Clinical Nutrition ESPEN 44 (2021) 194e199

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Clinical Nutrition ESPEN

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Original article

Prevalence and determinants of anemia during the third trimester of

pregnancy
Mohamed Eweis a, Eman Z. Farid a, Nesreen El-Malky a, Mazen Abdel-Rasheed b, *,
Sondos Salem b, Sherwet Shawky a
a
Department of Obstetrics and Gynecology, Faculty of Medicine, Beni-Suef University, Egypt
b
Department of Reproductive Health Research, National Research Centre, Egypt

a r t i c l e i n f o s u m m a r y

Article history: Background: Anemia during pregnancy is a significant health problem. We aim to measure the preva-
Received 2 February 2021 lence of anemia in the third trimester of pregnancy in a specific geographical area and identify its risk
Accepted 24 June 2021 factors.
Methods: A cross-section study was conducted in the antenatal clinic at Beni-Suef University Hospital on
Keywords: 383 pregnant women in the third trimester of pregnancy. All enrolled women were interviewed about
Anemia
age, education, occupation, family income, vitamin intake, medical history, and nutritional history. A
Hemoglobin
blood sample was examined for hemoglobin concentration from each enrolled woman.
Third trimester
Pregnancy outcome
Results: The prevalence of anemia was 72%. Multiparity, infrequent antenatal visits, irregular intake of
iron supplements, low weekly intake of meat and fruits, and frequent daily tea consumption were
identified as risk factors for anemia. About 23.6% of the anemic women had small-for-gestational-age
fetuses (RR ¼ 25.2).
Conclusion: Anemia by the third trimester of pregnancy represents a major health problem in Beni-Suef,
Egypt.
© 2021 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights
reserved.

1. Introduction babies, resulting in the deaths of 115,000 women and 590,000

The World Health Organization defined anemia as the fall down
of hemoglobin level concentration of less than 11 g/dl [1]. The
severity of gestational anemia varies according to the hemoglobin
level. Accordingly, it is considered severe if the hemoglobin level is
less than 7 g/dl, moderate if hemoglobin level falls between 7 and
9.9 g/dl, and mild if hemoglobin level falls between 10 and 10.9 g/dl
[2]. Worldwide, anemia affects about 32.4 million pregnant
women. It is considered a severe public health problem, specifically
in South East Asia and Africa, as it affects 48.7% and 46.3% of
pregnant women there, respectively. Moreover, maternal mortality
is recorded in about 20% of pregnant women suffering from ane-
mia, whereas most are detected in developing countries [3].
It was declared that anemia during the childbearing period,
pregnancy, and giving birth is a global dilemma for mothers and
* Corresponding author. 33 El-Buhouth St, Dokki, Cairo, 12622, Egypt.
E-mail address: doctor_mazen@hotmail.com (M. Abdel-Rasheed).
babies yearly [4]. There are consequences of gestational anemia
that usually happen in developing countries, such as miscarriage,
small-for-gestational-age (SGA) fetuses, antepartum, intrapartum/
postpartum bleeding, delivery complications, preterm birth, low
birth weight (LBW) babies, stillbirths, and maternal mortality [5].
Many factors were determined in defining the causes of gesta-
tional anemia, such as nutritional deficiencies of iron, folate, and
vitamin B12. Other socio-economic factors as cultural and religious
food taboos also significantly contribute to decreased hemoglobin
level during pregnancy [6]. Studies reported that Iron deficiency
anemia is the most common cause of gestational anemia in many
developing countries [2].
According to the World Bank collection of development in-
dicators in 2016, the prevalence of anemia in Egypt during preg-
nancy was 22.6%, compiled from officially recognized sources [7]. In
this study, we tried to measure the prevalence of anemia in the
third trimester of pregnancy in Beni-Suef University Hospital as a
tertiary referral center and to identify the possible risk factors.

https://doi.org/10.1016/j.clnesp.2021.06.023
2405-4577/© 2021 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights reserved.
M. Eweis, E.Z. Farid, N. El-Malky et al.
2. Materials and methods
This cross-sectional study was conducted at Beni-Suef Univer-
sity Hospital on 383 pregnant women who attended the antenatal
care clinic during their third trimester from April to June 2019. The
Ethics Committee of the Faculty of Medicine at Beni-Suef University
approved the study protocol. The study included pregnant women
who attended the antenatal care clinic during their third trimester.
Women with chronic medical illness were excluded from the study.
All women enrolled in this study have given written informed
consent for participation in the study. The consent included the
study's aim, methods carried out in research, and the subject's right
to be withdrawn from research anytime.
A proper history was taken from each participant regarding age,
educational level, residency (urban or rural), occupation, family
income, frequency of antenatal visits, obstetric history, medical
history, and surgical history. Nutritional history is taken to detect
the frequency intake of meat/month, chicken/week, fish/week,
fruits/week, vegetables/week, and tea/day. History of iron supple-
ments intake was taken. All women were subjected to routine
antenatal care, including a physical examination (e.g., measuring
blood pressure), ultrasound, and umbilical artery Doppler exami-
nation. A blood sample was taken from each enrolled woman for
standard laboratory tests such as complete blood picture, blood
group, RH type, and blood sugar test if there is a risk. A urine sample
was taken for urine analysis. Blood from each participant was
drawn from the cubital vein into appropriate blood collection tubes
using vacuum tube needles (Becton Dickinson Medical Devices Co.
Ltd., Franklin Lakes, USA). K2EDTA tubes were used for CBC. Sam-
ples were transported and tested within 4 h after collection.
Measured CBC parameters included RBC, HGB, HCT, mean corpus-
cular volume (MCV), mean corpuscular hemoglobin (MCH), MCH
concentration (MCHC), platelet count (PLT), WBC, and WBC differ-
entials, including percentages and absolute counts of neutrophils
(NEUT% and NEUT), lymphocytes (LYM% and LYM), monocytes
(MONO% and MONO), basophils (BASO% and BASO), and eosino-
phils (EO% and EO).
According to WHO criteria, anemia was diagnosed with a he-
moglobin level of less than 11.0 g/dl. Anemia was further divided
into three degrees; mild with hemoglobin level 10e10.9 g/dl,
moderate with hemoglobin level 7e9.9 g/dl, and severe with he-
moglobin level <7.0 g/dl [1].
The sample size was estimated to be 380 subjects to detect the
prevalence of anemia in pregnant women during the third
trimester with confidence level 95% and power 80%. Data were
analyzed using Statistical Program for Social Sciences (SPSS v. 25
Inc., Chicago, USA). Categorical variables were presented as the
frequency with percentage. Chi-square test was used to compare
categorical variables and calculate the Odds ratio with a 95% con-
fidence interval for the different risk factors. P-values of 0.05 were
chosen as the level of statistical significance. A multivariate logistic
regression model was used to identify the independent risk factors
of anemia in pregnancy.
3. Results
The study included 383 pregnant women, whose mean age was
28.75 ± 6.19 years, with the first pregnancy at 21.56 ± 3.53 years. All
women's personal and family characteristics regarding residence,
education, occupation, family income, and parity were shown in
Fig. 1. Regarding the prevalence of anemia in the third trimester, 107
women (27.9%) were normal, 81 women (21.1%) had mild anemia,
148 women (39%) had moderate anemia, and 47 women (12%) had
severe anemia. Most of the anemic women (86.6%) were related to
iron deficiency. Although ultrasound revealed 19 women among
195
Clinical Nutrition ESPEN 44 (2021) 194e199
the anemic group (6.88%) and two women among the non-anemic
group (1.87%) had placenta previa with mild antepartum hemor-
rhage, there was no statistical significance difference between both
groups.
Regarding the personal risk factors for anemia, younger age at
first pregnancy “below 20 years” [OR ¼ 1.728], rural residence
[OR ¼ 2.254], low level of education [OR ¼ 4.818], non-working or
manual working [OR ¼ 6.277 & 6.122 respectively], and lower
family income/month [OR ¼ 8.533 for <500 EGP & 7.467 for
500e1000 EGP] were identified as risk factors by univariate anal-
ysis (Table 1).
Regarding risk factors related to the history of pregnancy, high
parity “more than 2” [OR ¼ 2.177], short interval between current
and last pregnancy “less than two years” [OR ¼ 1.949], hemorrhage
during pregnancy [OR ¼ 10.5], placenta previa [OR ¼ 10.277],
infrequent antenatal visits “less than 5” [OR ¼ 11.818], and irregular
intake of the iron supplement [OR ¼ 19.697] were also identified as
risk factors by univariate analysis. Dietary risk factors, including
deficient intake of meat, poultry, fish, vegetables, and fruits with
excess daily tea consumption, were significantly associated with
anemia (p-value <0.001) (Table 1).
Logistic regression revealed that the following factors were
found as independent risk factors for anemia in pregnancy: high
parity “more than 2”, infrequent antenatal visits “less than 5”,
irregular intake of iron supplement, deficient intake of meat and
fruits meat, and excess daily consumption of tea (Table 2).
By studying the umbilical artery Doppler, nine women among
the anemic group developed absent/reversed end-diastolic flow.
On the other hand, only one woman among the non-anemic group
was affected, which was not significant. Regarding the estimated
fetal weight, 65 pregnant women had SGA fetuses, and one woman
had a large-for-gestational-age (LGA) fetus among women of the
anemic group. On the other hand, only one woman among the non-
anemic group had an SGA fetus (RR for SGA ¼ 25.2, p-value <0.001)
(Table 3).
4. Discussion
Gestational anemia is considered a potentially reversible risk
factor that results in unfavorable consequences. Peripartum and
postpartum morbidity and mortality for both pregnant women and
their outcomes should be expected. This research assessed the
occurrence of maternal anemia, its determinants, and its perinatal
outcomes among pregnant women attending Beni-Suef University
Hospital, which serves a low socio-economic area with a low level
of education among most of its population.
The current study revealed that the prevalence of anemia in
pregnant women during their third trimester was 72%, divided into
mild 21%, moderate 39%, and severe anemia 12%. Our observation is
closely similar to the findings of another study conducted at “Kar-
mouz family health unit” in Alexandria, which showed a high
prevalence of anemia (73.8%) [8]. Previous studies were also con-
ducted in different governorates of Egypt. The prevalence of
maternal anemia is 67% at Fayoum governorate, 66% at Menofyia
governorate, and 55% in rural areas of Belbis district, Sharkia
governorate [9e11]. All previous figures were higher than the na-
tional prevalence of maternal anemia in Egypt in 2016 (23%) [7].
The possible justification is low compliance with iron supplemen-
tation, which might be explained by the low socio-economic con-
ditions and deficient health awareness.
Compared to other populations in Africa, a study conducted in a
tertiary referral hospital in Northern Ghana revealed that about half
of the women were anemic, and the rate increased through tri-
mesters [12]. Also, in low resources setting in South-Eastern Nigeria,
the prevalence of anemia was 58% [13]. While at St. Paul's Hospital
M. Eweis, E.Z. Farid, N. El-Malky et al.
Fig. 1. Personal and family characteristics of all study subjects.
Millennium Medical College, Addis Ababa, Ethiopia, the incidence of
anemia was 11.6% [14]. The differences between incidence rates in
African countries may be due to geographical variations, socio-
economic status, dietary habits, and food regimens in different
countries. The odds of anemia are higher in the third trimester. This
observation is possibly due to the increase of red cell mass and the
cumulative expansion of the placenta for fetal tissue growth,
together with consequences of delivery, mainly the expected blood
loss, which increases iron demands [15].
Similar to our findings regarding the personal risk factors it is
used to declare hazards of anemia on blood supply and the effect of
anemia on pregnancy outcome, the results of a study conducted in
Northwest Ethiopia revealed that the likelihood of anemia was
higher among pregnant women living in rural areas [OR ¼ 3.03, 95%
CI 1.17, 7.82], which recommended the improvement of the socio-
economic status [16]. Also, Elzeiny et al. recognized that 76.3% of
women with primary education were anemic. Besides, manual
work was the most encountered occupation among husbands of
studied women (31.8%), with 79.7% of them were anemic [8].
The present study revealed an increased risk of anemia for
pregnant women with age, similar to a multicenter retrospective
study previously conducted in China. They found that maternal
anemia was significantly associated with maternal age 35 years
[17]. On the contrary, the results of a study conducted in Warri,
South-Southern Nigeria, revealed a bipolar distribution of anemia
for women above 40 years and below 20 years [18]. These differ-
ences may be due to the different local economic development
levels, lifestyles, and dietary habits.
A Longitudinal Study in the Northwest of Ethiopia on the effect
of pregnancy on hemoglobin level revealed that the hemoglobin
level in the first pregnancy and subsequent pregnancies before
gestation were 12.41 g/dl and 10.78 g/dl, respectively. These levels
were decreased by multiparty multiple pregnancies, 0.16 g/dl [95%
CI: 0.07e0.24] [19]. In our study, a statistically significant associa-
tion was found between anemia and high parity “> 2” [OR ¼ 2.177]
as well as a short interval between pregnancies “< 2 years”
[OR ¼ 1.949].
In the current study, infrequent antenatal visits “less than 5”
[OR ¼ 11.818] and irregular intake of the iron supplement
[OR ¼ 19.697] were also identified as risk factors by univariate
analysis. It was observed that 97% of candidates who receive an
irregular supply of iron were anemic. These results were similar to a
retrospective study done in Turkey that declared that parity >3,
196
Clinical Nutrition ESPEN 44 (2021) 194e199
number of antenatal visits <5, and duration of iron supplementa-
tion <3 months could raise the prevalence of anemia during
pregnancy [20]. A study from rural Bihar in India also reported that
women were likely to take iron and folic acid regularly if they
received good nutritional counseling during their regular antenatal
visits [21]. This raises questions regarding the antenatal counseling
protocol followed, the visitors' compliance, and whether they took
the iron supplementations irregularly, in inadequate doses, or did
not take it at all.
The main obstacles to receive adequate supplements were
forgetfulness followed by cost and adverse effects, continuous
training of health care providers, traditional belief that the intake of
any gestational medication could have its consequences on the
outcome. Varghese et al. ensured a constant supply of iron and folic
acid in North India during pregnancy [22]. WHO program recom-
mended iron supplementation during gestation, starting from the
second trimester that continues until delivery [23].
The current study observed that the dietary risk factors for
gestational anemia were inadequate intake of meat, poultry, fish,
vegetables, and fruits with excess daily tea consumption. A survey
performed in Poland to ensure dietary behavior related to the
quality and quantity of food per day, and they recommended con-
sumption of meat with poultry preference [24]. Another study in
Hodeida Province, Yemen, confirmed that the infrequent con-
sumption of vegetables/fruits, meat, fish, and chicken with tea
drinking showed a significant role in provoking iron deficiency
anemia [25]. This was justified as dietary regimens, including meat,
poultry, and fish rich in hemoglobin and myoglobin, are the pri-
mary sources of heme iron, whereas cereals, pulses, legumes, fruits,
and vegetables are sources of nonheme iron. Meat is a good source
of heme iron as well as high biological value protein. The absorption
of iron is enhanced by fruits rich in ascorbic acid [26].
Consequences and adverse effects of anemia on perinatal out-
comes were observed in the current study. A significant correlation
between gestational anemia and SGA was found as 23.5% of anemic
mothers (65 cases) had SGA fetuses. In contrast, among the non-
anemic mothers, only one woman had an SGA fetus. Similar re-
sults were observed in a cross-sectional study from Jharkhand, In-
dia, which stated that a low hemoglobin level during pregnancy
usually ended with LBW babies [27]. In Kayseri, Turkey, a study
revealed severe and moderate iron deficiency anemia in the last
trimester resulted in SGA fetuses [28]. Cochrane Pregnancy and
Childbirth's Trials Register, ClinicalTrials.gov, the WHO International
M. Eweis, E.Z. Farid, N. El-Malky et al. Clinical Nutrition ESPEN 44 (2021) 194e199

Table 1
Personal, pregnancy-related, and dietary risk factors for anemia.

Anemia No Anemia P-Value OR (95% CI)

Age
20 21 (48.8%) 22 (51.2%) <0.001 N/A
20e25 53 (60.9%) 34 (39.1%)
25e30 82 (82.8%) 17 (17.2%)
30e35 79 (79.8%) 20 (20.2%)
35e40 34 (72.3%) 13 (27.7%)
>40 7 (87.5%) 1 (12.5%)
Age of First Pregnancy
20 126 (78.3%) 35 (21.7%) 0.021 1.728 (1.082e2.760)
>20 150 (67.6%) 72 (32.4%) 1
Residence
Rural 161 (79.7%) 41 (20.3%) <0.001 2.254 (1.426e3.561)
Urban 115 (63.5%) 66 (36.5%) 1
Education
Illiterate/Read & Write 157 (87.2%) 23 (12.8%) <0.001 4.818 (2.867e8.098)
School/University 119 (58.6%) 84 (41.4%) 1
Occupation
Not Working 249 (74.6%) 85 (25.4%) <0.001 6.277 (2.476e15.915)
Manual Working 20 (74.1%) 7 (25.9%) 6.122 (1.766e21.227)
Employee 7 (31.8%) 15 (68.2%) 1
Family Income/month (In Egyptian Pound)
<500 42 (85.7%) 7 (14.3%) <0.001 8.533 (3.517e20.705)
500e1000 189 (84%) 36 (16%) 7.467 (4.430e12.584)
1000 45 (41.3%) 64 (58.7%) 1
Parity
>2 188 (78%) 53 (22%) <0.001* 2.177 (1.380e3.433)
2 88 (62%) 54 (38%) 1
The interval between Current and Last Pregnancy
2 Years 89 (84%) 17 (16%) 0.030* 1.949 (1.059e3.588)
>2 Years 137 (72.9%) 51 (27.1%) 1
History of Mode of Delivery
Cesarean section 157 (80.1%) 39 (19.9%) 0.63 1.692 (0.969e2.955)
Normal vaginal delivery 69 (70.4%) 29 (29.6%) 1
Hemorrhage during Pregnancy
Yes 46 (95.8%) 2 (4.2%) <0.001* 10.500 (2.502e44.071)
No 230 (68.7%) 105 (31.3%) 1
Placental insertion
Placenta Previa 45 (95.7%) 2 (4.3%) <0.001* 10.227 (2.435e42.953)
Normal Insertion 231 (68.8%) 105 (31.2%) 1
Frequency of Antenatal Visits
<5 Visits 208 (90.4%) 22 (9.6%) <0.001* 11.818 (6.867e20.340)
5 Visits 68 (44.4%) 85 (55.6%) 1
Regular Intake of Iron
Irregular Iron intake 100 (97.1%) 3 (2.9%) <0.001* 19.697 (6.090e63.703)
Regular Iron intake 176 (62.9%) 104 (37.1%) 1
Meat/Month
0e1 273 (80.1%) 68 (19.9%) <0.001* 52.191 (15.657e173.974)
>1 3 (7.1%) 39 (92.9%) 1
Chicken/Week
0e1 65 (97%) 2 (3%) <0.001* 16.173 (3.884e67.341)
>1 211 (66.8%) 105 (33.2%) 1
Fish/Week
0e1 275 (72.6%) 104 (27.4%) 0.035* 7.933 (0.816e77.125)
>1 1 (25%) 3 (75%) 1
Fruits/Week
<4 272 (75.8%) 87 (24.2%) <0.001* 15.632 (5.202e46.978)
4 4 (16.7%) 20 (83.3%) 1
Vegetables/Week
<4 265 (80%) 66 (20%) <0.001* 14.966 (7.299e30.687)
4 11 (21.2%) 41 (78.8%) 1
Tea/Day
>1 272 (87.2%) 40 (12.8%) <0.001* 113.9 (39.381e329.425)
0e1 4 (5.6%) 67 (94.4%) 1

Categorical variables are represented as a number (%), and Pearson Chi-square test was used.
*: Statistically significant (p-value <0.05).

Clinical Trials Registry Platform (ICTRP), and reference lists of
retrieved studies recommended multiple-micronutrient (MMN)
supplementation would prevent and decrease the occurrence of
LBW, and a reduction in babies considered SGA. These recommen-
dations could be taken as guidelines for women seeking pregnancy
197
to add iron and folic acid supplements and MMN supplements,
especially those residing in low- and middle-income countries [29].
Pathological changes resulting from gestational anemia cause a
reduction of the fetus's oxygen and modification in fetal blood flow
[30]. There are no statistically significant differences observed in
M. Eweis, E.Z. Farid, N. El-Malky et al. Clinical Nutrition ESPEN 44 (2021) 194e199

Table 2
Independent risk factors for anemia in the study group.

Risk factors В P-Value OR (95% CI)

Parity > 2 0.825 0.025* 5.13 (1.201e6.977)

Antenatal Visits (<5) 0.969 0.009* 1.81 (1.134e2.33)
Meat (Less than Once/Week) 0.813 0.013* 2.19 (1.65e3.97)
Tea (More than Once/Day) 1.03 0.005* 1.54 (1.043e2.235)
Fruits (Less than 4 Times/Week) 0.973 0.049* 1.63 (1.202e4.979)
Irregular Iron Supplement Intake 0.791 0.037* 1.57 (1.22e3.114)

A multivariate logistic regression model was used.

*: Statistically significant (p-value <0.05).

Table 3
Effect of anemia on fetuses.

Anemia No Anemia P-Value RR (95% CI)

No. (%) No. (%)

Estimated fetal weight

SGA 65 (23.6%) 1 (0.9%) <0.001* 25.199 (3.449e184.117)
Non SGA 211 (76.4%) 106 (99.1%) 1
Umbilical artery diastolic flow
Absent/reversed end diastolic flow 9 (3.3%) 1 (0.9%) 0.2 3.489 (0.437e27.879)
Normal end diastolic flow 267 (96.7%) 106 (99.1%) 1

Categorical variables are represented as a number (%), and Pearson Chi-square test was used.
*: Statistically significant (p-value <0.05).

the current study regarding umbilical artery Doppler between
anemic and non-anemic women, consistent with the results ob-
tained by Agbaje et al. [31]. Also, the mode of delivery and gesta-
tional anemia showed no significant difference. Researchers at
Karmouz Family Health Unit in Alexandria ended with the same
results [8]. These results were against those obtained by Drukker
et al., who stated that CS is the recommended mode of delivery
whenever gestational anemia present at the time of birth [32].
Most of the anemic women (86.6%) were related to iron defi-
ciency. Although there was an increased incidence of antepartum
hemorrhage due to placenta previa among the anemic group in the
current study, it was statistically insignificant. However, a retro-
spective cohort study conducted in British Columbia detected
placenta previa insertion was higher among women manifested
with gestational anemic who received intrapartum/postpartum
blood transfusion more than non-anemic women [33]. Similarly,
Yılmaz et al. found that anemia raises the incidence of gestational
bleeding [34]. A possible explanation is that gestational anemia is
associated with uterine atony due to impairment of oxygen and
hemoglobin to the uterus.
The limitations of our study included that we excluded women
with chronic medical illness from the study. As a result, we could
not assess hemoglobinopathies, chronic inflammatory diseases,
and folic acid deficiency as causative factors for anemia during
pregnancy. Besides, we did not check for serum ferritin levels that
could help in diagnosing anemia. Limitations also included difficult
follow-up of pregnant women diagnosed with anemia and a short
time to compensate for anemia.
In Egypt, efforts were made to diminish and cut down the
prevalence of gestational anemia in the form of encouraging reg-
ular antenatal care visits, adequate dietary intake, iron, and MMN
supplementation. However, several pitfalls were recognized, such
as poverty, ignorance, malnutrition, unemployment, over-
population, and remote antenatal care services destination, which
complicates this dilemma. This research was done at Beni-Suef
University Hospital, which serves a low socio-economic area with
a low educational level among most of its population. The main-
stream was anemic, so the prevalence of anemia was higher than
198
expected. Moreover, some cases were lost during follow-up. It is
recommended to enforce proper prenatal care and education from
medical professionals to improve both mother and fetus's health
during pregnancy. The use of health educational aids (posters or
photos) during antenatal visits would raise women's awareness
about the complications of maternal anemia and the importance of
compliance with iron supplementation during pregnancy.
5. Conclusion
Anemia by the third trimester of pregnancy represents a sig-
nificant health problem in this geographical area of Egypt. Among
many risk factors studied, multiparity, infrequent antenatal visits,
irregular intake of iron supplements, low weekly intake of proteins
and vitamins. Apart from the maternal consequences of anemia,
possible perinatal implications could result in SGA fetuses.
Funding
This research did not receive any specific grant from any funding
agency in the public, commercial, or not-for-profit sectors.
Ethical approval
This study was approved by the Ethical Committee of the Faculty
of Medicine, Beni-Suef University. All mothers participated volun-
tarily; privacy and confidentiality of data were assured all through
the research work. Informed consent was taken from them.
Declaration of competing interest
None of the authors has a financial or any conflict of interest.
Acknowledgments
We would like to thank our colleagues from the Faculty of
Medicine, Beni-Suef University, who provided insight and expertise
that greatly assisted our research.
M. Eweis, E.Z. Farid, N. El-Malky et al. Clinical Nutrition ESPEN 44 (2021) 194e199

References [18] Omote V, Ukwamedua HA, Bini N, Kashibu E, Ubandoma JR, Ranyang A.
Prevalence, severity, and correlates of anaemia in pregnancy among antenatal
attendees in Warri, South-Southern Nigeria: a cross-sectional and hospital-
[1] World Health Organization. The global prevalence of anaemia in 2011. World
based study. Anemia 2020:2020.
Health Organization; 2015.
[19] Feleke BE, Feleke TE. The effect of pregnancy in the hemoglobin concentration
[2] Obai G, Odongo P, Wanyama R. Prevalence of anaemia and associated risk
of pregnant women: a longitudinal study. J Pregnancy 2020:2020.
factors among pregnant women attending antenatal care in Gulu and Hoima

lu M, et al. Prevalence and
[20] Taner CE, Ekin A, Solmaz U, Gezer C, Çetin B, Keleşog
Regional Hospitals in Uganda: a cross sectional study. BMC Pregnancy
risk factors of anemia among pregnant women attending a high-volume
Childbirth 2016;16:76.
tertiary care center for delivery. J Turk Ger Gynecol Assoc 2015;16:231.
[3] Kefiyalew F, Zemene E, Asres Y, Gedefaw L. Anemia among pregnant women
[21] Wendt A, Stephenson R, Young M, Webb-Girard A, Hogue C, Ramakrishnan U,
in Southeast Ethiopia: prevalence, severity and associated risk factors. BMC
et al. Individual and facility-level determinants of iron and folic acid receipt
Res Notes 2014;7:771.
and adequate consumption among pregnant women in rural Bihar, India. PLoS
[4] Feleke BE, Feleke TE. Pregnant mothers are more anemic than lactating
One 2015;10:e0120404.
mothers, a comparative cross-sectional study, Bahir Dar, Ethiopia. BMC
[22] Varghese JS, Swaminathan S, Kurpad AV, Thomas T. Demand and supply
Hematol 2018;18:2.
factors of iron-folic acid supplementation and its association with anaemia in
[5] Figueiredo AC, Gomes-Filho IS, Silva RB, Pereira PP, Da Mata FA, Lyrio AO, et al.
North Indian pregnant women. PLoS One 2019;14:e0210634.
Maternal anemia and low birth weight: a systematic review and meta-anal-
[23] World Health Organization. Guideline: daily iron and folic acid supplemen-
ysis. Nutrients 2018;10:601.
tation in pregnant women. World Health Organization; 2012.
[6] Dattijo L, Daru P, Umar N. Anaemia in pregnancy: prevalence and associated
[24] FAO, OMS. Food based approaches to meeting vitamin and mineral needs.
factors in Azare, North-East Nigeria. Int J Trop Dis Health 2016;11:1e9.
Hum Vitam Miner Requir 2001:7e25. FAO (Organizacion de las Naciones
[7] The World Bank. Prevalence of anemia among pregnant women. World Bank
Unidas para la Agricultura y la Alimentacion).
Data; 2016. https://data.worldbank.org/indicator/SH.PRG.ANEM. [Accessed 15
[25] Misan N, Paczkowska K, Szmyt M, Kapska K, Tomczak L, Bre˛ borowicz GH, et al.
July 2020].
Nutritional behavior in pregnancy. Ginekol Pol 2019;90:527e33.
[8] Elzeiny N, Sultan EA, Shetya HY. Perinatal outcomes of maternal anemia in
[26] Al-Alimi AA, Bashanfer S, Morish MA. Prevalence of iron deficiency anemia
Alexandria, Egypt. J High Inst Public Health 2019;49:117e24.
among university students in Hodeida province, Yemen. Anemia
[9] El Ashiry A, El Ghazali S, Habil I. Prevalence and determinants of anaemia in
2018;2018.
third trimester pregnancy in Fayoum governorate-Egypt. Acta Med Mediterr
[27] Kumari S, Garg N, Kumar A, Guru PKI, Ansari S, Anwar S, et al. Maternal and
2014;30:1045e51.
severe anaemia in delivering women is associated with risk of preterm and
[10] Gadallah M, Rady M, Salem B, Aly EM, Anwer W. The effect of nutritional
low birth weight: a cross sectional study from Jharkhand, India. One Health
intervention program on the prevalence of anemia among pregnant women
2019;8:100098.
in rural areas of Belbis district-Sharkia Governorate-Egypt. J Egypt Publ Health
[28] Col Madendag I, Eraslan Sahin M, Madendag Y, Sahin E, Demir MB, Acmaz B,
Assoc 2002;77:261e73.
et al. The effect of iron deficiency anemia early in the third trimester on small
[11] Fahmy K, Farahat M, El Jilany A, Helmy M. The effect of iron deficiency anemia
for gestational age and birth weight: a retrospective cohort study on iron
on pregnancy outcome. 2013.
deficiency anemia and fetal weight. BioMed Res Int 2019;2019.
[12] Wemakor A. Prevalence and determinants of anaemia in pregnant women
[29] Keats EC, Haider BA, Tam E, Bhutta ZA. Multiple-micronutrient supplemen-
receiving antenatal care at a tertiary referral hospital in Northern Ghana. BMC
tation for women during pregnancy. Cochrane Database Syst Rev 2019.
Pregnancy Childbirth 2019;19:495.
https://doi.org/10.1002/14651858.CD004905.pub6.
[13] Onoh R, Lawani O, Ezeonu P, Nkwo P, Onoh T, Ajah L. Predictors of anemia in
[30] Gandhi K, Mehta AV. Role of Doppler Velocimetry in growth restricted fetuses.
pregnancy among pregnant women accessing antenatal care in a poor
NHL J Med Sci 2015;4.
resource setting in South Eastern Nigeria. Sahel Med J 2015;18:182.
[31] Agbaje OA, Adeyomoye AAO, Omidiji OAT, Oboke OS, Afolabi BB. Evaluation of
[14] Gebreweld A, Bekele D, Tsegaye A. Hematological profile of pregnant women
umbilical artery Doppler indices in pregnant women with sickle cell anemia
at St. Paul's hospital Millennium medical College, Addis Ababa, Ethiopia. BMC
disease at a Nigerian tertiary hospital. J Diagn Med Sonogr 2018;34:466e78.
Hematol 2018;18:15.
[32] Drukker L, Hants Y, Farkash R, Samueloff A, Granovsky SG. 626: gestational
[15] Scholl TO. Maternal iron status: relation to fetal growth, length of gestation,
anemia is an independent risk factor for cesarean delivery and adverse
and iron endowment of the neonate. Nutr Rev 2011;69:S23e9.
perinatal outcome. Am J Obstet Gynecol 2014;210:S306e7.
[16] Derso T, Abera Z, Tariku A. Magnitude and associated factors of anemia among
[33] Smith C, Teng F, Branch E, Chu S, Joseph K. Maternal and perinatal morbidity
pregnant women in Dera District: a cross-sectional study in northwest
and mortality associated with anemia in pregnancy. Obstet Gynecol
Ethiopia. BMC Res Notes 2017;10:359.
2019;134:1234.
[17] Lin L, Wei Y, Zhu W, Wang C, Su R, Feng H, et al. Prevalence, risk factors and
[34] Yilmaz E, Işitan OY, Soysal Ç, Yilmaz ZV, Kara OF, Küçüko€ zkan T. The influence
associated adverse pregnancy outcomes of anaemia in Chinese pregnant
of anemia on maternal and neonatal outcomes in adolescent pregnant. J Surg
women: a multicentre retrospective study. BMC Pregnancy Childbirth
Med 2018;2:69e73.
2018;18:111.

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