Full text of DOI:10.1359/jbmr.2000.15.11.2245

JOURNAL OF BONE AND MINERAL RESEARCH
Volume 15, Number 11, 2000
© 2000 American Society for Bone and Mineral Research
Calcium Accretion in Girls and Boys During Puberty:
A Longitudinal Analysis
DONALD A. BAILEY,1,2 ALAN D. MARTIN,3 HEATHER A. MCKAY,3 SUSAN WHITING,1
and ROBERT MIRWALD1
ABSTRACT
The primary purpose of this study was to estimate the magnitude and variability of peak calcium accretion
rates in the skeletons of healthy white adolescents. Total-body bone mineral content (BMC) was measured
annually on six occasions by dual-energy X-ray absorptiometry (DXA; Hologic 2000, array mode), a BMC
velocity curve was generated for each child by a cubic spline fit, and peak accretion rates were determined.
Anthropometric measures were collected every 6 months and a 24-h dietary recall was recorded two to three
times per year. Of the 113 boys and 115 girls initially enrolled in the study, 60 boys and 53 girls who had peak
height velocity (PHV) and peak BMC velocity values were used in this longitudinal analysis. When the
individual BMC velocity curves were aligned on the age of peak bone mineral velocity, the resulting mean peak
bone mineral accrual rate was 407 g/year for boys (SD, 92 g/year; range, 226–651 g/year) and 322 g/year for
girls (SD, 66 g/year; range, 194–520 g/year). Using 32.2% as the fraction of calcium in bone mineral, as
determined by neutron activation analysis (Ellis et al., J Bone Miner Res 1996;11:843–848), these corre-
sponded to peak calcium accretion rates of 359 mg/day for boys (81 mg/day; 199–574 mg/day) and 284 mg/day
for girls (58 mg/day; 171–459 mg/day). These longitudinal results are 27–34% higher than our previous
cross-sectional analysis in which we reported mean values of 282 mg/day for boys and 212 mg/day for girls
(Martin et al., Am J Clin Nutr 1997;66:611–615). Mean age of peak calcium accretion was 14.0 years for the
boys (1.0 years; 12.0–15.9 years), and 12.5 years for the girls (0.9 years; 10.5–14.6 years). Dietary calcium
intake, determined as the mean of all assessments up to the age of peak accretion was 1140 mg/day (SD, 392
mg/day) for boys and 1113 mg/day (SD, 378 mg/day) for girls. We estimate that 26% of adult calcium is laid
down during the 2 adolescent years of peak skeletal growth. This period of rapid growth requires high
accretion rates of calcium, achieved in part by increased retention efficiency of dietary calcium. (J Bone Miner
Res 2000;15:2245–2250)
Key words: calcium, bone mineral content, longitudinal, children, dual-energy X-ray absorptiometry
bone loss, and, consequently, most fracture prevention strat-
egies attempt to reduce or reverse the loss, primarily
through drugs, exercise, and dietary supplementation. An
alternative approach, the enhancement of PBM, has been
INTRODUCTION
DULT BONE mass, the strongest predictor of osteoporotic
fracture risk(1) can be viewed as the peak bone mass
A
(PBM) of early adulthood, less the subsequent bone loss. hampered by a lack of data; there is still controversy as to
Most research has investigated the factors associated with the age of attainment of PBM, and there has been no
1Colleges of Kinesiology and Pharmacy and Nutrition, University of Saskatchewan, Saskatoon, Canada.
2School of Human Movement Studies, University of Queensland, Brisbane, Australia.
3School of Human Kinetics, University of British Columbia, Vancouver, Canada.
2245

2246
BAILEY ET AL.
adequate longitudinal investigation of bone mass accumu-
lation before PBM.
Because virtually all of the body’s calcium resides in the
skeleton, dietary calcium has the potential to be a limiting
factor in skeletal growth. Despite this, international consen-
sus has not been reached on calcium requirements of chil-
dren. Balance studies, although difficult and expensive, can
reveal calcium retention and accretion rates over the short
term, but few studies have been done in children. An alter-
native approach is the use of dual-energy X-ray absorpti-
ometry (DXA), which allows the precise and accurate de-
termination of whole-body bone mineral content (BMC),
with a minimal (about 1 mrem) radiation exposure. A series
of such scans in one individual over the adolescent growth
spurt reveals the change in BMC accrual rates. These can be
converted into calcium accretion rates, since the calcium
fraction of bone mineral has been determined.(2) Knowing
skeletal calcium retention rates through adolescence thus
can yield insight into calcium requirements during growth.
We recently reported a cross-sectional analysis of bone
mineral accrual rates from 978 whole-body BMC scans by
DXA in 113 boys and 115 girls.(3) This analysis revealed
peak calcium accretion rates of 212 mg/day in girls and 282
mg/day in boys, at ages 11.4 years and 13.3 years, respec-
tively. However, cross-sectional analysis is known to un-
derestimate true mean peak velocity values for growth vari-
ables.(4) We report here a longitudinal analysis of a
multiyear study in which annual whole-body DXA scans
were analyzed to yield peak calcium accretion rates in 60
boys and 53 girls.
Longitudinal versus cross-sectional analysis of growth
The peak value of any growth rate variable and the age at
which it occurs can be estimated in two ways. When data
following an adequate number of children longitudinally
through the peak period are lacking, it is commonplace to
pool data by chronological age. This cross-sectional ap-
proach results in a growth curve, each of whose points is
calculated as the mean value for all subjects of that age. This
can be seen in Fig. 1A, which shows a schematic view of
whole-body BMC velocity values (g/year) for 5 boys. The
dashed line shows the curve resulting from averaging the
individual BMC velocity values at each age from 12 to 16
years. The peak value of the composite curve is similar to
that of the smallest individual peak. The true mean peak
value can only be determined after aligning the five subjects
on peak BMC velocity (Fig. 1B). When this is done, it can
be seen that the true peak is considerably greater than the
cross-sectionally estimated peak, the true age at peak is
earlier, and the phase of rapid growth is much shorter. These
differences can be considerable. Thus our cross-sectionally
estimated peak calcium accretion rates for boys (282 mg/
day) and girls (212 mg/day) were reported with the caveat
that they were almost certainly lower than the true values.(3)
Since that study, enough of the children have passed
through their age of peak calcium accretion that a longitu-
dinal analysis is now feasible.
FIG. 1. Schematic representation of (A) cross-sectional
and (B) longitudinal analysis of BMC velocity curves for 5
boys.
MATERIALS AND METHODS
Subjects
All subjects were participants in the University of
Saskatchewan Pediatric Bone Mineral Study. Of 375 eligi-
ble students attending two elementary schools in Saskatoon,
Canada, 113 boys and 115 girls, ranging in age from 8 to 14
years, were initially enrolled in this multiyear longitudinal
study. Only those subjects who clearly showed a peak in
their height and BMC velocity curves were selected for the
longitudinal analysis, resulting in a final sample size of 60
boys and 53 girls. Subjects who were excluded were pri-
marily individuals who were beyond their age of peak
height velocity (PHV) when first measured. The previous
cross-sectional analysis, used here for comparative pur-
poses, was carried out on data from 471 scans from 113
boys and 507 scans from 115 girls. All study procedures
were approved by appropriate university and hospital ethics

CALCIUM ACCRETION DURING PUBERTY
2247
committees and have been described elsewhere.(5) All test-
ing was done at the Royal University Hospital (Department
of Nuclear Medicine) in Saskatoon.
Bone measurements
Annual DXA scans of the whole body, AP lumbar spine,
and proximal femur were carried out by one of two expe-
rienced operators using DXA (Hologic QDR 2000; Hologic,
Waltham, MA, U.S.A.) in the array mode using enhanced
global software version 7.10. To minimize operator-related
variability, the same qualified person analyzed all whole-
body scans, using enhanced software version 5.67A. In our
laboratory, in vivo short-term reproducibility for this pro-
cedure is 0.51%. A Victoreen ion chamber survey meter
(model 450p; Victoreen, Inc., Cleveland, OH, U.S.A.) mea-
sured entrance radiation dose. When this surface dose was
corrected for body attenuation, subject age, and type and
volume of tissue being irradiated, the effective dose equiv-
alent was less than 1 mrem.
FIG. 2. Frequency distribution of peak calcium accretion
rates in 60 boys and 53 girls.
TABLE 1. PEAK VALUES AND AGES AT WHICH
THEY OCCURRED
Variable
Boys
Girls
Age at PHV (years)
Age at peak BMC velocity (years) 14.0 (1.0)
Peak BMC velocity (g/year)
Peak Ca accretion rate (mg/day)
Mean Ca intake (mg/day)
13.4 (1.0)
11.8 (0.9)
12.5 (0.9)
322 (66)
284 (59)
Anthropometric and dietary assessments
407 (93)
359 (82)
1140 (392) 1113 (378)
36.5 (12.3) 29.6 (8.5)
Height and weight and a set of 35 other anthropometric
measures were taken on all subjects every 6 months. Dietary
assessments using a 24-h recall were carried out three times
a year for the first 3 years of the study and twice a year
thereafter. Initially, children were trained to identify food
portion sizes and on subsequent assessment occasions were
shown life-size representations of food portions to enhance
the accuracy of their recall. Intakes from the 24-h recall
were analyzed using the Nutritional Assessment System
(NUTS) program, version 3.7 (Quilchena Consulting, Vic-
toria, B.C., Canada). Recalls were coded, with the same
individual checking all forms, and analyzed according to
procedures described elsewhere.(6) On the basis of these
recalls, average daily macro- and micronutrient intakes in-
cluding calcium were determined for each subject.
Apparent retention efficiency (%)
SD in parentheses.
RESULTS
The data reported here are based on a set of six whole-
body DXA scans for each of 60 boys and 53 girls who were
measured annually. The peak bone mineral accrual rate and
the age at which it occurred were determined from a cubic
spline curve fitted around the peak for each child. Boys had
a 26% higher mean peak bone mineral accrual rate (407
g/year; SD ϭ 93 g/year) than the girls (322 g/year; SD ϭ 66
g/year). Assuming that calcium constitutes 32.2% of bone
mineral, the bone mineral values in grams per year convert
to peak calcium accretion rates of 359 mg/day (SD ϭ 82)
Data analysis
Because subjects were not remeasured on exactly the for the boys and 284 mg/day (SD ϭ 59) for the girls. There
same dates each year, whole-year velocity values were was considerable individual variability in peak calcium
calculated for each subject by dividing the time between the accretion rates (Fig. 2). Values for boys ranged from 199 to
quasi-annual BMC measurements by the age increment 574 mg/day and for girls from 171 to 458 mg/day. The
(mean value, 0.998 Ϯ 0.048 years). A cubic spline fit was boys’ peak occurred at 14.0 (SD ϭ 1.0) years and the girls’
then applied to the whole-year height and BMC velocity peak at 12.5 years (SD ϭ 0.9). The ages at PHV were 13.4
values for each child. This allowed the determination of the years (SD ϭ 1.0) in boys and 11.8 years (SD ϭ 0.9) in girls
peak bone mineral velocity value and the age at which it (Table 1).
occurred. Mean values and SDs were then calculated for
Because dietary recall data show considerable variability,
peak bone mineral accrual rate in boys and in girls. Corre- mean calcium intake was calculated as the mean of all
sponding rates of calcium accretion were calculated as assessments up to the age of peak accretion rate. The
32.2% of the BMC velocity values and expressed in milli- number of assessments that were averaged per child until
grams per day. Mean dietary calcium intake was determined the age of peak ranged from 6 to 13. The mean calcium
as the mean of all reported intakes. Apparent calcium re- intake determined in this way was 1140 mg/day (SD ϭ 392)
tention efficiency at peak accretion rate was defined as 100 for the boys and 1113 mg/day (SD ϭ 378) for the girls. The
times the peak calcium accretion rate divided by the mean averaging of all intake values up until the age of peak
daily dietary calcium intake for each child.
accretion is a reasonable and appropriate strategy to attempt

2248
BAILEY ET AL.
to determine usual dietary intake of the children, as in our
Individual variability in the magnitude of these peak rates
study the relationship between mean intake in the first year can be examined for the first time (Fig. 2). The upper values
of measurement and 4 years later was small (r ϭ 0.23 for are surprisingly large, with the highest individual value of
boys and r ϭ 0.36 for girls). The correlation coefficients for 574 mg/day. In boys, 48% had peak values greater than 350
peak calcium accretion rate and calcium intake were 0.05 mg/day and 31% of the values were greater than 400 mg/
for the boys and 0.07 for the girls, explaining less than 1% day. The girls’ values were lower than the boys but none-
of the variance. Apparent mean retention efficiencies (at theless represent a high skeletal accretion rate: 74% of the
peak accretion rate) were 36.5% (SD ϭ 12.3) for boys and girls were above 250 mg/day and 30% were over 300
29.6% (SD ϭ 8.5) for girls.
mg/day. The variability may reflect size differences because
smaller children might be expected to have lower peak
growth rates. Therefore the approximate 10-cm greater
height for boys at PHV (p Ͻ 0.001) might partially explain
the sex difference in peak calcium accretion rates. This
possibility was supported by the positive association be-
DISCUSSION
Virtually all dietary calcium is either excreted (fecal, tween peak calcium accretion and attained height at the age
renal, and dermal) or retained as bone mineral. Balance of PHV (r ϭ 0.40; p Ͻ 0.01).
studies estimate calcium in the body by difference: net
It is not known whether peak accretion rates are related to
absorption ϭ ingested Ϫ fecal; retained ϭ absorbed Ϫ total accretion, that is, adult BMC values, because full
(renal ϩ dermal ϩ endogenous secretion). Balance studies skeletal maturity could not be confirmed for most of our
have shown that adolescents continue to increase calcium subjects. However, we have confirmed that the bone mineral
retention at dietary intakes above 1500 mg/day.(7) On the growth spurt continues after height velocity has peaked. The
basis of this study and more recent data, dietary calcium ages of peak calcium accretion rates were 14.0 years (1.0
recommendations for adolescents have increased to 1300 years) in boys and 12.5 years (0.9 years) in girls, which
mg/day.(8) However, balance studies are expensive and dif- lagged behind PHV by 0.6 years (boys) and 0.7 years (girls).
ficult and give only a brief window through which to view This time lag could have important implications. If linear
calcium retention in the body. An alternative approach is to growth in stature may be taken to represent the growth of
measure bone mineral radiologically and determine accre- skeletal volume (i.e., bone breadths follow the same growth
tion rate as the difference between serial measures divided pattern as stature), the lag suggests that bone mineralization
by the time between them. Early measurement of calcium does not keep up with the rapidly expanding skeletal vol-
accretion rate during growth used extrapolation from re- ume. It has been hypothesized that in some children, if the
gional measures of bone mineral and yielded estimates of high demand for bone mineral cannot be met from dietary
300 mg/day for boys and 280 mg/day for girls, based on sources, the mineral could be “borrowed” from cortical
metacarpal,(9) and 200 mg/day for boys and 160 mg/day for bone and be “repaid” later when demand has declined.(13)
girls, based on radial BMC.(10)
The reported coincidence of the timing of PHV and the peak
The use of whole-body DXA avoids the errors arising rate of forearm fractures in boys and girls from the same
from extrapolation of bone changes at a single site to the geographical area as the present sample strongly supports
whole body. Several studies have estimated calcium accre- this hypothesis.(14) This raises the important question of
tion rates in this way. Mean accretion rate over 10 years of whether dietary calcium might be, in some children, a
growth from a cross-sectional study was found to be 160 limiting factor in bone mineralization. Three calcium sup-
mg/day with a suggested peak in the range of 300–400 plementation studies have investigated this. Lloyd et al.(15)
mg/day.(11) In a 6-month longitudinal investigation of ado- showed a 1.3% additional gain in skeletal bone mineral
lescent girls,(12) a calcium increment averaging 221 mg/day attributed to calcium supplementation of 354 mg/day in
was found (based on a 32.2% calcium fraction of bone premenarcheal girls. Similarly, Johnston et al.(16) reported a
mineral, not the 39% reported by these authors(12)), with significant, positive effect of calcium supplementation in a
slightly higher values for those supplemented with dietary double-blind monozygotic twin study in prepubertal chil-
calcium. In a preliminary analysis of earlier data from this dren, but not in those who were beyond this maturational
study,(3) we reported peak BMC velocity values and the stage. However, a more recent study showed a positive
corresponding calcium accretion rates after a cross-sectional effect of calcium in pubertal children. Nowson et al. sup-
analysis, because at that time there were too few children plemented 1 child of each of 42 pairs of twins with 1000 mg
with complete growth peaks for a longitudinal analysis. of calcium a day.(17) After 6 months, hip and spine bone
Peak calcium accretion rates were 282 mg/day for the boys mineral density (BMD) had increased significantly in the
and 212 mg/day for the girls. The longitudinal analysis supplemented twin (1.3% and 1.5%, respectively), but no
reported here revealed peak accretion rates that were, on further effect was seen in the subsequent year of supple-
average, 30% higher than we reported in our previous mentation. In a study of Hong Kong Chinese children on a
cross-sectional analysis (359 mg/day for boys and 284 mg/ habitually low-calcium diet (mean, 280 mg/day), those sup-
day for girls). It could be that the true peak accretion rates plemented with 300 mg/day of calcium showed significantly
are even higher than these values because our bone mineral greater increases in radial BMD than unsupplemented con-
velocities are based on annual measurement occasions as trols.(18) However, a follow-up study of these children 18
opposed to our height measurements, which were taken months later showed that the benefits had disappeared after
every 6 months.
supplementation was stopped.(19) On the other hand, in a

CALCIUM ACCRETION DURING PUBERTY
2249
variance in boys (r ϭ 0.05) and girls (r ϭ 0.07). Consid-
ering the vagaries involved in determining calcium intake
by dietary recall in children, this may be an underestimate of
the effect of calcium intake on peak accretion rates. Calcium
absorption efficiencies have been reported at 20.3% in ad-
olescent girls at calcium intake levels of about 1300
mg/day (23); retention efficiency must be lower than absorp-
tion efficiency because of urinary calcium excretion. How-
ever, our mean apparent calcium retention efficiencies were
36.5% for the boys and 29.6% for the girls. Efficiencies
would increase reasonably with skeletal demand; hence, our
values, which are at peak accretion rates, are greater than
those reported previously.(23) Alternatively, higher efficien-
cies could compensate for low dietary intake; in girls given
FIG. 3. The relationship between peak calcium accretion a low calcium diet after a high calcium diet, absorption
efficiencies more than doubled from 26.0% to 58.2%.(24)
rate and dietary calcium intake in boys and girls.
The graphical estimation of the relationship between cal-
cium absorption efficiency and calcium intake in girls re-
ported by these authors(24) showed that when intake drops
study by Bonjour et al.(20) there was a statistically signifi-
from 600 to 400 mg/day, absorption efficiency rises from
cant difference in the mean BMD between supplemented
40% to 50%. Recent evidence supports earlier suggestions
subjects and controls, which remained 1 year after the end
that skeletally driven increases in absorption efficiency are
of calcium supplementation. Thus, although it appears that
calcium supplementation can enhance BMD in children and
mediated by increased circulating calcitriol.(25)
There are limitations to the interpretation of these data. It
is possible that dietary intakes have been underreported
(leading to overestimates of retention efficiency), as is
known to occur especially in girls. However, this may be
less of an error with calcium, because snack foods, the items
most often omitted in recalls, are not typically rich in
calcium. The calcium fraction of bone mineral is not known
in children and we and others have used adult values. The
Hologic 2000 DXA used in this investigation has been
shown to yield bone mineral fractions consistent with neu-
tron activation analysis.(26) Although hydroxyapatite is
39.9% calcium by weight, the calcium content of bone
mineral has been estimated variously at 38%(11) and
34%.(24) We have used a lower value (32.2%) based on a
direct comparison of the Hologic 2000 DXA and neutron
activation analysis.(2) Our use of a lower value than others
would have the effect of lowering all our calculated effi-
ciencies.
We conclude that peak calcium accretion rates were
high with mean values of 359 mg/day (82) for boys and
284 mg/day (59) for girls, and an upper limit of 575
mg/day for 1 boy and 459 mg/day for 1 girl. We confirm
the underestimate arising from cross-sectional analysis of
growth velocities; our previously reported peak accretion
rates were 27–34% lower than those reported here. The
high accretion rates were associated with high apparent
calcium retention efficiencies: 36.5% for the boys and
29.6% for the girls. In addition, adolescence is clearly a
critical time for bone mineralization because 26% of
adult calcium was accumulated in the 2 years around the
age of peak calcium accretion. Although there appears to
be a compensatory mechanism that promotes an increase
in calcium retention at low dietary intakes, diets that
provide adequate calcium nutrition during the adolescent
adolescents, more studies are needed to determine whether
such increases are sustained and result in a higher adult
PBM.
The high bone mineral accretion rates in puberty mean
that a considerable fraction of adult BMC is gained in a few
years of adolescence. In the 2-year period spanning the age
of peak accretion rate, boys’ BMC increased by 720 g (150
g), while girls gained 569 g (105 g). Converting these values
to calcium equivalents gives a value of 231 g of calcium for
boys and 183 g for girls laid down over the 2-year period.
The young adult BMC values for these children are not yet
known, but corresponding data, measured on the same bone
densitometer, are available for several other samples of
adults. The mothers and fathers of some of our subjects have
been measured as part of a study of familial relation-
ships.(21) The 76 mothers (mean age, 40 years) had a BMC
of 2164 g and the 37 fathers (mean age, 45 years) had a
BMC of 2884 g. A separate unpublished study of 59 men
(mean age, 40 years) and 32 women (mean age, 36 years)
revealed BMC values of 2880 g and 2181 g, respectively.
Finally, a study of 57 younger women(22) (mean age, 21
years) revealed a BMC of 2180 g. Averaging these adult
values and converting to calcium equivalents gives a mean
young adult skeletal calcium of 928 g for men and 700 g for
women. If we take these to be estimates of the young adult
calcium values of the boys and girls in this study, approx-
imately 26% of adult calcium is gained in the 2 years of
peak skeletal growth.
The high calcium retention rates around puberty can be
caused by both increased dietary intakes and greater effi-
ciencies of absorption and retention. Our subjects consumed
moderate amounts of calcium; intakes were slightly lower in
the girls (1113 mg/day) than in the boys (1140 mg/day), but
variability was large (Table 1). Dietary calcium intake at
these levels showed virtually no association with peak cal-
cium accretion rates (Fig. 3), explaining less than 1% of the years should be encouraged.

2250
BAILEY ET AL.
16. Johnston CC Jr, Miller JZ, Slemenda CW, Reister TK, Hui S,
Christian JC, Peacock M 1992 Calcium supplementation and
increases in bone mineral density in children. N Engl J Med
327:82–87.
17. Nowson CA, Green RM, Hopper JL, Sherwin AJ, Young D,
Kaymakci B, Guest CS, Smid M, Larkins RG, Wark JD 1997
A co-twin study of the effect of calcium supplementation on
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18. Lee WT, Leung SS, Wang SH, Xu YC, Zeng WP, Lau J,
Oppenheimer SJ, Cheng JC 1994 Double-blind, controlled
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744–750.
ACKNOWLEDGEMENTS
This work was supported in part by a grant from the
National Health Research and Development Program,
Health Canada (D.A.B.)
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Address reprint requests to:
Dr. D.A. Bailey
College of Kinesiology
University of Saskatchewan
105 Gymnasium Place
Saskatoon, SK S7N 5C2, Canada
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Received in original form December 3, 1999; in revised form April
3, 2000; accepted May 25, 2000.