Dietary pattern and factors associated with anemia among

female adolescents in Islam private schools

Sanma Hayeemad 1, Mandhana Pradipasen1, Waraporn Satheannoppakao1, Ratchada Kaseamsub2
1. Nutrition Department, Faculty of Public health, Mahidol University
2. Pediatric Department, Queen Sirikit National Institute of Child Health

Abstract
Introduction The objective of this study was to identify the prevalence of anemia
(Hematocrit < 36% and/or Hemoglobin <120 g/L) among Muslim adolescents and identify
possible factors related to anemia.
Meterials and methode The study population consisted of 276 schoolchildren age
1315 years old attending in Islam private schools, located in the urban district of Songkhla.
Certain hematological indices of anemia status were measured. Dietary intake was estimated
using semiquantitative food frequency questionnaire (SFFQ).
Results The prevalence of anemia among female adolescents in Islam private schools
was 46.4%. The data showed that age, menstruation, nutritional status, costs, frequency of
meal, fruit consumption and beverages were not significantly associated with anemic
status(p>0.05). Nonanemia students consumed higher iron, copper and zinc than anemic
students (p<0.05), however, most of the students (85.5%) consumed food with iron value
lower than 67% RDA.
Conclusions the anemia prevalence was very high among Muslim adolescents from
urban district of Songkhla. The factor associated with anemia is a consumption of low iron
value food source.

Keyword: Dietary Patterns, Anemia, Female adolescents, Islam private school

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Introduction
Anemia is a condition of having lower than normal number of red blood cells
(erythrocytes) in the blood, indicated by a decrease in the amount of hemoglobin, based on
gender, age and country (Sriswasdi C.,1997). Even though is a common problem in clinical
practice, this condition is not a single disease but signs and symptoms of many diseases, such
as lack of nutrients including iron, folate, vitamin B12; Thalassemia; Sideroblastic Anemia;
etc.. Anemia is a significant public health problem because it represents a systemic condition
with numerous health consequences including fatigue, delayed or impaired growth and
development, increased susceptibility to infection secondary to depressed immune system
function, decreased intellectual performance and physical performance or exercise capacity.
More often that the persons anemic learn of their condition from the annual health check or
laboratory examination than from symptoms and signs of the disease (Hoffman R.et al.,
2005).
The physical change from children into adults at puberty in early adolescents such as
rapid of the body growth; a rapid increase in weight and height; changes of the body
proportion; etc, all increased of demand nutrients and energy for rapid growth and
development (Hoffman R.et al., 2005) Young women are particularly at high risk to iron
deficiency because rapid growth combined with menstrual bleeding could be one of reason
leading to iron deficiency and anemia.
A study by the World Health Organization found that the prevalence of anemia in
women aged 15-50 years worldwide was 30.2% (WHO, 2005). Anemia remains an important
health problem in Thailand, especially among school age children and early adolescents in
the Southern Thailand, where there are more Muslims than other part of the country. Food
and nutrition surveys (Nutrition Division ,2006) found the prevalence of anemia (hemoglobin
less than 120 g /L) in women aged 12 -14 years to be 17.2%, whereas in the southern it area
was up to 21%. Songkhla province is the province southern where population with Islamic
faith was 32.84% or 1/3 of the population (NSO, 2003). Muslims in the south prefer to send
their children to study in Islam private schools for learning and practicing the principles of
Islam and getting use to lifestyle of Islam in the future. Culture Muslims was different from
other religions, especially that related to consumption (Cheawnawin S., 2001). This may be
the factor that is associated with their high incidence of anemia. However, the literature
review showed very few studies about dietary consumption, dietary pattern or dietary
behavior associated health condition among Muslim in Thailand, especially adolescents.

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Therefore, the researcher is interested in studying dietary pattern and other factors which
might affect the occurrence of anemia among young female students in Islam private schools.

General Objective
To identify associations between dietary pattern and other lifestyle factors to anemia
status among female adolescents in Islam private schools.

Specific Objectives
1. To identify the prevalence of anemia among female adolescents in Islam private
schools.
2. To assess the dietary pattern related to anemia among female adolescents in Islam
private schools.
3. To assess factors (general characteristic, lifestyle and health behavior) influencing
anemic status among female adolescents in Islam private schools.

Materials and methods

Research design: the cross sectional study was carried out from Novamber to
Decamber 2009.
The study population was adolescent women who were students in Islam private
schools in the urban district of Songkhla province.
Sample consisted of secondary school girl, aged 13 15 years old, living in urban of
Songkhla province, south of Thailand. Inclusion of subjects was on voluntary basis;,
childrens parents or guardians were fully informed and prior to acceptance.
The 276 subjects were selected by simple random sampling from those who met the
inclusion criteria of this study.
Inclusion criteria were: studying in Islam private school for at least 1 term; 13 to 15
years of age; apparently healthy; no family history of genetic disorder such as thalassemia or
thalassemia trait, G6PD, etc.; no underlying chronic disease or chronic blood loss, such as
peptic ulcer, parasite infection, hemorrhoid, kidney disease, etc..
Instruments
The instruments 3 part self administered questionnaires: sociodemographic data,
dietary pattern and the semi quantitative food frequency (semi-FFQ) for collecting an
individuals habitual food intake during the past month.

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 Data collection
Researcher and co-researchers explained how to answer questionnaires and used food
model and photo of common Thai dishes of various portion to assess the type and amount of
foods and beverages consumed during the previous month. Subjects completed the
questionnaires without any time limitation, and were allowed to ask any questions.
Nutrition status assessment by measuring height and weighed. Students stand on the
middle of the plate of the digital computer barefooted and wear light clothing (participants
must remove the belt, bring out of pocket and wrapper out before weighting). Height was
measured by having participants standing in an upright position (occipital, both shoulders,
back side, haunch and both legs contact with a wall, eyes looking straight ahead with eyes
parallel with the floor level).
Blood samples were obtained for hematotological laboratory examination. A
professional nurse performed venipuncture for 2 ml blood. A EDTA-containing tube were
used for the collection of whole blood sample, which were analysed by Fully automatic blood
analyzer for the determination hemoglobin (Hgb) and hematocrit (Hct).
Data Analysis
The information of general characteristic (age, menstruation, nutrition status) and
dietary pattern of participants was analyzed for descriptive means, standard deviation,
frequency and percentage.
The nutrients related to anemia (iron, copper, zinc, folate, vitamin B12 and protein)
were derived primarily from Food Composition Tables standard reference, INMUCAL-N
program and USDA National Nutrient Database Standard Reference. Nutrients intake based
on the semi-FFQ was computed by multiplying the consumption frequency of each food by
the nutrients content of food.
The Pearson Chi-Square test was used to measure the association between variables.
Independent sample T-test was performed to compare the differences between groups. In all
analyses the level of statistical significance was set at p<0.05.
Anemia status was defined using the age and sex specific thresholds proposed by
UNICEF and the World Health Organization (INACG/WHO/UNICEF,1998): anemia was
defined as hematocrit < 36% and/or hemoglobin < 120 g/L; nonanemia as hematocrit 36%
and hemoglobin 120 g/L.
Protection of Human Rights
This study was approved ethically by the Human Right Committee at Mahidol
University. After the researcher explained the study objective of this study, the participant
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were entitled to have the right to accept or decline to participate in the study at anytime they
want. They were assured that the data would be treated with strict confidence and should be
reported as a group data.

Results
The characteristics of the subjects; the mean age was 14 0.77 years, 93.8% has
menstruation, mean age of menarche was 11 2.9 years with duration of 6.5 2 days and
volume estimated by self was moderate level (83.7%). Most students (92.8%) were classified
as having normal nutrition status, whereas the overweight and underweight were 3.3% and
4%, respectively. Most students (72.5%) lived with parents or guardians and 27.5% lived in
the school dormitory. 71.7% of students received money weekly at a mean cost was 79.9
27.8 baht per day which was accepted as enough for demand.
The prevalence of anemia (Hematocrit < 36% and/or Hemoglobin < 120 g/L) was
46.4% as presented in table 1.

Table1 Prevalence of nonanemic and anemic.

Anemic Status N (%)
Hematocrit 36% and Hemoglobin 120 g/L 148(53.6)
Hematocrit < 36% and/or Hemoglobin <120 g/L 128(46.4)

Dietary pattern show most students (62.2%) has 3 meals a day and 37.3% has 2 meals
a day, 35.9% has breakfast, 80.8% has lunch and 51.1% has dinner everyday. The dietary
intake of students was either from parents cooking or from food shops already cooked food.
Only 1.4% of in students did not eat beef and seafood. Most students (90.9%) ate fruits in
some meals. Popular beverage drink with a meal of students was water or sweetened juice,
cola beverage (6.2%), fruit juice (6.5%) and tea or coffee (4.7%), respectively. The
consideration or value of food choices of female adolescent in Islam private school was halal
(73.6%) and cleanness (46.4%), respectively. Stylishness was the last consideration of food
choices.
Frequency of consumption in the top five classified by 5 food groups as follow;
1. Flour, nut, seed products: Rice; Noodles; Bread; Instant noodle; and Glutanous rice
respectively.
2. Vegetable group: Swamp cabbage; Chinese white cabbage; Cabbage; Chinese
Kale; and Chinese cabbage respectively.

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 3. Fruit group: Oranges; Watermelon; Apple; Pie apple; and Guava respectively.
4. Meat product: Chicken; Eggs; Ball; Beef; and Mackerel respectively.
5. Milk product: Milk; Yoghurt drinking; and Yoghurt respectively.

Dietary intake of anemia related nutrients comparing with 2/3 or 67% Thai
Recommended Daily Intakes (Thai RDI) or Recommended Daily Allowance (RDA) for
population 13-15 years of age showed that most students had iron intake lower than
67%RDA and protein, copper, zinc, vitamin B 12, vitamin C and folate intake higher than
67%RDA (Table 2).

Table 2 The percentage of nutrients related anemia about consumed < 67% or 67% of Recommended
Daily Allowance (RDA).
Nutrients RDA 67%RDA <67%RDA 67%RDA
N (%) N (%)

Protein (g) 55 36.85 31(11.2) 245(88.8)

Iron (mg) 28.2 18.89 236(85.5) 40(14.5)
Copper (mg) 0.89 0.596 8(2.9) 268(97.1)
Zinc (mg) 7 4.69 34 (12.3) 242(87.6)
Vitamin B12 (mcg) 2.4 1.608 11(3.9) 265(96.0)
Vitamin C (mg) 65 43.55 30(10.8) 246(89.1)
Folate (mcg) 400 289 3(1.1) 273(98.9)

The demographic, dietary and lifestyle factors (age, menstruation, nutrition status,
address, cost, frequency of meals, fruits and beverages consumed with meal, health behavior
to prevent parasite infection, etc.) were not found to associate significantly with anemic status
of female adolescents in Islam private school (p > 0.05), the data of which were showed in
Table 3.

Table 3 Association between factors and anemia status.

Anemia status
Variables
Non anemia Anemia Total
148(100) 128(100) 276(100) p-value

Age 0.123
13 years 54(36.5) 34(26.6) 88(31.9)
14 years 59(39.9) 52(40.6) 111(40.2)
15 years 35(23.6) 42(32.8) 77(27.9)

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 Anemia status
Variables
Non anemia Anemia Total
148(100) 128(100) 276(100) p-value

Menstruation 0.148
Yes 136(91.9) 123(96.1) 259(93.9)
No 12(8.1) 5(3.9) 17(6.2)
Nutrition status 0.634
Overweight 6(4.1) 3(2.3) 9(3.3)
Normal 137(92.6) 119(93) 256(92.8)
Underweight 5(3.4) 6(4.7) 11(4)
Address 0.217
Parents 103(69.6) 97(75.8) 200(72.5)
Dormitory 45(30.4) 31(24.2) 76(27.5)
Cost 0.059
< 50 bath/day 13(8.8) 3(2.3) 16(5.8)
50100 bath/day 121(81.8) 115(89.8) 236(85.5)
>100 bath/day 14(148) 10(7.8) 24(8.7)
Meal 0.263
1 meal 2(1.4) 0(0) 2(0.7)
2 meals 59(39.9) 44(34.4) 103(37.3)
3 meals 87(59.2) 84(65.6) 171(62.2)
Breakfast 0.093
Every day 47(31.8) 52(40.6) 99(35.9)
Sometime 95(64.2) 75(58.6) 170(61.6)
Not 6(4.1) 1(0.8) 7(2.5)

Lunch 0.629
Every day 120(81.1) 103(80.5) 223(80.8)
Sometime 27(18.2) 25(19.5) 52(18.8)
Not 1(0.7) 0(0) 1(0.4)
Dinner 0.746
Every day 74(50) 67(52.3) 141(51.1)
Sometime 68(45.9) 54(42.2) 122(44.2)
Not 6(4.1) 7(5.5) 13(4.7)

Hands wash 0.538

Every time 39(26.4) 38(29.7) 77(27.9)
Sometime 109(73.6) 90(70.3) 199(72.1)
Wearing shoes 0.030
Every time 148(100) 124(96.9) 272(98.6)
Sometime 0(0) 4(3.1) 4(1.4)

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 Anemia status
Variables
Non anemia Anemia Total
148(100) 128(100) 276(100) p-value

Consumed antiparasites drug 0.278

Yes 9(6.1) 7(5.5) 16(5.7)
No 139(93.9) 121(94.6) 260(94.2)
Consumed fruit with meal 0.545
Every meal 4(2.7) 2(1.6) 6(2.2)
Sometime 132(89.2) 119(93) 251(90.9)
Not 12(8.1) 7(5.5) 19(6.9)
Beverages 0.270
Water or sweetened juice 116(78.4) 112(87.5) 228(82.6)
Cola beverage 10(6.8) 7(5.5) 17(6.2)
Fruit juice 12(8.1) 6(4.7) 18(6.5)
Tea or coffee 10(6.8) 3(2.3) 13(4.7)
Table 4 presents dietary intake by nutrients related to anemia and anemic status. The
data showed that nonanemic students consumed iron, copper and zinc higher than anemic
students (p<0.05). No other nutrients were found to be significantly different.

Table 4 Mean and comparisons of nutrients related anemia between nonanemia and anemia groups.
Total Nonanemia Anemia
Nutrients (n = 276) (n = 148) (n = 128) t

X SD X SD X SD
Protein (g) 66.39 25.7 68.4527.16 64.023.77 1.431
Iron (mg) 13.35 5.08 13.99 5.51 12.6 4.45 2.296*
Copper (mg) 1.3 0.49 1.370.55 1.23 0.42 2.278*
Zinc (mg) 7.78 2.85 8.17 3.08 7.332.5 2.470*
Vitamin B12 (mcg) 5.52 2.89 5.813.19 5.19 2.5 1.792
Vitamin C (mg) 128.58 84.33 133.6687.95 122.72 79.89 1.074
Folate (mcg) 1274.44 495.88 1296.0512.66 1249.51 476.54 0.776
*p<0.05
Discussion
Prevalence of anemia (Hematocrit < 36% and/or Hemoglobin < 120 g/L) among
female adolescent 13-15 years old was 46.4%. However, this prevalence was not exclusive of
thalassemia trait because those with thalassemia trait may or may not show symptom and sign
of anemia. The incidence of carriers or thalassemia and abnormal hemoglobin and diseases in
pregnant women of Songklanagarind Hospital, Songkhla province was 23% (Noparat C. et

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al.,1996) and prevalence of anemia (Hemoglobin < 110 g/L) among pregnant Muslims
women 27 6.3 years in Pattani province was 79.6% (Paimmongkol S. et al.,2006).Although,
not found studies among female adolescents in same area. However, data collection period of
this study was about 1.5-2 months after Ramadan fasting so that dietary pattern of students
during fast might lead to anemia. The results indicated that red blood cell production was
suppressed, as evidenced by lower levels of hemoglobin and red blood cell (RBC), in subjects
during the Ramadan period (Dewanti L. et al., 2006).
Dietary pattern showed that students had breakfast sometime (61.6%) which is
consistent with the study among students aged 15-19 years in the Department Home
Economics where students had breakfast sometimes and skip breakfast more often than other
meals (Mangkonpith A.,1999)
Means of anemia related nutrients showed that the nonanemic students consumed
iron, copper and zinc higher than anemic students. However, most students iron intake was
lower than 67%RDA in both groups which is consistent with the study among Thai-Muslim
pregnant woman in rural southern; iron intakes were lower than 50% of recommended
levels(Piammongkol S.,et al., 2004). This may caused by food sources that most students
consumed; chicken, balls and eggs more frequent than red meat and liver (good source of
heam iron bioavailability) and Halal food for Muslims, has low iron bioavailability. The
result of this study is consistent with the study among preschool children aged 1-4 years in
Krabi province; iron deficiency anemia was a critical problem in Ialamic families because
they consumed less meat, liver and blood (Sirirat S., 2006). Moreover, most students
consumed less green vegetable and fruits with meal (source of nonheam iron bioavialabilty
and vitamin C which enhances nonheam iron absorption, respectively). Few students drank
cola beverage, tea or coffee (source of inhibiting nonheam iron absorption).
However, Nutrient analysis did not include Halal food because Halal food, especially
meat and meat product must be slaughtered and cleaned follow the principles of Halal
(Wahab A.R., 2004) and some of Halal food was not included in Food Composition Tables
standard reference, INMUCAL-N program and USDA National Nutrient Database Standard
Reference. Therefore, nutrients intake may be lower or higher than the actual data. It is the
researchers opinion that iron intake should be lower than the actual data because Halal food
(meat and meat product) must be slaughtered and cleaned to assure maximum removal of
blood. Since blood is considered sewage in Islamic principles (The Halal Standard Institute of
Thailand., 2009).

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Suggestion
The schools should encourage students to cultivate and modify the behavior
consumption to the right pattern, particularly breakfast.
Most students iron intake was below 67% RDA. Therefore the director of school
must add knowledge of nutrition into the curriculum for increasing skills to choose food
sources with high iron bioavailability. He or she should scrutinize the quality and nutritional
value of foods sold in schools and school area, such as sausage, ball which were source of
protein that students have high consumption frequency.
The Public Health department should pay more interest to this because the prevalence
of anemia was relatively high. It is a problem that should be focused and corrected
immediately by giving iron tablet or finding the actual cause of the anemia, such as screening
parasite infection, ect..
There should be more of similar study among male students in the urban district as
well as both male and female student in the rural districts in the southernmost 5 province of
Thailand.

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