J Bone Miner Metab (****) **:*** *** Springer ****

DOI 10.1007/s00774-007-0814-4

ORIGINAL ARTICLE

Dario Prais Gary Diamond Avi Kattan Jacob Salzberg

Dov Inbar

The effect of calcium intake and physical activity on bone quantitative

ultrasound measurements in children: a pilot study

Received: January 18, 2007 / Accepted: August 27, 2007

Abstract Environmental factors, such as nutritional status, tion, its origins lie in early childhood and adolescence. The

physical activity, and drug therapy, can affect bone mineral- quantity of bone at any time in life depends upon the total

ization. Our objective was to evaluate the relationship amount at peak bone mass and the rate of bone loss there-

between nutritional status, physical activity, and bone min- after. More than 90% of peak bone mass is present by 18

eralization as assessed by multisite quantitative ultrasound years of age, making childhood and adolescence a critical

technology in children. The study group comprised 67 chil- stage. Teegarden et al. [1] and Wosje and Specker [2] pro-

dren, aged 6 17 years (mean, 9.4), attending a primary care posed that individuals could reduce their future risk of

clinic. Data on calcium intake and physical activity were osteoporosis by building up the largest possible bone mass

collected using a detailed questionnaire. Speed of sound during their growth stages.

measurements were performed at the distal 1/3 radius and Although genetic factors play a major role in determin-

the midshaft tibia using Sunlight Omnisense apparatus. The ing peak bone mass, many environmental factors, such as

reported mean calcium intake was 1105 mg/day. There was nutritional status, physical activity, drug therapy, and pres-

a signi cant difference in Z-scores at the radius and tibia ence of chronic illnesses (e.g., malabsorption, endocrine

between the low- and high-calcium-intake groups (P = pathology), may have an impact. Findings regarding child-

0.004, P = 0.035, respectively). A similar difference was hood dietary calcium intake are inconsistent, some showing

found between the low- and normal-physical-activity groups positive effects of increased calcium intake on bone mass

(P = 0.015, P = 0.036, respectively). In this pilot study, a accretion [2 5] and others reporting no such association

positive association was found between calcium intake, [6,7]. Several prospective studies noted that exercise, par-

physical activity, and bone status, as assessed by the quanti- ticularly strength and aerobic, exerts a positive in uence on

tative ultrasound technique. bone mineral density in children [8,9].

The development of reliable methods to measure bone

Key words bone mineralization quantitative ultrasonogra- mineral content in the pediatric population has signi cantly

phy calcium increased our understanding of the in uence of dietary

calcium on bone accretion in children. In adults, dual X-ray

absorptiometry (DXA) is currently the most widely used

method of assessing bone mineral density and predicting

Introduction

fracture risk. However, exposure to radiation and depen-

dency of the measurements on bone size limits its use in

Osteoporosis is the most common skeletal disorder world- children. When comparing two bones of identical true

wide. Although frequently identi ed with the aging popula- density, but of varying sizes, the smaller bone will have a

lower reading [10]. Moreover, DXA measurements do not

D. Prais distinguish between trabecular and cortical bone, which

Department of Pediatrics C, Schneider Children s Medical Center of

may differ in turnover rates and response to hormones,

Israel, and Sackler Faculty of Medicine, Tel Aviv University, 14

Kaplan Street, Petah Tikva 49202, Israel drugs, and mechanical loading. It also does not show the

Tel. +972-*-*******; Fax +972-*-*******

bone microarchitecture or other aspects of bone quality.

e-mail: abpo2l@r.postjobfree.com

To overcome these problems, researchers have intro-

G. Diamond J. Salzberg D. Inbar

duced a new multisite quantitative ultrasound system

The Child Development and Rehabilitation Center, Schneider

(QUS), which measures the speed of sound (SOS) transmit-

Children s Medical Center of Israel, and Sackler Faculty of Medicine,

ted axially along the long bone shafts. The QUS offers the

Tel Aviv University, Petah Tikva, Israel

possibility of assessing bone parameters other than bone

A. Kattan

density, such as elasticity and microstructure, which have

Clinical Department, Sunlight Medical Ltd., Tel Aviv, Israel

249

been strongly suggested to contribute to bone strength [11]. 0.30

0.20

The QUS involves no ionizing radiation, making it appro- 0.20 0.13

priate for children. Studies have been shown that QUS bone

0.10

measurements correlate signi cantly with DXA ndings in

0.00

both adults and children [12 14]. In addition, QUS can dif-

ferentiate between women with hip fractures and healthy -0.10

P=0.004 P=0.035

controls and predict osteoporotic fractures in adults [15]. -0.20

The present study was designed to evaluate the relation-

-0.30

ship between nutritional calcium intake and physical activ-

-0.40

ity and bone mineralization, as assessed with multisite QUS -0.38

technology in children. -0.50 -0.50

-0.60

Z_ RAD Z_ TIB

Materials and methods

>1000mg/d

The study group was composed of normal children and

adolescents aged 6 17 years attending a pediatric primary Fig. 1. Z-score at radius and tibia in the low- and high-calcium intake

care community-based clinic. Children who were acutely ill, groups

on medication for more than 3 days, had taken chronic

ultrasonic waves ( speed of sound or SOS in m/s) propa-

drugs within the past 6 months, or had any disease known

gating along the distal one-third of the radius, the midshaft

to affect bone metabolism were excluded. Only one boy on

tibia, the proximal third phalanx, and/or the fth metatar-

antiepileptic treatment was dropped. A questionnaire was

sal, using the critical angle concept (Omnipath) [19,20].

lled out by the investigator for each subject. Items included

The probe is designed to measure skeletal sites at different

were demographic data, anthropometric parameters, and

soft tissue thicknesses up to 9 mm. The probe (length, 1.97

medical history.

inch; width, 0.8 inch) operates at a frequency of 1.25 MHz

A Harpenden stadiometer (UK) measured height; height

and contains two transmitters and two receivers housed

standard deviation score (SDS) was determined according

tightly together in a compact holder.

to the National Center for Health Statistics growth charts

Omnisense utilizes the phenomenon that ultrasound

[16]. Pubertal status was evaluated according to the Tanner

waves propagate faster through the bone than through soft

criteria using a standardized self-report instrument with

tissue. The SOS of ultrasound waves in soft tissue (i.e., skin,

drawings and descriptions of the various stages [17]. Age at

fat, muscle, or blood) is approximately 1540/s. The SOS in

menarche was recorded.

cortical bones ranges from 3300 to 4200 m/s and in trabecu-

lar bones from 1650 to 2300 m/s.

The transducer generates an array of ultrasound waves

Calcium and nutritional intake

that move through the soft tissue and enter the bone. Upon

Data on calcium intake were collected using a nutritional reaching the surface of the bone, the sound waves are

questionnaire developed by the International Nutrition refracted and direction of propagation changes. The waves

Center of Ben-Gurion University of the Negev, Israel [18]. that enter at a critical angle are refracted such that their

A weekly calcium intake report based on a list of foods subsequent direction of travel through the bone is along its

specifying quantity and frequency of intake was completed. long axis, within the bone and parallel to its surface. The

Daily calcium intake was calculated as the sum of the receiver detects a small fraction of the original beam. The

product of the quantity, frequency, and speci c calcium rst waves to be detected are used to calculate SOS. SOS

content of each food consumed. is known to be dependent on several material or bone

parameters, including cortical thickness, density, micro-

structure and elasticity. It has been proven that this type of

Physical activity

dependency exists until cortical thickness is >4 mm.

In our study, two skeletal sites were measured, the distal

Children were divided into four subgroups according to the

1/3 radius and midshaft tibia. The tibia measurement was

level of physical activity reported during the last year: low

obtained by a midline marked halfway down the knee in a

(no regular exercise), normal (school-based exercise), high

sitting position (distance between the top of the knee to the

(regular exercise after school), and very high (participation

sole). The probe was placed parallel to the bone. A scan

in competitive sports).

began from the medial to lateral and back, moving the

probe in a straight line until contact with the tibia was lost.

The operator then moved the probe, again in a straight line,

Speed of sound (SOS) measurements from the lateral side of the leg to the medial side and back

and forth again, until the device indicated that the cycle was

Sunlight Omnisense (Sunlight Medical, Israel) is a quanti- complete. To obtain a radius measurement, a midline was

tative ultrasound bone sonometer measuring velocity of marked, halfway from the elbow to the tip of the third

250

Table 1. Study population characteristics, classi ed by gender

Females Males Total

Mean SD Mean SD Mean SD

n n P value n

Age (years) 42 9.3 2.1 25 9.6 2.8 0.52 67 9.4 2.4

Height (cm) 42 128.7 12.9 25 129.0 14.3 0.92 67 128.8 13.3

Weight (kg) 42 29.1 11.4 25 26.7 8.7 0.36 67 28.2 10.5

BMI 42 17.0 3.7 25 15.6 1.9 0.90 67 16.5 3.2

Ca intake (mg/day) 42 1118.8 462.4 25 1080.5 564.5 0.76 67 1104.5 499.0

Tanner-females 42 1.3 0.6 Not relevant 42 1.3 0.6

Tanner-males 25 1.4 0.8 Not relevant 25 1.4 0.8

Physical activity level 41 1.8 0.4 25 1.6 0.6 0.15 66 1.7 0.5

BMI, body mass index

Table 2. Calcium intake in relation to recommended dietary allowance (RDA)

Age % RDA % Mean Ca intake (mg/day) SD RDA

n

150% 14 42.4 1540.1 346.6

Total 33 100.0 1137.4 461.7

150% 3 8.8 2332.7 216.2

Total 34 100.0 1072.6 537.8

RDA, recommended dietary allowance

nger. The forearm was then outstretched while the wrist Helsinki and the laws and regulations of the Israel Ministry

was placed vertical to the surface. The probe was placed of Health. All parents of the children participating in the

parallel to the radius on its medial surface, and a wide scan study signed an informed consent form.

from side to side was performed.

According to previous studies, the rate of precision of the

Sunlight Omnisense is 0.4% 0.8% [21]. Precision for the Results

population of the present study (based on two separate

measurements of 35 children) was 0.36% [95% con dence

Sixty-seven patients (42 girls, 25 boys) were enrolled in the

interval (CI), 0.25% 0.47%] for the radius and 0.30%

study. Their demographic characteristics are presented in

(0.20% 0.40%) for the tibia.

Table 1. No signi cant differences were found between the

sexes for any of the parameters. Mean age was 9.4 years

Statistical analysis (range, 6 17 years). Most children (76% of girls and 80% of

boys) were at Tanner stage 1. Ninety-three percent of the

Data were analyzed with the SPSS Version 11 statistical girls were premenarche. Sex and social status were not

analysis software. Comparison of the mean and standard found to be a signi cant factor for calcium intake, physical

deviation (SD) of age, anthropometric parameters, calcium activity, and SOS measurements.

intake, physical activity and pubertal stage (descriptive sta-

tistics), was performed separately for boys and girls using

Calcium and nutritional intake

the Student s t test. A P value of 1000 mg/day, n = 34) (Fig. 1). A signi cant difference was

Discussion

found in Z-scores at the radius and tibia between the two

groups (P = 0.004, P = 0.035, respectively). Moreover, the

Our pilot study evaluated the association between bone

low-calcium-intake group had signi cantly lower Z-scores

than the normal controls ( 0.50 and 0.38 SD). status, assessed by QUS technology, and environmental

factors known to in uence bone growth. We found both

Because most of the subjects were in Tanner 1, we per-

calcium intake and physical activity to be positive indepen-

formed the same analysis in those children (low calcium

intake, n = 27; high calcium intake, n = 25). The results were dent predictors of bone growth. The low-calcium-intake

group and the low-physical-activity group had signi cantly

similar to those of the entire group showing a signi cant

lower SOS measurements than the corresponding high-

difference in Z-score between the low- and high-calcium-

intake group (P = 0.003 for radius and P = 0.033 for tibia). level groups.

Z-scores were also lower than normal controls ( 0.51 and Observational study ndings in associating dietary

0.29 for radius and tibia, respectively). Level of physical calcium intake and bone assessment in childhood are incon-

sistent, with some reporting that high calcium intake

activity and age did not signi cantly differ between the two

predicts higher rates of bone mineralization in diverse pop-

groups.

ulations [5,24,25] and others noting no such correlation

[6,26]. This discrepancy may be partially explained by the

Physical activity and SOS measurements different techniques used to collect calcium intake data, the

variety of measured parameters (radial vs. femoral bone

Normal level of physical activity was reported by 68% of mass density, bone mineral content, etc.), different popula-

the children, low level by 30%, and high level by 2% (only tions studied (female vs. male, prepubertal vs. pubertal),

one subject). No differences were found between males and and diverse calcium intake baselines in the different

females. The Student s t test performed between the low- populations.

and normal-activity groups (high-activity group had only Calcium is considered a threshold nutrient where intake

one subject) yielded a signi cant difference in Z-scores at beyond a certain level does not further contribute to bone

the radius and tibia (P = 0.015, P = 0.036, respectively) mineralization [27]. Several studies have used the interven-

(Table 3), but not in calcium intake or Tanner stage. The tional study approach to directly assess the effects of calcium

supplementation on bone mass in young children: Johnston

Table 3. Z-score at the radius and tibia and physical activity level et al. [3] reported on a 3-year trial involving 70 pairs of

identical twins in which one twin received 1000 mg/day

Activity Mean SD

n ANOVA P value*

supplemental calcium and the others received placebo.

0.59

Z-RAD Low 20 1.16 0.015 Among the pairs who were prepubertal for the entire

Normal 43 0.07 0.89 period, those that received supplemental calcium had a sig-

0.53

Z-TIB Low 20 0.96 0.036

ni cantly higher radial and lumbar bone mass density. In

Normal 45 0.03 0.97

the pubertal and postpubertal pairs, no bene t of supple-

ANOVA, analysis of variance; Z-RAD. Z-score at radius; Z-TIB, Z-

mentation was observed. Similarly, Lee et al. [4], in a ran-

score at tibia

domized double-blind controlled trial, demonstrated that

* Between low- and normal-level groups (only one subject reported

calcium supplements resulted in an increase in bone mass

high level of physical activity)

Table 4. Calcium intake, physical activity, and Z-scores at the radius and tibia

Activity Ca intake Radius Z-score Tibia Z-score

Mean SD Mean SD

n P value n P value

1000 mg/day 0.8 0.9

Low 11 1.3 0.50 11 0.8 0.03

>1000 mg/day 0.4

9 1.0 9 0.0 1.0

1000 mg/day 0.4 0.2

Normal 20 0.9 0.002 21 1.1 0.23

>1000 mg/day 23 0.5 0.7 24 0.2 0.8

252

at lumbar and radial areas. However, follow-up reports of a signi cant increase in SOS in male gymnasts compared

these two studies, published 3 years later [28,29], showed with less active control subjects.

that the differences noted between the two groups at the Our observation that children with low levels of physical

end of the trial period were no longer evident once treat- activity have lower Z-scores is in agreement with these

ment was terminated. These ndings indicate that the effects previous studies. Furthermore, within the various physical

on bone accretion rates observed in some clinical trials may activity groups, Z-score at the tibia and radius increased in

not persist into adulthood. Further support for this assump- accordance with the level of calcium consumed (see Table

tion was provided by an extensive review of interventional 4), but without statistical signi cance.

studies by Wosje and Specker [2], who concluded that The main limitation of the present study was the small

increases in bone mass density owing to higher calcium sample size. Although most of the population study were at

intake among children appear to occur primarily in cortical the same pubertal stage (76% of girls and 80% of boys in

bone sites, are most apparent among populations with low Tanner stage 1), the cohort was too small to perform any

baseline calcium intakes, and do not seem to persist beyond strati cation. In addition, there have been no guidelines

the calcium supplementation period. published to date regarding the use of ultrasonography Z-

All the foregoing studies used common X-ray based score in clinical practice. More extensive research is needed

techniques (DXA, single-energy X-ray absorptiometry, to corroborate our ndings.

and quantitative computed tomography). More recently, an In this pilot study, we found a positive association

alternative technique for bone densitometry, in the nonin- between calcium intake, physical activity, and bone status,

vasive assessment of bone mineralization, based on quan- as assessed by the quantitative ultrasound technique.

titative ultrasound (QUS), was introduced [30,31]. Weiss

Acknowledgments The authors thank P. Curchack Kornspan for her

et al. [15] found that the QUS was able to discriminate

editorial and secretarial services.

between patients with osteoporotic hip fracture and normal

controls. Furthermore, some studies have used QUS to

evaluate the association between calcium intake and bone

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