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Journal of Clinical Endocrinology & Metabolism, doi:10.1210/jc.2005-0537
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The Journal of Clinical Endocrinology & Metabolism Vol. 90, No. 9 5077-5081
Copyright © 2005 by The Endocrine Society

Height and Height Z-Score Are Related to Calcium Absorption in Five- to Fifteen-Year-Old Girls

Steven A. Abrams, Ian J. Griffin, Keli M. Hawthorne and Lily Liang

United States Department of Agriculture/Agricultural Research Service, Children’s Nutrition Research Center; and Department of Pediatrics, Sections of Nutrition and Neonatology, Baylor College of Medicine and Texas Children’s Hospital, Houston, Texas 77030

Address all correspondence and requests for reprints to: Steven A. Abrams, M.D., United States Department of Agriculture/Agricultural Research Service, Children’s Nutrition Research Center, 1100 Bates Street, Houston, Texas 77030. E-mail: sabrams{at}bcm.edu.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Context: Understanding the relationship between calcium absorption and growth has been limited. We have developed a database of calcium absorption measurements in 315 girls aged 5.0–15.0 yr.

Design: We have used this database to assess the relationship between height, its age- and gender-normalized value (height Z-score), and calcium absorptive efficiency.

Results: Overall, height was significantly related to calcium absorption (corrected for calcium intake, age, Tanner, stage, and ethnicity) (P = 0.001). Similarly, height Z-score was significantly related to calcium absorption (P < 0.007). About 3–3.5% of the variability ({eta}2) of absorption was associated with height or height Z-score. We found that calcium absorption was significantly lower in girls with height Z-score equal to or less than zero compared with those with a height Z-score more than zero (difference, 3.9 ± 1.4%, mean ± SEM; P = 0.007). Limiting the analysis to those girls in which Tanner staging was performed or those age 9 yr or older did not substantively affect these relationships.

Conclusion: These results indicate that a small but significant component of the variability in calcium absorption is due to height. Identifying genetic risk factors for lowered calcium absorption during growth could lead to individual approaches for prevention of inadequate bone mass.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
THE RAPID ACQUISITION of bone mineral during pubertal growth usually appears to be supported by an increased absorption of dietary calcium rather than an increased intake of dietary calcium or decreased excretion of calcium (1, 2). This regulatory adaptation is similar to that which occurs during pregnancy and is dependent on an adequate vitamin D status (3, 4). We have demonstrated that a specific polymorphism of the vitamin D receptor Fok1 gene was highly related to calcium absorption in pubertal children (5, 6). Our data further suggested a link between calcium absorption and height during growth, but the database was too small and too limited in age range to clearly identify this relationship (6).

Although it is reasonable to hypothesize that dietary calcium absorptive efficiency during childhood and adolescence is partly regulated by the body’s need for calcium to support longitudinal growth, no data demonstrate this relationship. This is due to the relatively small scale and limited accuracy of many calcium balance studies done before 1950 (1) and the small number of studies performed since then using more accurate techniques (7, 8).

Recently, the importance of understanding this relationship has increased due to confusing data regarding the effects of calcium supplementation in children. Several studies have failed to find benefit to supplementation over a long period of time, especially after the supplements were stopped (9, 10, 11). The longest supplementation study (9) found that a benefit to calcium supplementation was present only for those girls whose height was greater (after the end of their growth phase) than average for the study population. Although previous studies had demonstrated a link between milk supplementation and longitudinal growth, such studies generally were performed in subjects at risk for growth failure or with very low calcium intakes (12, 13, 14).

We have conducted studies of calcium absorption in girls at a single medical center using the reference dual-tracer stable isotope method for more than 13 yr. Most of our studies have involved no interventions other than manipulation of calcium intake and have used virtually identical dietary and absorptive measurement methods. Our database of absorptive measurements is larger than recent studies using reliable methodologies (7, 15). We have pooled the data from our studies for this analysis with the intent of specifically identifying the relationship during growth between calcium absorption and height. We hypothesized that the genetic growth potential, as assessed by the height Z-score, would be significantly related to calcium absorption during growth.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Calcium absorption (reported as percentage of dietary calcium absorbed and referred to in this manuscript as "calcium absorptive efficiency") was measured in a total of 315 healthy girls aged 5.0–15.0 yr. These measurements were made as part of nine separate previously published human research investigations that were conducted in the Metabolic Research Unit of the Children’s Nutrition Research Center or the adjacent General Clinical Research Center of Texas Children’s Hospital over a 13-yr period from 1991 to 2004. To be enrolled in the protocols, girls had to be free of any chronic illness, not receiving any medications including vitamin or mineral supplements or hormones, nonsmokers, and usually needed to be not overweight based on estimates of body weight and height obtained from parents during telephone screening.

No duplicate measurements of the same subject were used for this analysis. Of the 315 measurements, 201 were from four investigations related to calcium absorption and kinetics in which no dietary manipulations occurred before the study (2, 5, 6, 16, 17, 18, 19, 20). An additional 60 measurements were from two investigations that compared absorption on very low calcium intakes with absorption on recommended intakes (21, 22). In this case, the measurement made at the normal intake was used. An additional 54 were from three investigations of calcium absorption from various dietary sources of calcium or with various food calcium supplements (23, 24, 25). Included in this analysis are only the first measurements for which subjects received milk or calcium-fortified orange juice without any supplements.

The analytical methods and balance protocols all have been described in detail previously (2, 5, 6, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25). All measurements were conducted using a dual-tracer stable isotope method: one calcium isotope was given orally (usually 46Ca) and a second intravenously (usually 42Ca). Calcium absorption was determined from the relative recovery of the oral tracer compared with the intravenous tracer during the 24 h after dosing.

Written informed consent was obtained from a parent or legal guardian for each subject; written or verbal assent was obtained based on age from study subjects. The Institutional Review Board of Baylor College of Medicine and Affiliated Hospitals approved all protocols. No complications related to the isotope studies were seen in any subjects.

Dietary methods were standardized in all investigations. Based on the planned dietary intake for the 24 h of the study, subjects received approximately one third of the calcium at breakfast, into which the calcium stable isotope had been mixed. Complete weighed 24- to 72-h dietary intakes were performed. In studies in which the diet was manipulated to a high or low intake, adaptation had been done for at least 14 d beforehand. Approximately half of the studies were performed using the oral isotope mixed with milk and approximately half with isotope mixed in calcium-fortified orange juice. We have shown previously that these sources produce no significant differences in calcium absorption (25).

In early investigations, we used self-assessment of Tanner staging (n = 101 girls). In later investigations (n = 214 girls), Tanner stage was assessed by physical examination performed by one of two pediatric endocrinologists or a specially trained pediatric nurse. Because self-assessment might not be accurate, we have included the Tanner stage data (breast staging) only for the measurements in which it was assessed by physical exam.

The 5.0- to 15.0-yr age range of subjects included studies of prepubertal and pubertal girls. Calcium absorptive efficiency increases during pubertal growth (2), which might affect the relationship between it and height and height Z-score. In addition to including Tanner stage (when available) as covariates in analyses, we also performed additional analysis of the data limited to girls equal to or more than 9.0 yr old.

Statistical methods

Height Z-scores were determined using the Epi Info program (version 3.3; Center for Disease Control and Prevention, Atlanta, GA). Within this program, we chose the most globally used standard: height Z-scores based on the 1978 World Health Organization/Center for Disease Control and Prevention database.

Analyses were performed using a generalized linear model analysis of covariance (ANCOVA) with covariate adjustment based on the specific analysis conducted using SPSS (Windows version 12.0). Age, calcium intake, and ethnicity were covariates in all models. Other covariates (such as Tanner stage) were included in some analyses. In most cases, calcium absorptive efficiency was the dependent variable, and height, or height Z-score, was the independent variable.

Data are reported for the magnitude of effect of height and its Z-score on absorption using the partial {eta}2 calculation of SPSS, the use of which in this type of analysis has been described previously (26). {eta}2 is the percentage of variation in the dependent variable (calcium absorptive efficiency) that is accounted for the independent variable after controlling for other independent covariates. All data are shown as mean ± SEM.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Subject characteristics

Mean age of the study subjects was 11.0 ± 0.1 yr. Their mean height was 146.3 ± 0.7 cm, and mean height Z-score was 0.26 ± 0.06. The mean calcium intake was 1105 ± 20 mg/d (27.62 ± 0.50 mmol/d), and their mean calcium absorptive efficiency was 35.6 ± 0.7%. A distribution plot of height Z-score and fractional absorption are shown as Fig. 1Go, A and B. Of the 214 girls for whom Tanner stage was available (breast), 16.4% were Tanner stage 1, 32.7% Tanner stage 2, 24.3% Tanner stage 3, 9.3% Tanner stage 4, and 1.9% Tanner stage 5. Overall, 52.4% of the 315 girls were non-Hispanic Caucasians, 28.3% African Americans, 14.9% Hispanics, and 4.4% Asians. Although subjects who were identified as overweight during the recruitment process were excluded from these studies, a few subjects were found to be overweight at the time of the study but were allowed to continue. Mean body mass index (BMI) was 18.7 ± 0.2 kg/m2. Of the 315 girls, 15 had a BMI more than 25.0 kg/m2, and only one had a BMI more than 30.0 kg/m2.



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  		FIG. 1. Histograms of height Z-score distribution (A) and calcium absorption distribution (B) for 315 measurements in 315 girls aged 5–15 yr. Data are divided into 30 increments for histogram.

 
Relationship between height and height Z-score and calcium absorption

Results for the relationship between calcium absorption efficiency and height and height Z-score are shown in Tables 1Go and 2Go, respectively. Results are very similar and show a significant relationship of both height and height Z-score to calcium absorption in both the whole group and in the subanalysis limited to those in which Tanner staging was done and those equal to or more than 9 yr of age.


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  		TABLE 1. Relationship of height and other factors to calcium absorptive efficiency (percentage dietary calcium absorbed) in girls aged 5–15 yr

 

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  		TABLE 2. Relationship of height Z-score and other factors to calcium absorptive efficiency (percentage dietary calcium absorbed) in girls aged 5–15 yr

 
In general, about 3–3.5% of the variability in calcium absorptive efficiency (partial {eta}2) was related to height or height Z-score (Tables 1Go and 2Go). We did not include body weight as a covariate in the analyses shown in the tables. When included as a covariate with age, ethnicity, calcium intake, and height or height Z-score, body weight was not closely related to calcium absorptive efficiency (P > 0.4). Performing analyses using the logarithmic transform of calcium absorptive efficiency also did not substantially affect the results.

The relationship between height Z-score and calcium absorptive efficiency also was assessed using linear regression analysis without correcting for age, ethnicity, or intake. This result (Fig. 2Go) showed a significant correlation (r = 0.18; P = 0.001).



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  		FIG. 2. Relationship between height Z-score and calcium absorption. n = 315; y = 2.12x + 35.1; r = 0.18; P = 0.0013.

 
Comparison of absorption for subjects based on height Z-score

To determine the magnitude of the effect on calcium absorption of less than average height compared with greater than average height, the calcium absorption for those measurements conducted in subjects with height Z-scores more than 0 were compared with those conducted in subjects with Z-scores equal to or less than 0. Results showed a significantly greater absorption, 36.1 ± 1.2% (n = 191), for those with height Z-score more than 0, compared with 32.2 ± 1.3% (n = 124) for those with height Z-scores equal to or less than 0, for a difference of 3.9 ± 1.4% (P = 0.007).


   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
Achieving peak bone mass in adolescence is believed to be an important aspect of reducing the ultimate risk of osteoporosis (8, 27). Although increased calcium intakes are strongly recommended during pubertal growth, more than 80% of U.S. girls do not reach recommended intakes, and often calcium intake is increased minimally or even decreases during puberty, especially in girls (8). Therefore, because urinary calcium excretion slightly increases during puberty, adaptation to meet bone mineral accretion needs must come via increasing the proportion of dietary calcium that is absorbed, i.e. increasing calcium absorptive efficiency.

Our finding of a significant relationship between height Z-score (and height) and calcium absorptive efficiency demonstrates that the increase in absorptive efficiency is partly regulated to meet the needs of the ultimate skeletal size. Height is a highly heritable characteristic that demonstrates close tracking during puberty (28, 29). By using the height Z-score in this analysis, we specifically identified the effects on calcium absorption of being above or below the average population height. Although the percentage of absorptive efficiency variation accounted for by height or its Z-score was small (3–3.5%), this relationship has not been identified previously and was comparable in magnitude with the variation accounted for by previously identified factors such as age and calcium intake. Furthermore, the differences in calcium absorptive efficiency between those with height Z-scores equal to or less than 0 and those with height Z-scores more than 0 of 3.9% would represent a substantial distinction close to that of the increase of calcium absorptive efficiency during early puberty (20).

As expected, Tanner stage was significantly correlated to calcium absorption (Table 1Go); however, this was not significant when height Z-score rather than actual height was used as the covariate. Although it is apparent that pubertal progression affects calcium absorption efficiency (7), there remains a significant relationship between height and its Z-score and calcium absorption efficiency when pubertal stage is considered.

We did not assess the relationship between calcium absorption efficiency and bone mineralization. Bone mineralization data were not available for many of the subjects in this study. For one of the individual studies that provided 50 subjects to this database, total body bone mineral content Z-scores were available. For these subjects, when combined with 49 boys of similar ages (6), we found a marginal significant relationship between whole body bone mineral content and height Z-score (P = 0.09) (Abrams, S. A., unpublished observation). This lower significance may be related to the smaller sample size and inclusion of males and females but may also reflect the multiple other factors, such as body weight, that are associated with bone mineralization.

Bone mineralization is highly dependent on weight as well as height during childhood (12, 30, 31), and we did not find a significant relationship between weight when used as a covariate with height and calcium absorptive efficiency. Furthermore, the optimal measures of bone mineral status during childhood and adolescence are unclear, and large database Z-score data are not available for whole body or regional bone mineral content (or density) in pediatric populations compared with the well-established globally derived height Z-score data. It is reasonable to hypothesize that calcium absorption efficiency during growth is more closely related to height than bone mineral content, but this would require additional investigation.

The mechanism by which height and height Z-score is related to calcium absorption efficiency is uncertain. Our findings support a genetic component regulating calcium absorption efficiency during childhood, a finding consistent with identified genetic effects such as differences between males and females in skeletal calcium accretion during puberty (30, 31) and ethnic differences in calcium absorption (15). Additional evidence for a genetic regulation of calcium absorptive efficiency is our finding that a specific polymorphism of vitamin D receptor, the Fok1 genotype, was significantly related to both calcium absorption and bone mineralization in a group of pubertal boys and girls (5, 6).

It is also possible that a significant aspect of this relationship is attributable directly to the larger intestinal surface of taller individuals. This is consistent with the findings that a relationship between calcium absorption and height is present as well in adults (Heaney, R. P., personal communication). However, our dataset of growing children in which absorption is linked to both height and height Z-score, but less so with chronological age, suggest a genetic component as well, at least during growth.

Although it has been known for many years that increased calcium intake, such as by milk drinking (13, 14), is associated with an increase in height, such data were collected mostly on individuals with very low calcium intakes or significant malnutrition. Also, results conflict over the benefits of high calcium intakes and even milk drinking for ultimate bone mass in adolescents (32). Several recent studies have not confirmed a substantial long-term benefit to calcium supplementation for increasing bone mineral density (9, 10, 11, 32). One recent study demonstrated that calcium supplementation above a baseline of 800 mg/d enhanced bone mineral density in girls who were above the average height of the group but not for those who were below the average height (9).

Clearly, an adaptive mechanism of increased calcium absorptive efficiency could be inadequate to meet the needs of very tall individuals or those with a severely deficient calcium intake, especially over a prolonged period of time (22). However, the results of recent controlled trials generally suggest that adequate mineralization of the skeleton does not require very high calcium intake levels during growth (11, 32). The ability to adapt calcium absorptive efficiency to biological needs for calcium is likely part of the reason that more moderate calcium intakes are adequate even during pubertal growth (9, 11, 32). Subjects with underlying health problems such as malabsorptive states may not adapt well, however, and could require higher intakes of calcium and vitamin D.

In summary, using a large database of clinical studies, we demonstrated that height and its age- and gender-normalized Z-score are significant predictors of calcium absorptive efficiency in girls during childhood and early adolescence. These findings further support the concept of genetic regulation of calcium absorptive efficiency, especially in supporting skeletal growth. Ultimately, individual risk profiles based on a variety of factors (e.g. gender, parental height, medical conditions, genetic polymorphisms, and family history of osteoporosis) might be used to establish individual risk analyses by which appropriate monitoring and intervention can be proposed at an early age.


   Acknowledgments
 
We acknowledge the assistance of the nursing staff of the Metabolic Research Unit of the Children’s Nutrition Research Center and the General Clinical Research Center of Texas Children’s Hospital for caring for the study subjects; Sheila Gunn, M.D., Kenneth Copeland, M.D., and Dorothy Powledge, R.N., for Tanner staging; and E. O’Brian Smith, Ph.D., for biostatistical review.


   Footnotes
 
This work was supported in part with federal funds from the United States Department of Agriculture (USDA)/Agricultural Research Service (ARS) under Cooperative Agreement 58-6250-6-001, and the National Institutes of Health/National Center for Research Resources General Clinical Research for Children Grants RR00188, AR43740, and HD36591.

This work is a publication of the USDA/ARS, Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine and Texas Children’s Hospital, Houston, Texas. Contents of this publication do not necessarily reflect the views or policies of the USDA, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government.

First Published Online May 17, 2005

Abbreviations: ANCOVA, Analysis of covariance; BMI, body mass index.

Received March 10, 2005.

Accepted May 5, 2005.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

  1. Matkovic V 1991 Calcium metabolism and calcium requirements during skeletal modeling and consolidation of bone mass. Am J Clin Nutr 54:245S–260S
  2. Abrams SA, Stuff JE 1994 Calcium metabolism in girls: current dietary intakes lead to low rates of calcium absorption and retention during puberty. Am J Clin Nutr 60:739–743[Abstract/Free Full Text]
  3. Outila TA, Karkkainen MU, Lamberg-Allardt CJ 2001 Vitamin D status affects serum parathyroid hormone concentrations during winter in female adolescents: associations with forearm bone mineral density. Am J Clin Nutr 74:206–210[Abstract/Free Full Text]
  4. Ritchie LD, Fung EB, Halloran BP, Turnlund JR, Van Loan MD, Carr CE, King JC 1998 A longitudinal study of calcium homeostasis during human pregnancy and lactation and after resumption of menses. Am J Clin Nutr 67:693–701[Abstract]
  5. Ames SK, Ellis KJ, Gunn SK, Copeland KC, Abrams SA 1999 Vitamin D receptor gene Fok1 polymorphism predicts calcium absorption and bone mineral density in children. J Bone Miner Res 14:740–746[CrossRef][Medline]
  6. Abrams SA, Griffin IJ, Hawthorne KM, Chen Z, Gunn SK, Wilde M, Darlington G, Shypailo R, Ellis K 2005 Vitamin D receptor Fok1 polymorphisms affect calcium absorption, kinetics and bone mineralization rates during puberty. J Bone Miner Res 20:945–953[CrossRef][Medline]
  7. Jackman LA, Millane SS, Martin BR, Wood OB, McCabe GP, Peacock M, Weaver CM 1997 Calcium retention in relation to calcium intake and postmenarcheal age in adolescent females. Am J Clin Nutr 66:327–333[Abstract/Free Full Text]
  8. Institute of Medicine (U.S.). Standing Committee on the Scientific Evaluation of Dietary Reference Intakes 1997 DRI, Dietary Reference Intakes: for calcium, phosphorus, magnesium, vitamin D, and fluoride. Washington, DC: National Academy Press
  9. Matkovic V, Goel PK, Badenhop-Stevens NE, Landoll JD, Li B, Ilich JZ, Skugor M, Nagode LA, Mobley SL, Ha EJ, Hangartner TN, Clairmont A 2005 Calcium supplementation and bone mineral density in females from childhood to young adulthood: a randomized controlled trial. Am J Clin Nutr 81:175–188[Abstract/Free Full Text]
  10. Chevalley T, Rizzoli R, Hans D, Ferrari S, Bonjour JP 2005 Interaction between calcium intake and menarcheal age on bone mass gain: an eight-year follow-up study from prepuberty to postmenarche. J Clin Endocrinol Metab 90:44–51[Abstract/Free Full Text]
  11. Lloyd T, Beck TJ, Lin HM, Tulchinsky M, Eggli DF, Oreskovic TL, Cavanagh PR, Seeman E 2002 Modifiable determinants of bone status in young women. Bone 30:416–421[Medline]
  12. Bonjour J-P, Theintz G, Buchs B, Slosman D, Rizzoli R 1991 Critical years and stages of puberty for spinal and femoral bone mass accumulation during adolescence. J Clin Endocrinol Metab 73:555–563[Abstract]
  13. Takahashi E 1984 Secular trend in milk consumption and growth in Japan. Hum Biol 56:427–437[Medline]
  14. Black RE, Williams SM, Jones IE, Goulding A 2002 Children who avoid drinking cow milk have low dietary calcium intakes and poor bone health. Am J Clin Nutr 76:675–680[Abstract/Free Full Text]
  15. Bryant RJ, Wastney ME, Martin BR Wood O, McCabe GP, Morshidi M, Smith DL, Peacock M, Weaver CM 2003 Racial differences in bone turnover and calcium metabolism in adolescent females. J Clin Endocrinol Metab 88:1043–1047[Abstract/Free Full Text]
  16. Abrams SA, O’Brien KO, Liang LK, Stuff JE 1995 Differences in calcium absorption and kinetics between black and white girls age 5–16 years. J Bone Miner Res 10:829–833[Medline]
  17. Abrams SA, Grusak MA, Stuff J, O’Brien KO 1997 Calcium and magnesium balance in 9–14-y-old children. Am J Clin Nutr 66:1172–1177[Abstract/Free Full Text]
  18. Bronner F, Abrams SA 1998 Development and regulation of calcium metabolism in healthy girls. J Nutr 128:1474–1480[Abstract/Free Full Text]
  19. Abrams SA, Copeland KC, Gunn SK, Stuff JE, Clarke LL, Ellis KJ 1999 Calcium absorption and kinetics are similar in 7- and 8-year-old Mexican-American and Caucasian girls despite hormonal differences. J Nutr 129:666–671[Abstract/Free Full Text]
  20. Abrams SA, Copeland KC, Gunn SK, Gundberg CM, Klein KO, Ellis KJ 2000 Calcium absorption, bone accretion and kinetics increase during early pubertal development in girls. J Clin Endocrinol Metab 85:1805–1808[Abstract/Free Full Text]
  21. O’Brien KO, Abrams SA, Liang LK, Ellis KJ, Gagel RF 1996 Increased efficiency of calcium absorption during short periods of inadequate intake in girls. Am J Clin Nutr 63:579–583[Abstract/Free Full Text]
  22. Abrams SA, Griffin IJ, Hicks PD, Gunn SK 2004 Pubertal girls only partially adapt to low dietary calcium intakes. J Bone Miner Res 19:759–763[CrossRef][Medline]
  23. Abrams SA, Griffin IJ, Davila P, Liang L 2001 Calcium fortification of breakfast cereal enhances calcium absorption in children without affecting iron absorption. J Pediatr 139:522–526[CrossRef][Medline]
  24. Griffin IJ, Davila PM, Abrams SA 2002 Non-digestible oligosaccharides and calcium absorption in girls with adequate calcium intakes. Br J Nutr. 87:S187–S191
  25. Abrams SA, Griffin IJ, Davila PM, Hawthorne KM 2003 Calcium absorption is similar from milk and two types of fortified orange juice at high intake levels. J Bone Miner Res. 18(Suppl 2):S104 (Abstract)
  26. Pierce CA, Block RA, Aguinis H 2004 Cautionary note on reporting eta-squared values from multifactor ANOVA designs. Educ Psychol Meas 64:916–924[Abstract]
  27. Heaney RP, Abrams SA, Dawson-Hughes B, Looker A, Marcus R, Matkovic V, Weaver C 2000 Peak bone mass. Osteoporos Int 11:985–1009[CrossRef][Medline]
  28. Ferrari S, Rizzoli R, Slosman D, Bonjour JP 1998 Familial resemblance for bone mineral mass is expressed before puberty. J Clin Endocrinol Metab 83:358–361[Abstract/Free Full Text]
  29. Loro ML, Sayre J, Roe TF, Goran MI, Kaufman FR, Gilsanz V 2000 Early identification of children predisposed to low peak bone mass and osteoporosis later in life. J Clin Endocrinol Metab 85:3908–3918[Abstract/Free Full Text]
  30. Bailey DA, Martin AD, McKay HA, Whiting S, Mirwald R 2000 Calcium accretion in girls and boys during puberty: a longitudinal analysis. J Bone Miner Res 11:2245–2250
  31. Whiting SJ, Vatanparast H, Baxter-Jones A, Faulkner RA, Mirwald R, Bailey DA 2004 Factors that affect bone mineral accrual in the adolescent growth spurt. J Nutr 134:696S–700S
  32. Ervin RB, Wang CY, Wright JD, Kennedy-Stephenson J 2004 Dietary intake of selected minerals for the United States population: 1999–2000. Adv Data 27:1–5



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