology of hip fracture. Clin Calcium 2006;16:1954–9. [13] Barrett-Connor E, Siris ES, Wehren LE, et al. Osteoporosis and fracture risk in women of different ethnic groups. J Bone Miner Res 2005;20:185–94. [14] Marcus R, Greendale G, Blunt BA, Bush TL, Sherman S, Sherwin R, Wahner H, Wells B. Correlates of bone mineral density in the postmenopausal estrogen/progestin interventions trial. J Bone Miner Res 1994;9:1467–76. [15] Zhai FY, Yang XG. Report of Chinese National Survey of Nutrition and Health in 2002, dietary intake; 2006. p. 251–2. [16] Standards Press in China. Calcium assay in foods. National standards in China 2005;GB/T 5009.92-2003 612-618. [17] Yang Y, Wang G, Pan X. Chinese food composition table. Medical Press of Beijing University; 2002. [18] Bachrach LK, Hastie T, Wang MC, Narasimhan B, Marcus R. Bone mineral acquisition in healthy Asian, Hispanic, black, and Caucasian youth: a longitudinal study. J Clin Endocrinol Metab 1999;84:4702–12. [19] Martin AD, Baily DA, McKay HA, Whiting S. Bone mineral and calcium accretion during puberty. Am J Clin Nutr 1997;66:611–5. [20] Abrams SA. Calcium turnover and nutrition through the life cycle. Proc Nutr Soc 2001;60:283–91. [21] Xiao XC, Su YX, Luo XL. Study of calcium metabolism in premenarche Chinese girls. Acta Nutrimenta Sinica 2005;27:517–20. [22] Huang ZW, Dong J, Piao JH, et al. Relationship between the absorption of dietary calcium and the Fok I polymorphism of VDR gene in young women. Zhonghua Yu Fang Yi Xue Za Zhi 2006;40:75–9. [23] Abrams SA, O'brien KO, Liang LK, Stuff JE. Differences in calcium absorption and kinetics between black and white girls aged 5–16 years. J Bone Miner Res 1995;10: 829–33. [24] Lee WT, Leung SS, Xu YC, Wang SH, Zeng WP, Lau J, Fairweather-Tait SJ. Effects of double-blind controlled calcium supplementation on calcium absorption in Chinese children measured with stable isotopes (42Ca and 44Ca). Br J Nutr 1995;73:311–21. [25] Weaver CM. Age related calcium requirements due to changes in absorption and utilization. J Nutr 1994;124:1418S–25S. [26] Hill KM, Braun M, Kern M, Martin BR, Navalta JW, Sedlock DA, et al. Predictors of calcium retention in adolescent boys. J Clin Endocrinol Metab 2008;93:4743–8. [27] Weaver CM. The role of nutrition on optimizing peak bone mass. Asia Pac J Clin Nutr 2008;17(Suppl 1):135. [28] Ge K. An overview of Chinese nutrition science. People Health Press; 2004. [29] Zhai F, Zhang L, Wang C, Pan H. Study of normal reference values for bone mineral contents in children and adolescents in Beijing. Wei Sheng Yan Jiu 2004;33:172–6. [30] Braun M, Martin BR, Kern M, et al. Calcium retention in adolescent boys on a range of controlled calcium intakes. Am J Clin Nutr 2006;84:414–22. [31] Braun M, Palacios C, Wigertz K, et al. Racial differences in skeletal calcium retention in adolescent girls with varied controlled calcium intakes. Am J Clin Nutr 2007;85:1657–63.
Contents lists available at ScienceDirect
Bone j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / b o n e
Factors affecting calcium balance in Chinese adolescents Jing Yin, Qian Zhang, Ailing Liu, Weijing Du, Xiaoyan Wang, Xiaoqi Hu, Guansheng Ma ⁎ National Institute for Nutrition and Food Safety, Chinese Center for Disease Control and Prevention, 7 Pan Jia Yuan Nan Li, Beijing 100021, China
a r t i c l e
i n f o
Article history: Received 3 February 2009 Revised 21 September 2009 Accepted 21 September 2009 Available online 29 September 2009 Edited by: R. Baron Keywords: Calcium Retention Absorption efficiency Adolescence
a b s t r a c t Chinese dietary reference intakes (DRIs) for calcium were developed mainly from studies conducted amongst Caucasians, yet a recent review showed that reference calcium intakes for Asians are likely to be different from those of Caucasians (Lee and Jiang, 2008). In order to develop calcium DRIs for Chinese adolescents, it is necessary to explore the characteristics and potential influencing factors of calcium metabolic balance in Chinese adolescents. A total of 80 students (15.1 ± 0.8 years) were recruited stratified by gender from a 1-year calcium supplementation study. Subjects were randomly designed to four groups and supplemented with calcium carbonate tablets providing elemental calcium at 63, 354, 660, and 966 mg/ day, respectively. Subjects consumed food from a 3-day cycle menu prepared by staff for 10 days. Elemental calcium in samples of foods, feces, and urine was determined in duplicates by inductively coupled plasma atomic emission spectrometry. The total calcium intake ranged from 352 to 1323 mg/day. The calcium apparent absorption efficiency and retention in boys were significantly higher than that in girls (68.7% vs. 46.4%, 480 mg/day vs. 204 mg/day, P b 0.05). Calcium retention increased with calcium intakes, but did not reach a plateau. Calcium absorption efficiency in boys increased with calcium intake up to 665 mg/day, and decreased after that. In girls, calcium absorption efficiency decreased with calcium intake. Calcium absorption efficiency increased within 1 year after first spermatorrhea in boys, but decreased with pubertal development in girls. Sex, calcium intake, age, and pubertal development were the most important determinants of calcium absorption (R2 = 0.508, P b 0.01) and retention (R2 = 0.745, P b 0.05). This study indicates that sex, calcium intake, age, and pubertal development are important factors for calcium retention and absorption during growth, which should be considered for the development of calcium DRIs for Chinese adolescents. © 2009 Elsevier Inc. All rights reserved.
Introduction Calcium is responsible for maintaining the stiffness of the skeleton, and is also important in soft tissue and in cellular metabolism. The integrity of the skeleton would be at risk if calcium supply falls short of requirements [2]. Obtaining adequate calcium intake during childhood through early adulthood is crucial to osteoporosis prevention, as almost 40% of adult peak bone mass is acquired during those years [3,4]. Impaired acquisition of bone during puberty is an important risk factor for the development of osteoporosis in later life [5]. Dietary calcium reference intakes (DRIs) in China were developed by Chinese Nutrition Society in 2000, mainly using data obtained from studies conducted in other countries. However, ethnic differences in bone mass and its accretion rate are evident among Asian, Black, Caucasian, and Hispanic adolescents in the US [1]. The smaller bone size of Asians was assumed to be one of the main reasons for differences in bone mineral between Asians and Caucasians [6], and
⁎ Corresponding author. Fax: +86 10 67711813. E-mail address: [email protected] (G. Ma). 8756-3282/$ – see front matter © 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.bone.2009.09.022
hip axis length was found to be shorter in mature Asians and Blacks than Whites [7]. Calcium requirements might vary between cultures for dietary, genetic, lifestyle, and geographical reasons [2]. There is some evidence for associations between polymorphism of the vitamin D receptor (VDR) gene and Ca absorption in adolescents [8,9]. Black adolescents retained more calcium than their White counterparts with the same calcium intake [10,11]. Furthermore, Asian adults have lower average body weight and bone mass than Caucasians of the same age [1]. Hip fractures for Asian people were lower than those for Caucasians living in Northern Europe and North America [12]. Another study found that Asian women had lower incidence of hip fracture over 1 year of follow-up than White and Black women, although Asian women had the lowest BMD [13]. However, it also reported that there is no significant interethnic differences with BMAD (bone mineral apparent density (BMAD, g/cm3) correcting the values for height [14]. The 2002 China National Nutrition and Health Survey (CNNHS) found that the average calcium intake was 376 mg/day for boys and 343 mg/day for girls aged 14–17 years [15], which was only about 30% of calcium adequate intake (AI, 1000 mg/day). The gap between recommended AI and actual calcium intake, as well as the factors that potentially affect calcium balance, varied widely in a group of Chinese
J. Yin et al. / Bone 46 (2010) 162–166
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Material and methods
water of all subjects were collected and processed daily for 10 days. Urine samples were 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. The urine was acidified using concentrated hydrochloric acid (1%, by vol.). Fecal samples were collected in preweighed containers and pooled as 24-h collections, diluted with concentrated hydrochloric acid and double distilled water, and homogenized with a blender. All samples were frozen at −20 °C. Aliquots were sampled. Samples and calcium carbonate tablets were digested using the wet method [16]. Calcium in samples was measured with inductively coupled plasma atomic emission spectrometry (Optima 3000, Perkin Elmer).
Study population
Anthropometric measurement
A total of 337 healthy adolescents (average 13.5 years old) were recruited from two junior middle schools in Beijing, China (172 boys, 165 girls). Students were randomly assigned to four groups stratified by gender, each group included about 40 students. Each participant ate three pieces of chewable calcium carbonate tablets each day. Supplementation doses of calcium in the four groups were 63, 354, 660, and 966 mg/day, respectively. All subjects completed questionnaires about medical and family fracture history. Those with any family history of bone or arthritic diseases, intake of medicine that could affect bone or cartilage or calcium metabolism, were excluded. Compliance of calcium supplementation was estimated 1 year later with an interview about recalling intakes of calcium tablets during holidays and study terms. After 1 year, 10 boys and 10 girls (aged 12–17 years) were randomly selected from each group to participate in a 10-day balance study. These 80 students were asked to live in schools and during a 3-day adaptation period and 7-day metabolism period. The study protocol and questionnaires used were approved by the Ethical Committee of National Institute for Nutrition and Food Safety, Chinese Center for Disease Control and Prevention. A written consent form was obtained from each participant and his/her guardian.
Height and weight were measured in a standing position wearing indoor clothing following a standardized procedure by trained interviewers. Body mass index (BMI) was calculated as weight in kilograms divided by height in meters squared (kg/m2). Information on past illnesses and date of first spermatorrhea in boys or menarche in girls was obtained using interview-administrated questionnaires.
adolescents. Therefore, the body of evidence required to formulate recommendations for calcium intake in this population is currently insufficient and requires additional metabolic studies. Calcium balance studies provide one of the most important lines of evidence for the development of calcium DRIs. In this paper we discuss characteristics of calcium metabolism and some potential influencing factors in Chinese adolescents undergoing calcium balance assessment. These results may provide the basis for developing calcium DRIs to guide adolescents on calcium intake, which is of great importance for the prevention of osteoporosis.
Food preparation and intakes A 3-day cycle menu was developed referring to local dietary habits and vegetables supplied by market. Actual food intakes were recorded in every meal by weighing each food before and after meals were consumed. Subjects were asked to only consume foods prepared by the staff during the adaptation period and metabolism period, and were asked to eat a calcium carbonate tablet under the supervision of staff before each meal. We supplied similar foods to every student and encouraged them to eat as during the prior 12 months. Collection and measurement of metabolic samples Samples of cooked foods were collected and homogenized using a blender with blades of stainless steel. Samples of feces, urine, and
Dietary intake Dietary intake during the calcium supplementation study was assessed with a 24-h dietary recall method for 3 consecutive days (two weekdays and one weekend day) by trained interviewers. The Chinese Food Composition Tables were used to calculate nutrient intakes [17]. Statistical analysis Calcium retention was determined by calcium intake minus urinary and fecal calcium excretion during balance period. Calcium apparent absorption efficiency was determined by calcium intake minus fecal calcium excretion, and then divided by calcium intakes. One-way ANOVA was used for analyzing differences in age, height, body weight, BMI, pubertal development, calcium intake, and retention among the four groups. The Kruskal–Wallis test was used for analyzing calcium apparent absorption efficiency. P values less than 0.05 were considered significant. The factors which might be related to calcium absorption and retention potentially were analyzed using multivariable stepwise regression. Pubertal development was classified as the first spermatorrhea or menarche, 12 months for boys and 24 months for girls. Pubertal development entered in the models as a categorical variable. P values for entry and removal of terms into and out of the model were 0.10. Curve estimations of calcium apparent absorption efficiency and calcium retention were done with calcium intake as the independent variable. All statistical analysis was done with the SAS Statistical Package (SAS 8.2e for Windows, SAS Institute, Inc.).
Table 1 Comparison on characteristics of subjects among four groups. Boys
n (n1) Age (years) Height (cm) Weight (kg) BMI (kg/m2) Period (mo)a
Girls
Group 1
Group 2
Group 3
Group 4
Group 1
Group 2
Group 3
Group 4
9 (8) 15.3 ± 0.7 167.3 ± 8.6 63.6 ± 18.6 22.6 ± 6.1 14 ± 6
10 (8) 15.5 ± 0.5 169.0 ± 5.2 57.7 ± 9.2 20.2 ± 2.4 13 ± 6
9 (7) 15.3 ± 0.5 170.4 ± 9.8 59.8 ± 6.2 20.7 ± 2.5 22 ± 15
7 (5) 15.2 ± 0.7 166.4 ± 5.1 56.8 ± 13.4 20.3 ± 3.5 15 ± 11
10 (10) 14.6 ± 1.1 159.0 ± 5.6 53.3 ± 12.1 20.9 ± 3.6 29 ± 16
8 (8) 14.9 ± 0.8 157.9 ± 6.5 52.7 ± 10.7 21.0 ± 3.1 34 ± 22
10 (10) 15.0 ± 1.1 159.0 ± 6.0 52.5 ± 6.3 20.7 ± 2.1 32 ± 10
10 (10) 14.7 ± 0.8 159.9 ± 6.1 51.1 ± 6.7 19.9 ± 1.7 30 ± 9
One-way ANOVA test among four groups, P N 0.05. n1, number after first spermatorrhea or menarche. a Months since spermatorrhea for boys, or months since menarche for girls.
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Table 2 Comparison on Ca metabolic balance among four groups ðx F sÞ.
Boys (n = 37) Ca intake from dietary and water (mg/day) Total Ca intake (mg/day) Urine Ca (mg/day) Feces Ca (mg/day) Ca retention (mg/day) Ca apparent absorption efficiency (%) Girls (n = 38) Ca intake from dietary and water (mg/day) Total Ca intake (mg/day) Urine Ca (mg/day) Feces Ca (mg/day) Ca retention (mg/day) Ca apparent absorption efficiency (%)
Group 1
Group 2
Group 3
Group 4
P
352.0 ± 56.4 427.1 ± 48.2a 55.0 ± 31.9 129.0 ± 28.0a 243.1 ± 82.1a 69.3
369.6 ± 64.6 723.6 ± 64.6b 74.1 ± 37.3 177.1 ± 83.8a,b 472.4 ± 109.2b 75.3
308.2 ± 81.2 1002.0 ± 46.2c 115.0 ± 57.5 291.8 ± 139.2b 595.5 ± 153.9b,c 71.0
345.1 ± 100.5 1323.0 ± 85.1d 94.2 ± 78.5 582.7 ± 180.9c 645.7 ± 196.0c 55.6
0.368 0.000 0.128 0.000 0.000 0.057
289.4 ± 51.3 352.4 ± 51.3a 110.3 ± 64.6 161.8 ± 69.9a 80.3 ± 60.1a 55.0
265.9 ± 40.9 619.9 ± 40.9b 156.0 ± 66.7 326.9 ± 117.8b 137.0 ± 102.0a,b 47.6
305.6 ± 39.1 965.6 ± 39.1c 186.3 ± 53.6 550.0 ± 91.8c 229.3 ± 103.1b 43.0
294.2 ± 40.8 1260.0 ± 40.8d 154.4 ± 59.2 750.8 ± 120.6d 355.0 ± 127.9c 40.4
0.296 0.000 0.065 0.000 0.000 0.136
One-way ANOVA. Kruskal–Wallis Test for rate comparison. a,b,c,d Different letter means there were significant difference between groups.
A total of 73 of 80 students completed the 10-day metabolic balance study. The characteristics of the subjects appear in Table 1. The average age of subjects was 15.1 ± 0.8 years. There were no significant differences in age, height, and body weight among the four groups (P N 0.05). First spermatorrhea occurred in the past 12 months for 13 boys, and menarche occurred 24 months ago for 27 girls. The total calcium intakes (from dietary, water, and calcium carbonate tablets) of boys were 427, 724, 1002, and 1323 mg/day for four groups, respectively, while that of girls were 352, 620, 966, and 1260 mg/day. Calcium retention as well as calcium excreted in feces increased significantly with total calcium intake among the four groups (P b 0.05), but there were no significant differences among the four groups on calcium intake from dietary and water, calcium apparent absorption efficiency, and calcium excreted in urine (Table 2). The average calcium intake was similar between boys and girls (839 mg/day vs. 809 mg/day), but calcium apparent absorption efficiency as well as retention differed significantly between boys and girls (46.4% vs. 68.7%, 480 mg/day vs. 204 mg/day) (P b 0.05)
(Table 2). Calcium intake, retention, and apparent absorption efficiency of boys were significantly higher than that of their girl counterparts in respective groups (P b 0.05). Using curve estimation, calcium retention increased with calcium intake, but did not reach a plateau in both boys and girls. Trends of Ca absorption efficiency differed between boys and girls. Calcium absorption efficiency increased to 78.6% in boys when their calcium intakes reached 665 mg/day, but then decreased with more calcium intakes. However, in girls, calcium absorption efficiency decreased with calcium intake, and the plateau of calcium apparent absorption efficiency approached 45.0% when calcium intake was 650 mg/day (Figs. 1 and 2). Using multivariable stepwise regression, we found that sex and calcium intake were the two most important contributors for calcium balance in Chinese adolescents, explaining about 50% of the variability in calcium absorption, with pubertal development also playing a role. Calcium apparent absorption efficiency increased in boys with time after first spermatorrhea, peaking at 12 months and decreasing thereafter. Calcium apparent absorption efficiency decreased in girls with time after menarche up to 24 months, and steadied after that. Sex, calcium intake, and age were the most important determinants for calcium retention, explaining 74.5% of variability in calcium retention (Table 3, Fig. 3).
Fig. 1. Relationship between Ca intake and Ca metabolism balance in boys.
Fig. 2. Relationship between Ca intake and Ca metabolism balance in girls.
Results
J. Yin et al. / Bone 46 (2010) 162–166 Table 3 Multivariable stepwise regression analysis with Ca apparent absorption efficiency or Ca retention as a dependent variable and age, sex, weight, height, Ca intake, and pubertal development as independent variables. β
SE
Standard β P
Ca apparent absorption efficiency 0.508 Sex 21.044 3.217 0.593 Ca intake −0.015 0.004 −0.294 Pubertal development −5.953 3.229 −0.167 Ca retention Sex 291.457 28.714 0.66 Ca intake 0.367 0.04 0.567 Age −51.734 17.918 −0.188
0.000 0.001 0.07 0.745 0.000 0.000 0.005
R2 0.394 0.089 0.025 0.404 0.309 0.032
Both standard of enter model and remove model were 0.10. Pubertal development was classified by periods between Ca balance experiment and first spermatorrhea or menarche: 12 months for boys and 24 months for girls.
Discussion This study represents the first attempt to evaluate calcium balance among Chinese adolescents over 1-year period and to evaluate characteristics and potential influencing factors of calcium metabolism and calcium balance in Chinese adolescents, including sex, age, calcium intake, and pubertal development in order to develop calcium DRIs based on characteristics of calcium balance in Chinese adolescents. It was recommended to use gender- and ethnic-specific standards for interpreting pediatric bone densitometry data [18]. There were significant differences in calcium absorption and retention between boys and girls in this study, which probably reflected differences in stage of pubertal development between boys and girls. At the time of this study, first spermatorrhea or menarche had been experienced by most subjects, and girls were more mature in pubertal development than boys. Bachrach et al. reported that Black and Asian females and Asian males tended to reach a plateau in BMD earlier than the other ethnic groups [18]. Martin et al. found BMC velocity peak at 13.3 years of age for boys and 11.4 years for girls in Canada. Within 3 years on either side of peak BMC velocity peak, boys had consistently higher BMC and BMC velocity compared with girls and the discrepancy increased steadily through puberty [19]. The rates of bone calcium deposition reached a maximum in girls shortly before menarche, which was approximately five times that of adulthood, and the decline in bone calcium deposition rate is gradual after menarche [20]. Girls in this study were in the stage of slower BMC velocity, but boys were at the peak in BMC velocity, which could contribute to observed differences in calcium absorption and retention. In this study, we found that pubertal development explained only 2.5% of the variability in calcium absorption. Calcium absorption of girls in this study was 46.4%, which was 52–55% in Chinese girls in 9–11.5 years before menarche [21], but 34% in Chinese young women aged 18–23 years [22]. Calcium absorption of girls in this study was shown in Fig. 3, which indicated calcium absorption decreased with pubertal development in Chinese girls. Calcium absorption of Chinese girls in this study was similar to postmenarcheal girls who were Black (44%), but not those who were White (25%) [23]. Calcium absorption of Chinese boys in this study was higher than true fractional calcium absorption (61%) in 7-year-old Chinese children [24], and was significantly higher than that in pubertal Caucasian boys (30%) [25]. Sex and calcium intake were found to be the most important contributions to calcium balance in Chinese adolescents, which explained more than 70% of variability in calcium retention. Of these, calcium intake explained about 30% of variation. A recent metabolic study in White American boys aged 13–15 years found that calcium intake explained 21.7% of the variability in calcium retention, suggesting that calcium intake is the greatest predictor of calcium retention in adolescent boys [26]. Weaver reviewed that dietary calcium could predict 10–15% of skeletal calcium retention during
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adolescence with race and sexual maturity in the model [27]. These studies support the notion that adequate calcium intake during adolescence is important for calcium retention and bone accrual during skeletal growth. We did not achieve a plateau of calcium retention in this study, but we tried to calculate calcium requirement for Chinese adolescents using the results of other studies, such as studies on daily calcium retention in bone. Martin found that PBMCV was 320 g/year in boys and 240 g/year in girls. Assuming that calcium comprises 40% of bone mineral [28], Zhai et al. found that maximal daily calcium retention was 338 mg in Chinese boys and 261 mg in girls with a cross-sectional study [29]. To maintain these values for the skeleton, taking into account 100 mg for urinary calcium, and 40 mg for other losses not accounted for elsewhere, the net absorbed calcium during this period needs to be 478 mg/day for boys and 401 mg/day for girls. This requires an intake of 625 mg/day for boys and 872 mg/day for girls. To meet the needs of pubertal development, we presumed that recommended adequate intakes of calcium were more than 600 mg/ day in 12- to 17-year-old boys and 900–1000 mg/day in girls during the phase of peak growth, values that differ greatly from recommended intakes for American boys. Braun found that maximal calcium retention in 12- to 15-year boys was achieved at an intake of 1140 mg/day. Calcium retention was higher (by 171 ± 38 mg/day) in boys than in girls at all calcium intakes studied [30]. This difference could be the result of ethnic variability in calcium absorption and retention. Blacks had 185 mg/day greater mean skeletal calcium retention than did Whites as a result of significantly greater net calcium absorption and lower calcium excretion [31].There are several limitations in our results. Firstly, subjects in this study had taken part in the intervention study of calcium supplementation for 1 year, but only 60% complied with calcium supplementation when they recalled actual tablet intakes after the study. This might be one explanation of the observed high absorption efficiency, although we included a 3-day adaptation period. Longer balance equilibration periods may be helpful in future studies. Secondly, we did not document the progression of pubertal development by Tanner stage in this study. Pubertal information was collected prior to initiating the supplementation program, which precluded stratifying study results by Tanner stage. We analyzed pubertal development with date of first spermatorrhea in boys or menarche in girls, which might be difficult to evaluate in boys and might cause recall bias. Lastly, no fecal markers were used in this study; therefore, we could only estimate true
Fig. 3. Trends of Ca absorption with pubertal development. Ca absorption efficiency decreased with pubertal development in girls, but increased in boys within 1 year after first spermatorrhea.
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calcium absorption and excretion compliance. Based on these results, we suggest that adequate intakes of calcium for Chinese adolescents exceed 600 mg/day in 12- to 17-year-old boys and 900–1000 mg/day in girls during the peak growth phase. Further metabolic balance studies with biochemical markers are needed to confirm these results. In conclusion, sex, calcium intake, age, and pubertal development are important contributors for calcium retention and absorption during skeletal growth. These factors should be taken into consideration for the development of calcium DRIs in Chinese adolescents. Acknowledgments The authors wish to thank all subjects for their participation in this study. A special thanks to Dr. Laura Laslett for assistance on English reviewing. This study was supported by China National Natural Science Foundation (Project No. 30471453). References [1] Lee WT, Jiang J. Calcium requirements for Asian children and adolescents. Asia Pac J Clin Nutr 2008;17(Suppl 1):33. [2] Report of a Joint FAO/WHO Expert Consultation. Human vitamin and mineral requirements; 2002. [3] Weaver CM. The growing years and prevention of osteoporosis in later life. Proc Nutr Soc 2000;59:303–6. [4] Matkovic V, Jelic T, Wardlaw GM, et al. Timing of peak bone mass in Caucasian females and its implication for the prevention of osteoporosis. Inference from a cross-sectional model. J Clin Invest 1994;93:799–808. [5] Suuriniemi M, Mahonen A, Kovanen V, et al. Association between exercise and pubertal BMD is modulated by estrogen receptor alpha genotype. J Bone Miner Res 2004;19:1758–65. [6] Bhudhikanok GS, Wang MC, Eckert K, Matkin C, Marcus R, Bachrach LK. Differences in bone mineral in young Asian and Caucasian Americans may reflect differences in bone size. J Bone Miner Res 1996;11:1545–56. [7] Wang MC, Aguirre M, Bhudhikanok GS, Kendall CG, Kirsch S, Marcus R, Bachrach LK. Bone mass and hip axis length in healthy Asian, black, Hispanic, and white American youths. J Bone Miner Res 1997;12:1922–35. [8] Abrams SA, Griffin IJ, Hawthorne KM, et al. Vitamin D receptor Fok1 polymorphisms affect calcium absorption, kinetics, and bone mineralization rates during puberty. J Bone Miner Res 2005;20:945–53. [9] Ames SK, Ellis KJ, Gunn SK, Copeland KC, Abrams SA. Vitamin D receptor gene Fok1 polymorphism predicts calcium absorption and bone mineral density in children. J Bone Miner Res 1999;14:740–6.
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