Archives of Osteoporosis (2018) 13:36

https://doi.org/10.1007/s11657-018-0447-3

ORIGINAL ARTICLE

Assessment of dietary calcium intake of university students: a pilot

study in Turkey
Semra Navruz-Varlı 1 & Süleyman Köse 1 & Tuğba Tatar 1 & Sabriye Arslan 1 & Eda Köksal 1

Received: 4 November 2017 / Accepted: 19 March 2018

# International Osteoporosis Foundation and National Osteoporosis Foundation 2018

Abstract
Summary The aim of this study was to adapt the rapid assessment method (RAM) and International Osteoporosis Foundation
Food Frequency Questionnaire (IOF FFQ) tools, used for the assessment of daily calcium intake in university students, and to
compare the data obtained using 24-h recall (24-HR) data. There was a moderate positive correlation between the RAM and IOF.
Purpose/introduction Calcium is an essential mineral that plays vital roles in metabolism and it is very important to accurately
assess the amount of calcium intake on the diet. It was aimed to assess the daily calcium intake of university students by two
different food frequency questionnaires (FFQs) developed specifically for evaluating calcium intake, and 24-h recall method.
Method The study was conducted with a total of 183 female university students aged 18–31. In the study, a questionnaire
including sociodemographic information, a calcium calculator, IOF FFQ, prepared in seven different languages, and RAM was
applied. In addition, 1-day food consumption records were obtained using 24-HR method.
Results The daily average calcium intakes of individuals according to two different food frequency questionnaires (RAM FFQ
and IOF FFQ) and 24-h food consumption records are respectively 1594.2 ± 810.9, 897.9 ± 368.4, and 605.6 ± 278.3 mg. When
the daily average calcium intake was compared with the other two methods, RAM was found to be statistically higher (p < 0.001).
There was a moderate positive correlation between the RAM and IOF FFQ methods (Pearson r = 0.528, p < 0.01) and the intra-
class correlation coefficient between these two methods was found to be significant and moderate (ICC r = 0.452, p < 0.01).
Conclusion In terms of protecting and improving health, it is important to make suggestions using fast and short tools to ensure
adequate calcium intake from young age. It is thought that FFQs are the most appropriate methods in assessing daily calcium
intake for this study group because it is observed that the list of foods and the amount of portions in FFQs reduce the problem of
remembering at 24-h method to a great extent.

Keywords Calcium intake . Food frequency questionnaire . Young adults . 24-h dietary recall method . Rapid assessment method

Introduction

Calcium is an essential mineral that plays an important role in

* Süleyman Köse blood clotting, in the activation of many enzymes, and in
suleyman.kose@windowslive.com
neuromuscular functions and provides skeletal rigidity [1, 2].
Semra Navruz-Varlı
Calcium is being investigated in the pathogenesis and treat-
semranavruz@gazi.edu.tr ment of osteoporosis, hypertension, obesity, and many other
diseases [2–5]. In these studies, using the methods of assess-
Tuğba Tatar
dyt.tugba@hotmail.com ment and determining the amount of calcium intake in the diet
are very essential [3–5].
Sabriye Arslan
Food consumption data can be collected using a wide vari-
sabriyebolluk@hotmail.com
ety of methods and procedures. Twenty-four-hour dietary recall
Eda Köksal (24-HR) method is the most commonly used assessment tool in
betkoksal@yahoo.com
children and adults in large cross-sectional surveys. This meth-
1
Faculty of Health Sciences, Department of Nutrition and Dietetics, od has many advantages even if it does not provide nutritional
Gazi University, Beşevler, 06500 Ankara, Turkey safety and the changes in nutritional habits. One of the
36 Page 2 of 6 Arch Osteoporos (2018) 13:36

advantages of 24-HR method is the ability to seek in detail and RAM form was applied to the individuals in the study. In
check to ensure the correctness of the responses [6, 7]. Hence, addition, 1-day food consumption record was taken from in-
24-HR or more daily recording methods can be used to deter- dividuals by using 24-h recall (24-HR) method. Individuals
mine the validity of other food consumption record tools [8, 9]. with a daily energy intake of < 600 or > 3500 kcal were ex-
Otherwise, food frequency questionnaires (FFQs) have been cluded from the study due to very low or extremely high levels
developed to quickly detect food consumption. These question- [25]. Moreover, if the individual’s FFQ data were missing,
naires can be used to assess the intake of a single food or they were excluded.
nutrient as well as the total diet [10–12]. Block et al. [5] and Ethical approval was obtained from the ethics commission
Willett et al. [6] have established and validated FFQs for eval- of Gazi University (12/09/2016, no: E.149482).
uation of the entire diet; besides, different FFQs have been
designed to identify only one nutrient dietary intake [9, Instruments used to assess calcium intake
12–14]. Among frequency questionnaires designed specifically
for single nutrient intake, there are several FFQs for assessing Rapid assessment method
approved calcium intake to be used in some population sub-
groups [15–18]. In that respect, FFQs are considered to be quite The rapid assessment method (RAM) is an assessment tool
suitable for the assessment of dietary calcium intake [15–18]. that was comprised using the Second National Health and
A calcium-specific FFQ (IOF FFQ) has been developed by Nutrition Examination Survey data and involves basic calci-
the International Osteoporosis Foundation (IOF) for the as- um sources in the American diet [20]. Similar foods are listed
sessment of dietary calcium intake in the general population in groups to facilitate the record of foods. These groups are
and is available online [19]. This questionnaire can be used as milk-yoghurt-cheese, fruit-vegetables, bread-cereals, meat-
a rapid method for the assessment of calcium intake in large fish-chicken-legumes, and fat-sugar-alcohol. This question-
epidemiological studies or clinically. In addition, it can distin- naire asks to quantify the servings of food consumed in the
guish between inadequate and high levels of calcium intake. previous 7 days. Household measures (cups, slices, etc.) are
One of the commonly used FFQs for assessing dietary calci- used to allow participants to more easily estimate portion
um intake in clinical trials is rapid assessment method (RAM). sizes. In this study, RAM was used with a modification.
A variety of studies have been conducted to determine wheth- Buttermilk and kefir, bulghur, cheese/kashar cheese pita, and
er RAM is reliable and valid in adults [20–24]. pita/lavash/flatbread/yufka were added to the list of foods that
Although 24-HR is the most commonly used diet assess- are commonly consumed in Turkey. In addition, walnut, ha-
ment tool in validation studies, using 24-HR is time- zelnut, halvah, and sesame were added to the questionnaire.
consuming and often requires expertise and special software Besides, subgroups were formed in some food groups. For
for analysis. On the other hand, FFQs can be implemented example, in the cheese group, hard cheese, white cheese,
quickly and easily. The aim of this study was to adapt the and soft cheeses were questioned separately. Similarly, the
RAM and IOF FFQ tools used for the assessment of daily vegetables were divided into subgroups as cooked and raw;
calcium intake in university students and to compare the data fruits were divided as berries, other fresh fruits, dried figs, and
obtained using 24-HR data. other dried fruits. Calcium-enriched orange juice, bread, and
quiche were removed from the survey because they were not
consumed in Turkey. In addition, quantities of both home
Method measurements and grams were provided for more convenient
determination of portion sizes of foods. The Turkish Nutrition
Participants and procedure Guidelines 2015 was used in determining the portion sizes
[26]. To determine the calcium content of foods, Nutritional
The study was conducted with 183 females aged 18–31 years Information Systems (BeBiS) program developed specifically
who were studying at Gazi University, Department of for Turkish foods was used [27].
Nutrition and Dietetics. G Power 3 program was used to de-
termine the number of samples. According to the results of International Osteoporosis Foundation Food Frequency
this analysis, when the reference values in the studies that are Questionnaire
closest to the design of the study are taken into consideration,
it is determined that it is sufficient to reach 159 individuals in International Osteoporosis Foundation Food Frequency
the 80% confidence interval [12, 18, 25]. Questionnaire (IOF FFQ) is an assessment tool that asks how
Body weight and height were recorded according to the often the stated foods in the questionnaire are consumed within
statements of the individuals participating in the study and a week [19]. In this tool, the frequency of the intake of calcium
body mass index (BMI) was calculated. A questionnaire in- supplements and 78 foods are questioned. It is possible to reach
cluding the sociodemographic information and IOF FFQ and it online and it has seven different language translations. In this
Arch Osteoporos (2018) 13:36 Page 3 of 6 36

study, strained yoghurt, airan, probiotic yoghurt, kefir, labne Table 1 Characteristics of the participants (n = 183)
cheese, mineral water, and soda which were not included in Age (years)a 20.2 ± 1.8
IOF FFQ but consumed frequently in Turkey were added to Weight (kg)a 56.7 ± 7.9
the questionnaire. Calcium contents of these added foods were Height (cm)a 164.2 ± 5.9
obtained from the BeBiS program [27]. Body mass index (kg/m2)a 21.0 ± 2.5
Body mass index classification (%)
24 h recall
Underweight 26 (14.2)
Normal weight 131 (71.6)
On the day the FFQ questionnaires were applied, dietary re-
Overweight 14 (7.7)
cords were obtained using 24-HR method from all participants
Dietary supplementation (%)
through experienced dietitians. Subjects were asked to recall
Yes 14 (7.7)
everything consumed (including foods, beverages, sauces,
No 169 (92.3)
and condiments) the day prior to the interview. The contents
Commonly used supplements (%)b
of the dishes consumed by the individuals were calculated
Calcium 1 (7.1)
using the book Examples from Turkish Cuisine [28]. The data
Fish oil 1 (7.1)
were analyzed using the BeBiS program for total energy in-
Probiotic 1 (7.1)
take and nutrient intake [27]. Furthermore, the daily calcium
Multivitamin 1 (7.1)
intake of individuals was compared to the Dietary Reference
Vitamin D 3 (21.4)
Intake (DRI) for three methods [29].
Iron supplement 7 (50.2)
Statistical analysis a
Mean ± standard deviation
b
Percentages were taken over 14 participants using supplements
SPSS 22.0 program was used for statistical analysis. The nor-
mal distribution suitability of variables was examined by vi-
sual and analytical methods. Descriptive analyzes were day was 964.1 ± 560.7, 549.5 ± 277.4, and 348.7 ± 136.8 mg,
expressed as means and standard deviations for continuous respectively. When the daily average calcium intake was com-
variables with symmetrical distribution; other variables were pared with the other two methods, RAM FFQ was found to be
expressed as medians with interquartile ranges. The relation- statistically significantly higher (p < 0.001) (Table 2).
ship between daily calcium intake, calculated by 24-HR, The agreements between the data derived from the 24-h
RAM, and IOF FFQ questionnaires, was assessed by the recall and the RAM, or the IOF, are evaluated using the
Pearson and intra-class correlation coefficient (ICC). The Pearson correlation coefficients (r) and intra-class correlation
maximum ICC value is 1.00 and ICC values close to 1.00 coefficients (ICC) in Table 3. There was a moderate positive
indicate that the reliability is high. If correlation coefficient correlation between the RAM and IOF FFQ methods (Pearson
is 0.05–0.30, it indicates low/insignificant correlation, 0.30– r = 0.528, p < 0.01), and the intra-class correlation coefficient
0.40 low middle correlation, 0.40–0.60 medium correlation, between these two methods was found to be significant and
0.60–0.70 good correlation, 0.70–0.75 very good correlation, moderate (ICC r = 0.452, p < 0.01).
and 0.75–1.00 excellent correlation. Statistical significance It was determined that 24-h recall (91.3%) and IOF FFQ
was assessed using the Friedman test, as it was determined method (67.2%) could not meet daily calcium intake accord-
that the calcium intake values determined by the 24-HR, IOF, ing to DRI recommendations in most of the individuals.
and RAM FFQ did not meet the parametric test assumptions. However, in the RAM FFQ method, a large proportion of
Statistical significance was assessed at p < 0.05. individuals (74.3%) met the daily recommendations (Table 4).

Results
Discussion
Table 1 shows the demographic characteristics of the individ-
uals. All of the individuals participating in the study are wom- Calcium is the most abundant mineral in the body and has
en. The average age of the individuals is 20.2 ± 1.8 years. many important functions. Calcium insufficiency causes
The daily average calcium intakes of individuals according many medical problems such as kidney stones, breast and
to two different food frequency questionnaires (RAM FFQ colon cancers, hypertension, and osteoporosis. Inadequate in-
and IOF FFQ) and 24-h food consumption records are respec- take of calcium on a diet is a global health problem [30]. It is
tively 1594.2 ± 810.9, 897.9 ± 368.4, and 605.6 ± 278.3 mg, suggested that the increase of dietary calcium intake decreases
and the amount of calcium they consume per 1000 kcal per the risk of chronic diseases in the general population [31].
36 Page 4 of 6 Arch Osteoporos (2018) 13:36

Table 2 The mean, standard deviation (SD), median, interquartile range Table 4 Adequate/inadequate calcium intake according to Dietary
(IQR), and minimum and maximum values of the individuals’ daily Reference Intakes
calcium intake (n = 183)
Variables Adequate (≥ 1000 mg/d) Inadequate (< 1000 mg/d)
Variables Mean ± SD Median ± IQR Min-max
n % n %
Daily calcium intake
24-h recall (mg/d) 605.6 ± 278.3 570.9 ± 331.1 112.4–1869.1 24-h recall (mg/d) 16 8.7 167 91.3
IOF FFQ (mg/d) 897.9 ± 368.4 831.2 ± 403.0 256.0–2629.0 IOF FFQ (mg/d) 60 32.8 123 67.2
RAM FFQ (mg/d) 1594.2 ± 810.9 1416.4 ± 1004.0 207.0–4205.0 RAM FFQ (mg/d) 136 74.3 47 25.7
p < 0.001 < 0.001
Daily calcium intake per 1000 cal
24-h recall (mg/d) 348.7 ± 136.8 336.1 ± 178.0 96.0–817.0 remembering at 24-h method to a great extent. Also, house-
IOF FFQ (mg/d) 549.5 ± 277.4 521.3 ± 297.5 116.0–2178.3 hold measures (cups, slices, etc.) in FFQs are used to allow
RAM FFQ (mg/d) 964.1 ± 560.7 831.6 ± 714.9 121.3–3753.0 participants to more easily estimate portion sizes. It was
p < 0.001 < 0.001 assessed only for 24 h in 24-HR recall method, while FFQs
were used for the last 7 days. In assessing calcium intake, it
may be more beneficial to use FFQs, which can detect longer
In a study conducted in Spain, the mean daily calcium consumption habits than 24-HR recall method. It was deter-
intake values obtained by using 2-day 24-HR recall and mined that most of the participants could not meet DRI daily
FFQ in healthy adolescents were 564.6 ± 232.0 and 895.9 ± calcium intake recommendations derived from data of 24-HR
343.1, respectively [32]. In another study, the calcium intakes recall (91.3%) and IOF FFQ (67.2%). According to RAM,
obtained using 24-HR recall and FFQ were 949 ± 384 mg and 74.3% of participants met the daily recommendations at a high
1141 ± 387 mg, respectively [33]. In studies, the mean calci- rate. That contradicts the other two methods. This can be ex-
um intake of participants showed many different results. The plained by the differences in declarations of the participants.
variety between the results of calcium intake in different stud- The RAM and IOF FFQ methods have a moderate positive
ies may be due to differences in the populations. Foodways correlation and it was found to be significant but moderate. In
and cultures of different nations may have diversified daily these two methods, correlation is higher than 24-HR because
calcium intake in study groups. In another study, 3-day 24- the participants may be helped to remember because the nu-
HR recall and FFQ were performed to Danish adolescents. trients are listed in both methods.
The daily mean calcium intakes were found to be 867 and In a postmenopausal women study, the correlation between
873 mg/d, respectively [34]. Similarly in this study, the daily FFQ and 24-HR was investigated and found moderate [15]. In
mean calcium intake of the participants according to the RAM another study, the agreement between 7-day FFQ and 24-HR
and IOF FFQ was found higher than the 24-h food consump- recall was examined and a moderate positive correlation was
tion records. Generally, studies have shown that FFQs tend to found [38]. On the contrary, in the study, intra-class correla-
predict more calcium intake than the 24-HR recall [12, 35, tion coefficient between calcium intakes calculated by IOF
36]. Food frequency questionnaire may have led to more FFQ and 24-HR recall was low and statistically not signifi-
markings of consumption by facilitating the selection of nu- cant. In addition, in the present study, there was no significant
trients in the list [37]. Also, when conducting 24-HR recall relationship between the RAM and 24-HR recall. However,
method, participants sometimes may have forgotten their con- there are some studies that an agreement between these two
sumption of food and made a false statement unintentionally. scales was found [21, 22, 35]. In a study conducted on female
In the study group, it is observed that the list of foods and the athletes, the 6-day 24-HR recall and the RAM were performed
amount of portions in these FFQs reduce the problem of and a moderate agreement was found [22]. In another study on
athletes using calcium supplements, the RAM and a 3-day 24-
Table 3 The agreements between the data derived from the 24-h recall HR recall were recorded. A strong positive correlation was
and the RAM, or the IOF, are evaluated using the Pearson correlation
found between the two methods and the interclass correlation
coefficients (r) and intra-class correlation coefficients (ICC)
coefficient was found to be good [21]. A study conducted on
Dependent Independent Pearson ICC adolescents showed a significant moderate correlation be-
variable variable tween the RAM and 24-HR recall [35]. In this study, when
r p r p
Bland-Altman analysis was used to determine the agreement
24-h recall RAM FFQ 0.044 0.557 0.019 0.393 of the methods, no agreement was found between these three
24-h recall IOF FFQ 0.121 0.103 0.127 0.098 methods. Similarly in a study, when Bland-Altman analysis
RAM FFQ IOF FFQ 0.528 < 0.01 0.452 < 0.01 was used, no agreement was found between the methods that
were used [36]. It should be taken into consideration that these
Arch Osteoporos (2018) 13:36 Page 5 of 6 36

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