Iran J Pediatr. 2015 February; 25(1):e177.
DOI: 10.5812/ijp.177
Research Article
Published online 2015 February 20.
Calcium Intake, Major Dietary Sources and Bone Health Indicators in Iranian
Primary School Children
1,*
2
3
4
Nasrin Omidvar ; Tirang-Reza Neyestani ; Majid Hajifaraji ; Mohammad-Reza Eshraghian ;
1
5
5
5
Arezoo Rezazadeh ; Saloumeh Armin ; Homa Haidari ; Telma Zowghi
1Department of Community Nutrition, National Nutrition and Food Technology Research Institute, Faculty of Nutrition and Food Technology, Shahid Beheshti University of Medical Sciences, Tehran, IR Iran
2Laboratory of Nutrition Research, National Research Institute, Tehran, IR Iran
3Department of Food and Nutrition Policy and Programming Research, Tehran, IR Iran
4National Department of Epidemiology and Biostatistics, Faculty of Public Health, Tehran University of Medical Sciences, Tehran, IR Iran
5Department of Nutrition Research, National Nutrition and Food Technology Research Institute, Faculty of Nutrition Sciences and Food Technology, Shahid Beheshti University
of Medical Sciences, Tehran, IR Iran
*Corresponding author: Nasrin Omidvar, Department of Community Nutrition, National Nutrition and Food Technology Research Institute, Faculty of Nutrition and Food Technology, Shahid Beheshti University of Medical Sciences, Tehran, IR Iran. E-mail: omidvar.nasrin@gmail.com
Received: August 15, 2014; Revised: November 18, 2014; Accepted: December 5, 2014
Background: Adequate calcium intake may have a crucial role with regards to prevention of many chronic diseases, including
hypertension, hypercholesterolemia, different types of cancer, obesity and osteoporosis. In children, sufficient calcium intake is especially
important to support the accelerated growth spurt during the preteen and teenage years and to increase bone mineral mass to lay the
foundation for older age.
Objectives: This study aimed to assess daily calcium intake in school-age children to ensure whether they fulfill the FGP dairy serving
recommendations, the recommended levels of daily calcium intake and to assess the relationship between dietary calcium intake and
major bone health indicators.
Patients and Methods: A total of 501 Iranian school-age children were randomly selected. Calcium intake was assessed using a semiquantitative food frequency questionnaire. Bone health indicators were also assessed.
Results: Dairy products contributed to 69.3% of the total calcium intake of the children. Daily adequate intake of calcium was achieved by
17.8% of children. Only 29.8% met the Food guide pyramid recommendations for dairy intake. Dietary calcium intake was not significantly
correlated with serum calcium and other selected biochemical indicators of bone health.
Conclusions: The need for planning appropriate nutrition strategies for overcoming inadequate calcium intake in school age children in
the city of Tehran is inevitable.
Keywords: Calcium Intake; Food Groups; Children
1. Background
Adequate calcium intake may have a crucial role with
regards to prevention of many chronic diseases, including hypertension (1, 2), hypercholesterolemia (3), different types of cancer (4, 5), obesity (6-8) and osteoporosis
(9). In children, sufficient calcium intake is especially
important to support the accelerated growth spurt during the preteen and teenage years and to increase bone
mineral mass to lay the foundation for older age (10-12).
In terms of density and bioavailability, milk and other
dairy products are the best dietary sources of calcium
(13). Considering the nutritional value of milk and dairy
products and the poor food choices in today’s daily intake
of children and adults, consumption of dairy products is
being perceived as an important indicator of adequate
calcium intake in one’s diet (14). However, the contribution of other sources of calcium to children’s diet can
vary between different nations due to social, cultural
and economic factors that affect dietary pattern (15-18).
Recent reports have shown low calcium intake and dairy
products consumption globally, especially in children
and adolescents (19-22).
In Iran, based on the last national household food consumption survey data, calcium is the most limiting nutrient in the nation’s diet (23). On the other hand, previous research done in 23 provinces of Iran reported the
prevalence of hypocalcaemia in approximately 60% of
eight to ten year old school children (24). In addition,
an increase in the prevalence of osteoporosis in the
country (2) and recent reports on the high prevalence of
vitamin D deficiency in urban children (25), has raised
concern about the dietary calcium intake in Iranian
children and adolescents. Limited data is available on
the dietary intake of Iranian children. From a public
health point of view, therefore, determining the extent
to which calcium inadequacies may be occurring is of
great value.
Copyright © 2015, Growth & Development Research Center. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License (http://creativecommons.org/licenses/by-nc/4.0/) which permits copy and redistribute the material just in noncommercial
usages, provided the original work is properly cited.
Omidvar N et al.
2. Objectives
We assessed calcium intake in school children to ensure
whether they fulfill the Food Guide Pyramid (FGP) dairy
serving recommendations, the recommended levels of
daily calcium intake and also to evaluate the circulating
bone health indicators and their relation to dietary calcium intake.
3. Patients and Methods
rolled in the study. Students provided written consent
to enroll in the study. Overall 501 students from grades
4 and 5 from 47 (out of 60 schools in the original study)
elementary schools were included in this sub-study. The
study protocol was scientifically and ethically approved
by the Research Council and the Ethical Committee of the
National Nutrition and Food Technology Research Institute, respectively (25).
3.2. Dietary Intake
3.1. Subjects
The study population was a subsample of a larger study
entitled “vitamin D status of 9 - 12-year-old primary-school
children in Tehran during autumn and winter 2007 - 2008
(25) who were selected randomly from the main sample.
For the main study, a two-stage sampling was performed.
In the first stage, sixty primary schools were selected
through systematic random sampling from the schools
in all nineteen districts of the Ministry of Education in
the city of Tehran. In the second phase, sixteen to twenty
children from each school from grades 4 and 5 were en-
For this study, calcium intake was assessed using a 60item quantitative food frequency questionnaire (FFQ),
specifically designed for dietary sources of calcium. The
steps followed for design and validation of the questionnaire has been reported elsewhere (26). The questionnaire
was completed through face-to-face interviews with the
children by trained nutritionists at schools. A food photo
album and measuring cups were used to ensure accuracy
of the reported servings. For each food item in the FFQ,
frequency of intake was asked on a “day/week/month/or
never" basis. Following this, serving size was assessed as
"usual serving size in each time of consumption".
Table 1. Food Groupings in the Study Based on Dietary Guidelines and Calcium Contents
Food Groups
Items
Dairies
Fluid milk
milk, cocoa milk, coffee milk, chocolate milk, flavoured milk
Yogurt
regular yogurt and drained yogurt
Cheese
all types, mainly feta
Others
kashk/evaporated yogurt, ice cream, dough/yogurt drink
Breads and Cereals
Breads
Rice and pasta
Cookies, sweet rolls
different types of Iranian flat breads, white bulky breads, French and other breads
all types of rice, pasta, wheat
all kinds of cookies, sweet rolls (biscuits, cookies, cakes, confectionaries, Danish roll)
Fruits
Citrus
orange, tangerine
Other fruits
apple, dogberry, plums, other
Dried fruits
raisins, dried sloe, dates, tamarind
Fresh fruit juice
natural fruit juice (orange, apple)
Vegetables
Tomatoes
Cucumber
tomatoes (cooked or raw)
cucumber
Lettuce
lettuce (salad/leaves)
Cabbage
cabbage (white/red/cauliflower/broccoli/ Brussel sprouts as pickled, cooked/raw)
Green leafy vegetables
and spinach
green leafy vegetables, spinach (raw, cooked, stewed)
Meats and alternatives
Meats and eggs
Fish
Legumes
Nuts
2
red meat:(stew /broth/muscle/kebab, minced meat, hamburger, chicken, eggs
any type of fresh or frozen fish, canned tuna fish
lentil, beans: red /white/wax bean, peas, split peas, and soy nut
walnuts, almonds, peanuts, pistachios, hazelnuts, sunflower seeds, watermelon seeds, pumpkin
seeds, hemp, sesame, Halva Shekari/sesame sweets, and chocolate
Iran J Pediatr. 2015;25(1):e177
Omidvar N et al.
FFQs were analyzed for the daily amount and food
sources of calcium intake. All food items included in the
FFQ food list were also grouped according to Iran’s FoodBased Dietary Guideline (27). To determine the specific
food types, six main groups of the guidelines were then
subdivided into 20 groups Table 1.
Number (%) of children meeting the FGP recommendations and Recommended Dietary Allowance (RDA) was
identified. FGP recommendation for 9-13 year-old age is
three servings/day and RDA recommendation (Adequate
Intake: AI) is ≥ 1300 mg/day.
groups and post hoc Tukey HSD test was used to compare
within-group differences. The Chi square test was used
to compare qualitative data between groups. Energy adjusted calcium intake of different food groups was calculated using residual method. Correlations between nonnormally distributed variables including dietary calcium
intake and serum concentrations of calcium and other
bone biomarkers were evaluated using Spearman’s equation. P < 0.05 was considered statistically significant. All
statistical analyses were performed using SPSS version 17
(SPSS Inc., Chicago, IL, USA).
3.3. Socio-Economic Characteristics
4. Results
Socio-economic factors were evaluated through an interview with a questionnaire. Variables such as: family
size, father’s and mother’s education (illiterate, primary/
middle school, high school diploma, university degree),
father’s and mother’s occupation (unemployed, low,
middle, high) and Socio Economic Status (SES) by district
(low, middle, high) were included.
Characteristics of the 501 studied school-age children
are presented in Table 1. There were no differences in anthropometric profile and the socioeconomic characteristics between girls and boys.
3.4. Selected Circulating Bone Health Biomarkers
The procedure of blood sampling and handling is fully
described elsewhere (25). Briefly, venous blood samples
were taken and stored in the dark until serum separation. Sera were transferred to clean micro tubes in aliquots and kept at -80°C until the day of analysis. Serum
25(OH)D3 was determined using a competitive proteinbinding assay (Immunodiagnostic, Bensheim, Germany).
Concentrations of osteocalcin (OST; Biosource Europe SA,
Nivellles, Belgium), intact parathyroid hormone (iPTH;
DRG Instruments GmbH, Marburg, Germany) were all determined using enzyme immunoassay by an automatic
system (StatFax 3200 micro plate ELISA reader; Awareness
Technology, Inc., Palm City, FL, USA). Calcium, magnesium
and phosphorous serum levels were measured by commercial kits (Pars Azmoon, Iran) based on colorimetric
methods using an automatic device (Selectra E, Vitalab,
The Netherlands).
3.5. Estimation of Daily Calcium Intake
Calcium content of food items was determined based on
the revised edition of the Iranian food composition table.
Estimates of calcium intake per day were obtained using
Microsoft Office Excel 2007, by multiplying frequency per
day by the calcium content per gram and gram weight of
eaten food and adding together total intake.
3.6. Statistical Analysis
Normality of data distribution was evaluated using the
Kolmogrov-Smirnov test. Data were expressed as mean
and as a standard deviation. Comparison of normally distributed data between the two groups was done by using
an independent sample t test. One way-analysis of variance (ANOVA) was used for comparison of more than two
Iran J Pediatr. 2015;25(1):e177
4.1. Total Daily Calcium Intake
Total daily energy and dietary calcium intake of the
children and the adequacy of calcium intake compared
to RDA is presented in Table 2. The girls in the study consumed less dietary calcium in comparison to the boys but
the difference was not statistically significant. However,
after adjusting for energy intake, calcium intake of boys
from meats and alternatives (specifically meats and eggs
subgroups) and, bread and cereals (specifically breads)
were significantly higher than for girls. Dairy products
were the main food sources of calcium in the studied
children; whereas only one third of the children had adequate daily servings of dairy products, based on current
recommendations (two to four servings of dairy products daily) (28). Only 17.8% of participants had adequate
daily intake of calcium (≥ 1300 mg/day) and 29.8% met
the FGP recommendations for dairy intake (≥ 3 serving/
day). More than half of the children had calcium intake
below 75% of RDA, while inadequate dairy intake (< 1 serving/day) was observed in 10.2%. Dairies provided 69.3% of
total calcium intake of the studied children.
4.2. Major Sources of Dietary Calcium
As demonstrated in Table 3, major dietary sources of
calcium that contributed to total daily calcium intake
were dairy products (71.9%) [specifically yogurt and milk],
breads and cereals (10.5%) [specially breads], fruits (7.4%)
[specially citrus], meats and alternatives (6.6%) [specially
nuts], as well as vegetables (4.4%) [specifically green leafy
vegetables]. Except for the vegetables, the average calcium intake from the four other groups was higher in boys
as compared to girls; the differences were significant just
for breads and cereals and fruit groups (P < 0.05). After
adjusting for energy intake, the differences became significant only in meats and alternatives (specifically in
meats and eggs subgroups) and bread and cereals (specifically breads) (data are not shown in Table 3).
3
Omidvar N et al.
Table 2. Total daily Energy, Dietary Calcium Intake and Selected Bone Health Indicators of School age Children in Tehran, 2008 a, b, c
Variable
Girls (n = 244)
Boys (n = 257)
Total (n = 501)
P Value
Total energy intake/day
1437.0 (545.0)
1563.2 (597.6)
1501.8 (575.5)
< 0.05
Dietary calcium intake, g/day
901.2 (447.7)
932.8 (434.4)
917.5 (440.8)
0.42
Meeting AI, ≥ 1300 mg/day d
46 (18.9)
48 (18.7)
94 (17.8)
0.96
Inadequate calcium intake, Total Ca intake < 75% RDA d
151 (30.1)
149 (29.7)
300 (59.9)
0.37
Dairies consumption, serving/day
2.4 (1.3)
2.5 (1.3)
2.3 (1.2)
0.42
Meeting FGP recommendations, ≥ 3 serving/day d
74 (30.3)
71 (27.6)
145 (28.9)
0.58
27 (11.1)
24 (9.3)
51 (10.2)
0.58
Total calcium intake from dairies d
69.8 (13.8)
68.7 (12.0)
69.3 (12.9)
0.10
Serum Ca, mg/dL
9.6 (0.68)
9.7 (0.58)
9.6 (0.03)
0.51
Serum P, mg/dL
4.5 (0.61)
4.5 (0.60)
4.5 (0.03)
0.40
Inadequate dairy intake, < 1 serving/day d
Serum Mg, mg/dL
2.2 (0.17)
2.1 (0.16)
2.1 (0.01)
0.15
iPTH, mg/L
61.4 (41.2)
40.1 (18.6)
43.4 (0.83)
0.53
OST, ng/mL
43.9 (17.4)
42.9 (16.6)
50.7 (1.68)
< 0.001
25(OH)D3, nmol/L
16.9 (14.0)
28.5 (22.2)
22.8 (0.94)
< 0.001
a Data are presented as No. (%) or Mean ± SD.
b Significance calculated by independent t test or Chi-square test depending on the type of variables.
c Food guide pyramid (FGP) recommendations for 9 - 13 year old: three servings/day.
d % total calcium intake from dairies: dairy calcium intake, mg/day total calcium intake, mg/day × 100.
Table 3. Contribution of Food Groups (Mean ± SE) to Total Daily Calcium Intake, g/day of School age Children by Gender, Tehran,
Autumn and Winter 2007 - 2008 a
Food Group
Girls (n = 244)
Boys (n = 257)
Total (n = 501)
From Total Calcium intake, %
Dairies
653.6 (24.2)
666.2 (22.6)
660.3 (17.7)
71.9
P Value
0.91
Fluid milk
272.5 (13.7)
275.3 (11.7)
273.9 (9.0)
29.8
0.49
Yogurt
275.0 (16.1)
277.0 (16. 2)
276.1 (11.4)
30.2
0.93
Cheese
58.7 (3.4)
63.1 (3.3)
60.9 (2.4)
6.6
0.36
Others
47.3 (3.4)
50.7 (3.0)
49.4 (2.0)
5.3
0.43
Breads and Cereals
90.1 (1.3)
100.8 (3.3)
96.7 (2.3)
10.5
< 0.05
Breads
56.9 (3.3)
66.6 (2.4)
62.9 (1.6)
6.8
< 0.01
Rice and pasta
0.0 (0.0)
0.0 (0.0)
0.0 (0.0)
0.0
-
Cookies, sweet rolls
33.1 (2.3)
34.1 (1.8)
33.6 (1.4)
3.7
0.73
Fruits
62.5 (2.8)
73.4 (3.3)
68.0 (2.2)
7.4
< 0.05
Citrus fruits
46.6 (2.3)
54.8 (2.6)
50.8 (1.8)
5.5
< 0.05
Other fruits
3.5 (0.2)
4.2 (0.3)
3.8 (0.1)
0.5
0.06
Dried fruits
7.6 (0.8)
10.1 (1.2)
8.9 (0.3)
0.9
0.09
Fresh fruit juice
4.6 (0.4)
4.1 (6.3)
4.3 (0.3)
0.5
0.49
Vegetables
41.6 (2.4)
38.8 (0.3)
40.9 (1.5)
4.4
0.08
0.09
Tomatoes
3.8 (0.3)
3.1 (0.2)
3.5 (0.2)
0.3
Cucumber
9.0 (0.6)
9.5 (0.7)
9.3 (0.4)
1.1
0.57
Lettuce
2.0 (0.1)
2.2 (2.9)
2.1 (0.1)
0.2
0.47
Cabbage
6.0 (0.6)
5.9 (0.1)
6.0 (0.4)
0.6
0.95
Green leafy vegetables
and spinach
20.5 (1.7)
17.8 (1.3)
19.1 (1.0)
2.2
0.19
Meats and alternatives
59.8(4.2)
61.5 (3.7)
60.7 (2.8)
6.6
0.36
Meats and eggs
19.2 (0.9)
23.2 (1.0)
21.3 ( 0.6)
2.2
< 0.01
Fish
1.5 (0.1)
1.8 (0.1)
1.7 (0.1)
0.1
0.12
Legumes
10.9 (1.1)
12.6 (1.3)
11.8 (0.8)
1.2
0.21
Nuts
29.8 (3.5)
26.3 (2.8)
32.1 (2.6)
3.3
0.07
a Comparison of calcium intake between two genders was done by t-test. After adjusting for energy intake by residual method, differences between the
two genders in calcium intake, mean intake of fruits group, citrus fruits and breads subgroups became insignificant. Instead, the difference of calcium
intake of meats and alternatives became significant; breads and cereals group as well as meats and eggs subgroup remained significant (P < 0.05).
4
Iran J Pediatr. 2015;25(1):e177
Omidvar N et al.
4.3. Association Between Dietary Calcium Intake
and Socio-Demographic Factors
Comparison of total calcium intake (mg/day) according to the characteristics of socio-economic status (SES)
of the school age children by gender is presented in
Table 4. Total calcium intake of children was not significantly different between the three socioeconomic districts; however, among girls, mean total daily calcium
intake was significantly different between the three
SES districts. Comparisons within districts showed that
mean total calcium intake of girls in middle SES districts was significantly lower than in boys in both low
and high SES districts. Also, significant difference was
seen between the two genders' calcium intake in middle
SES districts (P < 0.05). No significant differences were
found between other socioeconomic variables within
genders.
Table 4. Comparison of Total Calcium Intake (mg/day) According to Socio-Economic Characteristics of the School age Children by
Gender, Tehran a, b, c, d
Variables
Girls (n = 244)
Boys (n = 257)
Total (n = 501)
P Value
≤3
960.0 (80.2)
879.9 (73.5)
934.5 (55.4)
0.39
>3
888.0 (30.4)
939.9 (30.1)
917.4 (21.4)
0.22
High
836.7 (59.0)
1029.1 (97.6)
920.5 (54.9)
0.09
Middle
944.5 (38.0)
938.7 (33.6)
941.6 (25.3)
0.90
Low
816.4 (69.2)
935.2 (67.6)
878.5 (48.5)
0.22
Unemployed
767.9 (43.2)
795.6 (71.6)
781.6 (70.1)
0.18
0.30
0.08
0.06
320.5 (167.2)
1403.2 (290.9)
1186.7 (312.5)
Primary/middle school
811.9 (47.4)
893.6 (47.6)
857.5 (33.9)
0.23
High school/Diploma
935.3 (50.8)
933.9 (44.1)
934.6 (33.6)
0.98
University degree
955.6 (53.7)
955.7 (54.4)
955.7 (38.1)
0.99
0.14
0.14
0.13
Family Size
Father’s occupation
P-value
Father’s education
Illiterate
P-value
0.19
Mother’s occupation
High
536.4 (127.8)
-
536.4 (127.8)
-
Middle
1059.5 (73.3)
1036.9 (65.7)
1046.4 (48.6)
0.82
Low
792.3 (273.5)
834.2 (174.8)
822.2 (80.8)
0.83
Unemployed
889.4 (32.4)
918.2 (32.7)
903.3 (23.0)
0.53
0.16
0.25
0.08
Illiterate
808.0 (234.4)
1416.6 (250.4)
1112.7 (256.3)
0.08
Primary/middle school
803.5 (45.0)
925.9 (415.0)
874.2 (32.8)
0.06
High school/ Diploma
949.2 (43.3)
907.4 (42.6)
929.4 (30.4)
0.49
University degree
902.9 (68.0)
1000.3 (58)
952.1 (44.9)
0.28
0.12
0.08
0.34
P-value
Mother’s education
P-value
SES by district
Low
973.0 (57.7)
940.3 (61.3)
958.1 (41.9)
0.41
Middle
780.3 (44.35)
964.5(48.5)
880.3 (33.9)
< 0.05
High
950.2 (46.5)
901.8 (37.6)
925.1 (21.5)
0.10
< 0.05
0.58
0.31
P-value
a Significance of differences between girls and boys calculated by independent t test or one way-ANOVA test depend on the type of variables.
b The independent sample t was not computed because High level occupation box in boys group was empty.
c One way-ANOVA test was used to compare mean of total calcium intake between groups in each gender and in total participants.
d P < 0.05 in comparison with Low and high SES districts. (Tukey HSD test was used in order to comparison within group.
Iran J Pediatr. 2015;25(1):e177
5
Omidvar N et al.
Table 5. Spearman Correlation Between Dietary Calcium Intake and Selected Parameters Affecting Calcium Homeostasis in Iranian
School age Children
Coefficient Parameters
Total
Dietary Ca, mg/day
Serum Ca, mg/dL
Serum P, mg/dL
Dietary Ca,
mg/day
Serum Ca,
mg/dL
Serum P,
mg/dL
Serum Mg,
mg/dL
iPTH, mg/L
OST, ng/mL
25(OH)D3,
nmol/L
-
0.09
-0.06
-0.02
-0.08
0.0
0.09
-
0.11 a
0.05
0.02
-0.18 b
0.02
-0.06
0.11 a
-
0.12 a
0.03
-0.12 a
0.08
-0.09
Serum Mg, mg/dL
-0.02
0.05
0.12 a
-
0.06
-0.10 a
Ipth, mg/L
-0.08
-0.22 b
0.03
0.06
-
0.11
-0.18 b
OST, ng/mL
0.0
-0.18 b
-0.12 a
-0.10 a
0.11
-
0.04
-0.09
-0.18 b
0.04
-
25(OH)D3, nmoL/L
0.08
0.02
0.08
a P < 0.05.
b P < 0.00.
4.4. Selected Parameters Affecting Calcium Homeostasis
There were no significant differences between boys and
girls in serum calcium, phosphorus, magnesium and
OST. However, boys had significantly lower serum iPTH
but higher 25 (OH) D3 than girls (P < 0.001) (Table 2).
Dietary calcium intake was not significantly correlated
with serum calcium or other biochemical biomarkers of
bone health. Serum concentrations of iPTH inversely correlated with those of 25(OH) D3. Table 5 shows the results
of Spearman analysis among other variables.
5. Discussion
The findings of this study revealed that the dietary calcium intake of Tehranian 9-12 year-old-children was relatively low, with more than half having inadequate intake.
Adequate intake of dairy product is associated with better linear growth and bone development during childhood (29). However, recent reviews of the effect of dairy
product and calcium consumption on bone health have
presented conflicting conclusions. In the present study,
no relationship between dairy product consumption and
circulating markers of bone health was observed.
Based on the last report of the American Dietetic Association in 2011, the AI of Ca in 9-13 year old school age
children (male and female) is 1300 mg/day (30). In the
present study only 17.8% of Tehran school children met
the AI. A study by Storey and colleagues on USDA data, on
calcium consumption of 9-13 year old girls and boys have
shown higher proportion of children with AI: 842 (65%
AI) and 1022 (79% AI) mg/day, respectively (18). However,
based on CSFII (Continuing Survey of Food Intake by Individuals) and NHANES (National Health and Nutrition Examination Survey) datasets, 18.4% of individuals aged 9-13
years had AI of Ca (13) while in non-Hispanic white girls
only 31% of 9 year old and 27% of 11 year old girls met the AI
of Ca (31). In a study that was done on 1176 Spanish 5 to 12
years old schoolchildren, calcium intake below 800 mg
per day was considered as insufficient intake; and 18% of
6
girls and 13% of boys did not consume these amounts (32).
In our study, more than half of children had inadequate
calcium intake (< 75% RDA). In comparison with present
study, in a representative sample of Spanish children (7
to 11 years) from 10 Spanish provinces, calcium intake was
lower than that recommended in 76.7% of the children
and 40.1% had insufficient intake (< 67% of recommended
intake) (33).
In this study, mean total calcium intake of girls and boys
was not significantly different however, girls in middle
socioeconomic districts had a significant lower intake
than in high and low SES districts. It has been shown that
good calcium intake during adolescence may improve
peak bone mass (34). This effect may be due to the linkage
of calcium intake with androgens, as low calcium intake
may be associated with decreased serum androgens in
pre-pubertal girls which may lead to delayed skeletal maturity (35). No difference was observed in calcium intake
of boys based on SES.
In the USDA report, there was a small difference in calcium intake between American boys and girls after controlling of confounders (age, race/ethnicity, diet, and
beverages); however, being female was significantly associated with 26 mg less calcium consumption in 9–18 year
old children (18). Also, an analysis on NHANES II data has
shown higher intake of calcium in 3-18 year old boys compared to girls (36). Fiorito and colleagues in a survey on
151 girls from middle-class, non- Hispanic white families
living in central Pennsylvania, showed that girls at age 9
and 11 years did not meet calcium and phosphorus recommendations (31).
Dairy products are the best sources of calcium because
of their high calcium content and bioavailability, high
amounts of other essential nutrients for bone health with
relative low cost (13). USDA’s Food Guide Pyramid (FGP)
recommends that individuals 2 years and over consume
2-3 servings of dairy per day depending on age (37). In our
study, almost two thirds of participants (69.7% of girls and
72.4% of boys) did not meet the Food Guide Pyramid (FGP)
recommendations for dairy intake. However, in datasets
Iran J Pediatr. 2015;25(1):e177
Omidvar N et al.
of the CSFII and NHANES, 44.5% of American children in
2-8 years of age and 19.2% of them in 9-18 years of age met
the FGP (13). Furthermore, Fiorito and colleagues found
that girls at age 7, 9, and 11 years did not meet the recommended dairy level for their age (three servings per day)
and only 39% of 11 year old girls met dairy recommendations (31). In the USDA survey, servings of milk products
had the strongest relationship with calcium consumption and each additional gram of milk product was associated with a 1.2 mg increase in calcium consumption
for ages 9-18 (18). Storey and colleagues showed that consumption of milk and milk products has the strongest association with calcium consumption (18). Also, Gao and
colleagues have reported that in American 9 to 18 year old
participants of NHANES from 2001-2002, average calcium
intakes in both females and males were lower in those
who did not consume dairy products in comparison with
those who consumed these products (38).
In the present study, some differences in food sources
of calcium were observed between the two genders. After
adjusting for energy intake, the calcium intake of boys
from meats and alternatives (specifically in meats and
eggs subgroups) and, bread and cereals (specifically in
breads) groups were significantly higher in the boys compared to the girls. In total sample, calcium was mainly
provided by dairy products (especially yogurt and milk).
Other sources of calcium, in order of the amount of consumption, were bread and cereals, meat and alternatives,
fruits and vegetables. In the current study, findings are
relatively comparable with results of the study in Spanish
schoolchildren in whom food dietary calcium came from
dairy products, dietetic products and infant formulae, cereals, vegetables, fruits, pre-cooked meals, meats, fish and
pulses, respectively and there was no difference between
genders (33). Furthermore, in 696 of 2.5-6.5 year-old Flemish preschoolers, in 58 food groups, calcium and vitamin
D intake was computed and milk, sweetened milk drinks
and cheese were the main sources of calcium intake (16).
Few studies have described socio-demographic factors
associated with low calcium intake (17, 39-41). In the present study, socioeconomic factors were not related with
mean calcium intake. However, calcium intake of middle
classes districts was lower than that of both wealthy and
deprived group and a significant result was seen only in
girls. In the current study, results are in line with those of
Eck and Hackett-Renner (36) on NHANES II data in 3-18 year
old boys and girls indicating that socioeconomic status
was not a significant predictor of Ca intake. In contrast,
Sanwalka and colleagues (17) in a study on calcium intake
and its sources in 400 adolescent boys and girls from
two lower and upper socioeconomic strata, in Pune, India, showed significant difference between districts and
genders. The highest median of calcium intake was in the
upper economic strata boys (893 mg, 689-1295) and the
lowest intake was in lower economic strata girls (506 mg,
380-674). The median calcium intake was much lower in
lower economic strata than in the upper economic strata
Iran J Pediatr. 2015;25(1):e177
both in boys and girls; and, girls from both groups had
less access to dairy products as compared to boys. Also,
the results of current study is consistent with findings
of the study performed by the Mexican National Health
and Nutrition Survey in 2006 that school-age children
at the lowest SES, showed the highest inadequacy for calcium intake (42). In 5-11 year old participants of NHANES
III , 44.0% of Low SES girls and 37.3% of Low SES boys had
enough dairies consumption (adequate dairy recommendation in this study was defined as ≥ 3 servings/day
in girls and ≥ 4 servings/day in boys) (43). However, in
the present study, only in the middle district mean intake
of boys was significantly higher than that of girls. This
does not appear to be due to less access to dairy products
or other calcium rich foods in girls, since dairy intake
and total calcium intake was not significantly different
between the two genders. There is no logic explanation
for the lower calcium intake observed in children from
middle districts; it may be attributed to low accuracy in
data collection or other factors that cannot be clarified
by the present data.
In the present study, dietary calcium intake was not correlated with serum calcium and other studied indicators
of bone health. Similar to our study, in white adolescent
girls at 11 to 16.9 years of age serum calcium and phosphate levels were not associated with calcium intake;
while 25 (OH) D levels was associated with calcium and
phosphate levels (44). In contrast, Bueno and colleagues
(45) assessed calcium and vitamin D intake and biochemical tests in 58 short-stature Brazilian children and adolescents and showed that there is a negative correlation
between calcium intake and PTH and a positive relationship between dietary calcium and serum 25(OH)D and
25(OH)D and serum calcium. Rajah and colleagues (46)
found same results and reported that 25(OH)D concentrations were directly correlated with calcium, phosphorous and PTH. However in our study, serum levels of calcium and 25(OH) D were not correlated. In another study
done on young Japanese women (aged 18-22) dietary intake and serum phosphorus and calcium were positively
correlated (47).
There were not any significant differences between boys
and girls in serum calcium, phosphorus, magnesium and
OST; but serum iPTH and 25(OH) D3 were significantly
higher in boys. Based on our previous report (25), 86%
of the children had vitamin D deficiency, with 38.3% being severely deficient (25(OH) D < 12.5 nmol/L) and 10.4%
of them being hypocalcemic (serum Ca < 9 mg/dL). In a
study conducted on 183 urban boys and girls ( ≤ 12 years
old living in Abu Dhabi, in 8-12 years old group, 31.2% had
vitamin D deficiency, and 14.5% were hypokalemic (46).
Serum iPTH was inversely correlated with serum 25-OH
D3 that is in accordance with other similar studies (44,
46, 48, 49) however, this result was not observed in a
study performed on short stature children in Brazil (45).
Scant evidence supports nutrition guidelines focused
specifically on increasing milk or other dairy product
7
Omidvar N et al.
intake for promoting child and adolescent bone mineralization (50).
In our study, serum calcium was directly correlated with
serum phosphorus and inversely correlated with serum
iPTH and osteocalcin, and serum calcium, phosphorus
and magnesium were inversely associated with serum
osteocalcin. Similar findings are reported by other studies (51, 52). In contrast to our findings, in a study done on
black children of South Africa, there was no correlation
between serum Ca and P concentrations (53).
To our knowledge, this is the first report on calcium intake of Iranian primary school children. The strength of
this study was the high response rate in all schools. The
study has some limitations attributed to all cross-sectional studies. The observational design of this study does not
allow one to conclude cause-effect relations.
The findings suggest inadequate calcium consumption
among both genders of Tehran’s school age children. Dietary calcium was not related to any of the bone health
indicators. Considering the fact that dairy products
were the main dietary source of calcium in the studied
children, the best way to increase calcium consumption
in studied samples is implementation of strategies and
nutritional educational programs that increase the consumption of dairy products in this vulnerable group. Also
based on Dietary Guidelines (13), other nondairy sources
of calcium (e.g. canned fish with bones, fortified orange
juice, fortified soy beverage, and some dark green leafy
vegetables) should be promoted in food baskets of Iranians in order to secure the amount of recommended calcium in the diet. Physical activity appears to be one of the
primary modifiable stimuli for increased bone growth
and development. Future studies should include modifying factors affecting on bone health and growth such as
physical activity in their design and analysis.
Acknowledgements
The authors would like to thank the subjects who participated in this study. We are grateful to the staff of the nutrition department. This study was part of a large study
of Vitamin D Study in NNFTRI School Children of Tehran
(VDST).
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
Funding/Support
20.
This work was supported by "National Nutrition and
Food Technology Research Institute" of Shahid Behehshti
University of Medical Sciences (grant No. 2027). None of
the authors had any personal or financial conflicts of interest.
21.
22.
23.
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