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The Journal of Clinical Endocrinology & Metabolism 90(9):5077–5081
Copyright © 2005 by The Endocrine Society
doi: 10.1210/jc.2005-0537
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
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 (␩2)
of absorption was associated with height or height Z-score. We found
T
HE 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
First Published Online May 17, 2005
Abbreviations: ANCOVA, Analysis of covariance; BMI, body mass
index.
JCEM is published monthly by The Endocrine Society (http://www.
endo-society.org), the foremost professional society serving the endocrine community.
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. (J Clin Endocrinol Metab 90: 5077–5081, 2005)
stopped (9 –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 (12–14).
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
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,
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J Clin Endocrinol Metab, September 2005, 90(9):5077–5081
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 –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 (23–25). 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 –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 selfassessment 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.
Abrams et al. • Height Effect on Calcium Absorption
Results
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. 1,
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 nonHispanic 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.
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
1 and 2, respectively. Results are very similar and show a
significant relationship of both height and height Z-score to
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 ␩2 calculation of SPSS, the use of which
in this type of analysis has been described previously (26). ␩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.
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.
Abrams et al. • Height Effect on Calcium Absorption
J Clin Endocrinol Metab, September 2005, 90(9):5077–5081
5079
TABLE 1. Relationship of height and other factors to calcium absorptive efficiency (percentage dietary calcium absorbed) in
girls aged 5–15 yr
Whole database
n
Height
Age
Calcium intake
Ethnicity
Tanner stage
315
0.001 (3.5)
0.07 (1.1)
0.004 (2.6)
0.004 (4.2)
Subjects in whom Tanner
staging was performeda
Age ⱖ 9.0 yr
214
0.007 (3.5)
0.15 (1.0)
0.07 (1.5)
0.17 (2.4)
0.008 (6.5)
271
0.01 (2.3)
0.03 (1.9)
0.002 (3.4)
0.011 (4.1)
Age ⱖ 9.0 yr and Tanner
staging performeda
189
0.01 (3.4)
0.71 (0.1)
0.03 (2.6)
0.20 (2.5)
0.51 (0.2)
P values for parameter (relationship to calcium absorptive efficiency) as determined by ANCOVA are shown with ␩2 values (as percentage)
given in parentheses.
a
Tanner stage (breast stage, assessed by physical exam) data were available for 214 of 315 subjects.
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.
In general, about 3–3.5% of the variability in calcium absorptive efficiency (partial ␩2) was related to height or height
Z-score (Tables 1 and 2). 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. 2) showed a significant correlation (r ⫽ 0.18; P ⫽
0.001).
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
Achieving peak bone mass in adolescence is believed to be
an important aspect of reducing the ultimate risk of osteo-
porosis (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 1); 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
TABLE 2. Relationship of height Z-score and other factors to calcium absorptive efficiency (percentage dietary calcium absorbed) in girls
aged 5–15 yr
Whole database
n
Height Z-score
Age
Calcium intake
Ethnicity
Tanner stage
315
0.007 (2.3)
0.053 (1.2)
0.006 (2.5)
0.003 (4.3)
Subjects in whom Tanner
staging was performeda
Age ⱖ 9.0 yr
214
0.007 (3.5)
0.08 (1.4)
0.02 (2.5)
0.24 (2.0)
0.74 (0.1)
271
0.049 (1.5)
0.76 (0.0)
0.003 (3.3)
0.009 (4.3)
Age ⱖ 9.0 yr and Tanner
staging performeda
189
0.01 (3.3)
0.11 (1.4)
0.03 (2.6)
0.22 (2.4)
0.52 (0.2)
P values for parameter (relationship to calcium absorptive efficiency) as determined by ANCOVA are shown with ␩2 values (as percentage)
given in parentheses.
a
Tanner stage (breast stage, assessed by physical exam) data were available for 214 of 315 subjects.
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J Clin Endocrinol Metab, September 2005, 90(9):5077–5081
FIG. 2. Relationship between height Z-score and calcium absorption.
n ⫽ 315; y ⫽ 2.12x ⫹ 35.1; r ⫽ 0.18; P ⫽ 0.0013.
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
Abrams et al. • Height Effect on Calcium Absorption
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 –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.
Received March 10, 2005. Accepted May 5, 2005.
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: [email protected].
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 Gen-
Abrams et al. • Height Effect on Calcium Absorption
eral 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.
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JCEM is published monthly by The Endocrine Society (http://www.endo-society.org), the foremost professional society serving the
endocrine community.