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Factors that Affect Bone Mineral Accrual in the Adolescent Growth Spurt

Article  in  Journal of Nutrition · April 2004

DOI: 10.1093/jn/134.3.696S · Source: PubMed

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 Nutritional Influences on Bone Growth in Children

Factors that Affect Bone Mineral Accrual in the Adolescent Growth Spurt1,2
Susan J. Whiting,*3 Hassanali Vatanparast,* Adam Baxter-Jones,† Robert A. Faulkner,†
Robert Mirwald,† and Donald A. Bailey†**
*College of Pharmacy and Nutrition, University of Saskatchewan, Saskatoon, Saskatchewan Canada, S7N
5C9; †College of Kinesiology, University of Saskatchewan, Saskatoon, Saskatchewan Canada, S7N 1M3; and
**Department of Human Movement Studies, University of Queensland, Brisbane, Australia

ABSTRACT The development of bone mass during the growing years is an important determinant for risk of
osteoporosis in later life. Adequate dietary intake during the growth period may be critical in reaching bone growth
potential. The Saskatchewan Bone Mineral Accrual Study (BMAS) is a longitudinal study of bone growth in
Caucasian children. We have calculated the times of maximal peak bone mineral content (BMC) velocity to be 14.0
⫾ 1.0 y in boys and 12.5 ⫾ 0.9 y in girls; bone growth is maximal ⬃6 mo after peak height velocity. In the 2 y of
peak skeletal growth, adolescents accumulate over 25% of adult bone. BMAS data may provide biological data on
calcium requirements through application of calcium accrual values to factorial calculations of requirement. As
well, our data are beginning to reveal how dietary patterns may influence attainment of bone mass during the
adolescent growth spurt. Replacing milk intake by soft drinks appears to be detrimental to bone gain by girls, but
not boys. Fruit and vegetable intake, providing alkalinity to bones and/or acting as a marker of a healthy diet,
appears to influence BMC in adolescent girls, but not boys. The reason why these dietary factors appear to be
more influential in girls than in boys may be that BMAS girls are consuming less than their requirement for calcium,
while boys are above their threshold. Specific dietary and nutrient recommendations for adolescents are needed
in order to ensure optimal bone growth and consolidation during this important life stage. J. Nutr. 134:
696S–700S, 2004.

KEY WORDS: ● calcium intake ● children ● adolescents ● calcium requirement ● soft drinks
● fruit and vegetables

Adolescence is a time of tremendous growth in height,
characterized by the adolescence growth spurt, during which
children gain physical, mental, and emotional maturity in a
very short period of time. Our research interests have centered
on how bone mineral is accrued during this time, as the
development of peak bone mass during the growth years is
considered an important determinant for future risk of osteo-
porosis in later life (1–3). Adequate nutrition to provide the
building blocks for bone, and sufficient activity to provide the
mechanical impetus for bone development, are critical factors
in maximizing bone growth potential (3). Surprisingly, little is
known about bone mineral accrual during adolescence as,
until recently, few longitudinal studies have been undertaken
to measure bone development through adolescence. There-
1
Presented at the Nutrition and Bone Health Working Group program at the
“American Society of Bone Mineral Research, 25th Annual Meeting,” held in
Minneapolis, MN, September 19 –23, 2003. The Nutrition and Bone Health Work-
ing Group program was organized by Susan J. Whiting and was sponsored by
The National Dairy Council. Supplement contents are solely the responsibility of
the authors and do not necessarily represent the official views of the National
Dairy Council. Guest editors for the supplement publication were Susan J. Whit-
ing, College of Pharmacy and Nutrition, University of Saskatchewan, Saskatoon,
Saskatchewan, and Frances A. Tylavsky, University of Tennessee, The Health
Science Center, Memphis, TN.
2
Supported by the Canadian Institutes of Health Research.
3 4
To whom correspondence should be addressed.
E-mail: susan.whiting@usask.ca.
fore, we present some of our findings to date and provide data
to suggest that a healthy diet and lifestyle can lead to consid-
erable mineral accrual through the adolescence. This gain in
bone through adolescence can be used as a functional indica-
tor for calcium requirements of adolescents.
The Saskatchewan Bone Mineral Accrual Study (BMAS)4
The Saskatchewan Pediatric Bone Mineral Accrual Study
began in 1991, with over 220 male and female children ages 8
to 14 y, from 2 elementary schools in Saskatoon, giving in-
formed consent for the study (4 –7). Bone mineral was mea-
sured yearly until 1997. A subgroup of subjects has complete
data spanning their age of peak height velocity. Nearly all
subjects were Caucasian, living in a middle-class area of Saska-
toon. All subjects and parent/guardians provided informed
written consent, and the University of Saskatchewan Advisory
Committee on Ethics in Human Experimentation approved
the protocol. Bone measurements were obtained by annual
dual-energy X-ray absorptiometry scans of the whole body,
anterior posterior lumbar spine and proximal femur (QDR
2000, Hologic) as described elsewhere (5). Dietary intake over
Abbreviations used: AI, adequate intake; BMAS, Saskatchewan Bone Min-
eral Accrual Study; BMC, bone mineral content; DRI, dietary reference intake.

0022-3166/04 $8.00 © 2004 American Society for Nutritional Sciences.

696S
 BONE MINERAL ACCRUAL IN ADOLESCENCE 697S

TABLE 1
Characteristics of Saskatchewan Bone Mineral Accrual Study subjects (mean ⫾ SD)

Measurement Boys, n ⫽ 66 Girls, n ⫽ 65

Age at peak height velocity (PHV), y 13.5 ⫾ 1.0 11.8 ⫾ 0.9

Height attained at age of PHV, cm 164.7 ⫾ 7.3 152.7 ⫾ 7.3
Weight attained at age of PHV, kg 51.4 ⫾ 11.1 47.7 ⫾ 12.5
Bone mineral content accrual from age 9 to 18 y, g/day 1601 1151
Daily calcium intake age 9–13 y, mg 11792 10422
Daily calcium intake age 13.1–18 y, mg 13862 9512
Daily calcium intake at age of PHV, mg 1243 ⫾ 4933 1075 ⫾ 3773
Daily fruit and vegetable intake at age of PHV, servings 3.7 ⫾ 2.8 3.9 ⫾ 2.1
Daily milk products at age of PHV, servings 3.0 ⫾ 1.7 2.7 ⫾ 1.2

1 Determined from average of yearly increments in bone mineral content (grams bone mineral/y) converted to calcium (using 32.2% as the fraction
of calcium in bone mineral) and expressed as a daily value.
2 Reference (6).
3 Reference (14) (n ⫽ 59 boys; n ⫽ 53 girls).

the 6-y collection period was assessed via serial 24-h recalls
conducted both at the participation schools and in the hospi-
tal setting at the time of the bone scans. There were 2 to 4
recalls for each subject every year. All days of the week, except
Friday and Saturday, were included. Similarly, activity assess-
ment was conducted with each diet recall and consisted of a
frequency questionnaire developed for our study (8,9). Table 1
shows characteristics of the subgroup of subjects having bone
mineral accrual data before and after age of peak height
velocity.
322 ⫾ 66 g. As more subjects are added to our analysis, we
have slightly revised our calculations of age of peak bone
mineral content of our BMAS cohort (Table 1).
Annual growth measures plotted over time, i.e., distance
curves, are useful to illustrate the rapid accumulation of bone
mineral content (measured as total body) during adolescence.
In Figure 1, bone gain is shown as a function of chronological
age. In contrast, Figure 2 shows bone gain as a function of
biological age, where age of zero is the age of peak height

BMAS subjects provide reference group data

for bone accrual
Our dataset is one of only a few having longitudinal mea-
sures of bone mineral accrual through adolescence. Although
our data do not cover the full 10 y (i.e., age 9 to 18 y) of
longitudinal data defined as adolescence by dietary reference
intake (DRI) age stage definitions (10) for every subject, these
data provide measurement of bone accrual during peak accre-
tion, and the age span of our cohort covers the entire adoles-
cent age range. Bone mineral content accrual is primarily
determined by height and body weight; thus, it is important to
compare BMAS subjects’ height and weight to reference stan-
dards for children. As shown in Table 1, mean height achieved
at age of peak height velocity was greater for BMAS subjects
than the corresponding median reference height for boys and
girls at the next incremental age, i.e., girls at age 12 y (151 cm)
and boys at age 14 y (164 cm) (10). Similarly, mean weight
achieved at age of peak height velocity was greater for BMAS
subjects than the corresponding median reference weight for
boys and girls at the next incremental age, i.e., girls at age 12 y
(41.6 kg) and boys at age 14 y (51.0 kg) (10). In terms of
dietary intake, BMAS subjects have greater intake of calcium
(6) than adolescents living in the United States of correspond-
ing age ranges as reported using NHANES III data (3).

Bone mineral accrual in adolescent boys and girls (BMAS)

We previously published results on bone mineral accrual
data through the adolescent growth spurt, initially from cross-
sectional analysis (4) and later when longitudinal analysis was
completed on ⬃50 boys and girls (7). With the latter analysis,
the age of maximal peak bone mineral content (BMC) veloc- FIGURE 1 Total body bone mineral content (g) of the BMAS
ity occurred at age 14.0 ⫾ 1.0 y in boys and 12.5 ⫾ 0.9 y in subjects at yearly age increments. Values are mean ⫾ SEM. Subject
girls; boys gained, on average, 407 ⫾ 92 g of bone mineral numbers vary at each age point but were derived from 66 boys and 65
during each of the 2 y surrounding this age, while girls gained girls.
698S SUPPLEMENT
FIGURE 2 Total body bone mineral content (g) of the BMAS
subjects at yearly age increments younger than (negative) or older than
(positive) zero biological age (age of peak height velocity). Values are
mean ⫾ SEM Subject numbers vary at each age point but were derived
from 66 boys and 65 girls.
velocity. Age of peak height velocity is the most commonly
used indicator of somatic maturity in longitudinal studies. In
our cohort, girls gain less bone mineral at every age, and after
age of peak height velocity there is a more rapid gain in bone
by boys than by girls. By age 18 y (Fig. 1) males have 22%
more BMC than do females. As discussed below, this gender
difference may be biological or may be a result of the higher
intake of calcium (6) and/or greater activity levels of BMAS
boys compared to BMAS girls (9), or both. In comparing our
BMC accrual data to data from other published studies, our
data are similar to those of Danish children (11).
Finding estimates of calcium requirement using
BMC accretion
One of the uses of BMC accrual during growth is determin-
ing calcium requirements of adolescents. Currently, there is
only an adequate intake (AI) level for calcium for adolescents
of 1300 mg/d (12). There is controversy around what the
calcium requirement is, in part because other dietary and
lifestyle factors may affect need for calcium. Nevertheless, not
having a requirement value (i.e., an Estimated Average Re-
quirement, EAR) for calcium limits the ability of nutritionists
to provide dietary advice and to assess nutrient intake (13).
In setting an AI for calcium for adolescent boys and girls,
the Panel for the Dietary Reference Intakes for Calcium
looked at 3 lines of evidence: a factorial approach, calcium
retention using a nonlinear regression model, and results of
clinical trials (11). The factorial calculation of calcium re-
quirements for adolescents was for the 2 y of maximal peak
bone mineral content accrual and involved summing estimates
of calcium need and losses, specifically calcium retained in
bone together with estimates of skin, urine, and fecal calcium
losses. The values originally used for calcium retention, 212
mg for girls and 282 mg for boys, were those found by us from
the cross-sectional analysis of bone mineral accrual within 2 y
of peak bone mineral content accrual (4). Since that time, as
indicated, we provided a more exact picture of BMC accrual
using longitudinal rather than cross-sectional data (7). As
shown in Table 2, estimates of calcium need during the 2 y of
peak bone accretion increase to ⬃1500 mg for girls, and 1700
mg for boys, assuming all other estimates of losses and absorp-
tion efficiency remain constant. This demonstrates that the
need for calcium is greater during this 2-y window of bone
accrual than previously estimated (11). However, it is impor-
tant to note that subjects were consuming less dietary calcium
during this time than the factorial calculation indicates was
needed.
Applying 2-y peak retention values for calcium provides the
best estimate of calcium requirements during the years of
greatest need for an adolescent. However, it overestimates
requirement throughout the whole adolescent period of 9 to
18 y. As shown in Table 2, if we apply the average accumu-
lation of calcium during the whole span of the DRI age range
for adolescents (ages 9 through 18 y), the factorial calculation
results in a calcium requirement estimate of ⬃1000 mg and
1200 mg per day for girls and boys, respectively. It should be
noted that timing of peak accretion for an individual cannot
be determined a priori. Therefore, public health recommen-
dations need to cover the broad span of ages for peak accretion
to cover most individuals. Further, this last calculation of
mean calcium requirement assumes that every other compo-
nent (i.e., losses, absorption efficiency) is valid for the entire
adolescence age range. The values for losses and absorption
efficiency were estimated specifically for females and measured
around the time of peak bone accrual (11). In particular, the
absorption efficiency for calcium will vary with stage of devel-
opment. These calculations assume that vitamin D levels are
adequate. Additionally, they assume equivalent absorption
efficiencies of boys and girls. However, studies showing gender
differences are emerging, and there are indications of differ-
ences between boys’ and girls’ handling of calcium (14). The
following example, of soft drink intake and bone, illustrates
this difference.
Soft drink intake affects bone accrual of girls, not boys
Two studies indicate that soft drink intake negatively im-
pacts on bone mineral accrual of adolescent girls but not
adolescent boys (15,16). The first of these was conducted on
data from BMAS subjects (15). We examined the effect of soft
drink consumption by our subjects on BMC and BMC accrual
during the 2 y of maximal bone mineral gain. Subjects drank
a variety of soft drinks, which we labeled low nutrient dense
beverages; these included carbonated (cola and noncola) and
noncarbonated, sugar-based beverages. While both boys and
girls showed significant negative correlations between low
nutrient beverages and fluid milk consumption, only girls
showed negative correlation between bone mineral content
accrual and low nutrient dense beverage intake. Recently, a
study with ⬎10 times as many subjects reported similar find-
ings (16). Girls’ heel bone mineral density was significantly
lower with carbonated beverage intake, whereas boys showed
no significant effect. In this latter study, pubertal stage was not
 BONE MINERAL ACCRUAL IN ADOLESCENCE 699S

TABLE 2
Comparison of factorial calculations for determining calcium requirements during the 2 y of peak calcium accretion
and during 10 y of adolescence (age 9 to 18 y) in white adolescents

During peak calcium accretion: During peak calcium accretion: Through adolescence:
Factorial criteria1 original calculation2 longitudinal analysis3 age 9 to 18 y

mg/day

Girls
Calcium accretion 2123 2843 1154
Urinary losses 106 106 106
Endogenous fecal calcium 112 112 112
Sweat losses 55 55 55
Total 485 557 388
Absorption, % 38% 38% 38%
Adjusted for absorption 1276 1466 1021
mg/day

Boys
Calcium accretion 2823 3593 1604
Urinary losses 127 127 127
Endogenous fecal calcium 108 108 108
Sweat losses 55 55 55
Total 572 649 450
Absorption, % 38% 38% 38%
Adjusted for absorption 1505 1708 1184

1 Criteria listed in Table 4-3 of reference (11).

2 Values taken from Table 4-3 of reference (11); girls age 11.4 ⫾ 1.0 y; boys 13.3 ⫾ 1.0.
3 Reference (7); girls age 12.5 ⫾ 1.0 y; boys age 14 ⫾ 1.0.
4 Calculated from yearly BMC accrual of 66 male and 65 female subjects (Table 1).

adjusted for, but 2 ages of children were examined, age 12 y
and 15 y. Milk intake dropped as soft drink consumption rose
for boys and girls. A difference in calcium intake was evident,
with girls consuming, on average, less than 900 mg per day
whereas boys’ intakes were ⬎1000 mg. Replacement of a
calcium-rich beverage (milk) by soft drinks was observed in
both studies and is a plausible mechanism for at least some of
the effect of soft drinks on bone accrual in female adolescents.
These studies suggest that being below (i.e., girls) or above
(i.e., boys) the calcium intake threshold determines vulnera-
bility to dietary influences on bone accrual.
Boys’ dietary needs for calcium may be different from those
of girls
As indicated, much less is known about calcium losses and
absorption efficiencies of boys than girls. There are indications
that boys and girls may have different efficiencies in handling
of calcium, and that boys may be more efficient (14). Our
beverage data (15) support gender differences in the effect of
dietary change (e.g., replacement of milk by soft drinks) on
bone accrual. It is possible that the boys’ need for calcium was
being met by their calcium intake, and we find that mean
intake of calcium by boys is greater than that by girls of similar
age (Table 1). However, at age of peak height velocity, this
difference was quite modest, with boys’ and girls’ mean cal-
cium intakes differing by ⬍200 mg. This suggests that the
gender difference in response to soft drinks may be mediated
by differences in calcium efficiencies that, in turn, determine
the calcium intake threshold.
Fruit and vegetable intake may affect bone accrual
during adolescence
There is evidence of a positive link between fruit and
vegetable consumption and bone health (17–19). Two differ-
ent studies of prepubertal girls indicate a similar protective
effect on bone growth (20,21). As shown in Table 1, mean
intake of the Vegetables and Fruit group of Canada’s Food
Guide For Healthy Eating (22) falls below the recommended
level of 5 servings per day for both boys and girls in BMAS.
Our preliminary analysis of BMAS data suggested that girls
consuming adequate amounts through adolescence showed a
greater bone mineral trajectory than girls consuming fewer
than 5 servings, whereas no similar relationship was seen when
boys’ data were plotted. Understanding food intake patterns
may be important in making dietary recommendations for
optimal bone growth of adolescents.
The challenges ahead
There are a number of challenges in determining diet-bone
relationships during growth. We have reported on the general
trend of underreporting dietary energy (23) that may affect the
accuracy of our nutrient intake measurements. A further con-
cern is how to account for physical activity, as an interaction
between nutrition and activity may exist for children. Our
analysis to date does not support a specific interaction (24).
However, we must contend with the likelihood that positive
behaviors are linked and may track together through adoles-
cence, making it difficult to separate effects. The difference in
bone mineral accrual between boys and girls through stages
surrounding pubertal development is striking, and further re-
search is needed to understand this gender difference.
Collection of BMAS continues as we add to the adolescent
cohort data on subjects for whom puberty has only recently
occurred. Additionally, we are measuring the subjects as young
adults. With the latter measurements, we hope to be able to
answer 2 important questions: what is the age of final bone
mineral accrual, and is there persistence in bone mineral
accrual when subjects with adequate calcium intake through
700S SUPPLEMENT
childhood and adolescence no longer maintain that dietary
pattern? Based on this work and that of others, age- and
gender-specific dietary and nutrient recommendations for ad-
olescents are needed in order to ensure optimal bone growth
and consolidation during this important life stage.
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