European Journal of Internal Medicine 23 (2012) 529–533

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European Journal of Internal Medicine

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Original article

Anemia—prevalence and risk factors in pregnancy

Gabriela Bencaiova ⁎, Tilo Burkhardt, Christian Breymann
Department of Obstetrics and Gynecology, Feto Maternal Hematology Group, University Hospital of Zurich, Switzerland

a r t i c l e i n f o a b s t r a c t

Article history: Background: To assess the prevalence of decreased iron stores and anemia in pregnant women. To determine
Received 4 August 2011 whether the risk factors: socio-demographic background, age, BMI, and parity are associated with abnormal
Received in revised form 11 April 2012 hemoglobin concentrations and/or abnormal iron status.
Accepted 11 April 2012 Methods: A longitudinal study was carried out at the Department of Obstetrics, University Hospital of Zurich
Available online 4 May 2012
to establish the risk factors and prevalence of the decreased iron stores and anemia in early pregnancy. In
order to determine the hematological parameters and ferritin levels, venous blood samples of 470 singleton
Keywords:
Anemia
pregnancies between 16 and 20 pregnancy weeks were collected. According to hemoglobin and iron status,
Iron depletion the patients were divided into four groups: patients with iron deficiency anemia, patients with decreased
Pregnancy iron stores, patients with anemia for other reasons and normal patients. The determinants socio-
Prevalence demographic background, age, BMI and parity were explored using multiple logistic regression analysis.
Risk factor Results: The prevalence of decreased iron stores (ferritin b 20 μg/l) was observed in 31.8% of subjects (149/
470) and anemia (Hb b 110 g/l) in 18.5% (87/470). The prevalence of iron deficiency anemia was higher
among women coming from former Yugoslavia and developing countries (p = 0.004 and p = 0.012). In pa-
tients coming from developing countries, a significant increase of anemia for other reasons was observed
(p = 0.027) and in patients older than 30 years, a significant increase of decreased iron stores (p = 0.018).
Conclusions: In our study population with low parity, the prevalence of abnormal hemoglobin and abnormal
iron status was 50.2% (236/470), and socio-demographic background was the most important risk factor of
anemia.
© 2012 European Federation of Internal Medicine. Published by Elsevier B.V. All rights reserved.

1. Introduction
Decreased iron stores and anemia affect a large proportion of the
population in developing and industrialised countries, particularly
risk groups like children, menstruating women and pregnant
women. During pregnancy there is a significant increase in the
amount of iron required to increase the red cell mass, expand the
plasma volume and to allow for the growth of the feto-placental
unit. In pregnant women not given supplementary iron, the hemoglo-
bin concentration (Hb) of the maternal blood falls from a non-
pregnant average of about 133 g/l to an average of about 110 g/l at
36 weeks [1]. The fall is steepest up to 20 weeks of gestation; the con-
centration remains fairly constant up to 30 weeks and then rises
slightly thereafter [2]. Thus, any estimation of hemoglobin concentra-
tion taken after the 20th week of gestation will be reasonably repre-
sentative of the fall induced by pregnancy. It is becoming clear that
the best time to detect any perinatal risk associated with maternal
anemia may be up until 20 weeks of gestation [3].
⁎ Corresponding author at: Department of Obstetrics, University Hospital of Zurich,
Frauenklinikstr. 10, CH-8091 Zurich, Switzerland. Tel.: + 41 44 255 5131; fax: + 41
44 255 4430.
E-mail address: benca@bluewin.ch (G. Bencaiova).
The prevalence of iron deficiency anemia (IDA) varies with age,
gender and socio-demographic background. About 6–30% of women
suffer from iron deficiency anemia during pregnancy. Previous stud-
ies showed that the risk of IDA is also increased with parity; nearly
three-fold higher for women with 2–3 children and four-fold greater
for women with 4 or more children [4–7]. On the other hand, in the
study by Idowu et al. anemia were more prevalent among primigravi-
dae than the multigravidae (p > 0.05) [8]. In other studies the risk of
anemia was increased in African-American and poor women
[5,9,10]. However, Deegan et al. demonstrated that total dietary iron
intake and lifestyle determinants make no significant impact on iron
status [11]. In the study by Charles et al. body mass index (BMI),
mid-upper arm circumference, and the number of antenatal care
visits showed a statistically significant association with anemia [12].
Al-Mehaisen et al. showed that gestational age, BMI, history of previ-
ous surgery, and multivitamin intake during pregnancy were signifi-
cantly associated with anemia [13]. The major determinants
identified for anemia in Ethiopia are chronic illnesses, deficiency of
iron and deficiency of folic acid [14,15].
There is evidence that an absence of iron stores has adverse conse-
quences on feto-placental development [16]. A reduction in body iron
is associated with a decrease in the level of functional compounds
such as hemoglobin. There is little doubt that iron supplementation
during pregnancy improves maternal iron and hematological status

0953-6205/$ – see front matter © 2012 European Federation of Internal Medicine. Published by Elsevier B.V. All rights reserved.
doi:10.1016/j.ejim.2012.04.008
530 G. Bencaiova et al. / European Journal of Internal Medicine 23 (2012) 529–533

in pregnancy and postpartum [17,18]. Perinatal and maternal mortal- chemiluminescence-immunoassay (ACS 190; Ciba/Corning Diagnos-
ity is substantially higher in anemic pregnant women, especially if tic Corp., Cleveland, OH).
their anemia is severe, but it can also occur in cases of moderate ane-
mia. Several studies have also described a positive correlation be-
2.4. Risk factors
tween maternal hemoglobin levels early in pregnancy and birth
weight, Apgar score and duration of pregnancy [17–19].
Multivariate logistic regression analysis was performed to identify
In the present study, the prevalence of decreased iron status, iron
potential risk factors for anemia and decreased iron stores such as low
deficiency anemia and anemia for other reason in 470 singleton preg-
maternal age, low BMI, high parity and socio-demographic back-
nancies between 16 and 20 weeks of gestation was determined. The
ground (origin, level of education and religion of the pregnant
independent risk determinants for anemia; socio-demographic back-
women). Odds ratios (OR) with 95% confidence intervals (CI) were
ground, parity, body mass index (BMI) and age were investigated
calculated. Maternal underweight was defined as BMI ≤ 18.5 kg/m 2
using multiple logistic regression analysis.
[23]. Statistical analysis was performed with Intercooled Stata® 8.2
for Windows (www.stata.com). Demographic characteristics were
2. Methods expressed as means (± standard deviation) and range. p Value was
based on the Fisher's exact test for categoric variables and the Stu-
2.1. Study population dent's t test for continuous variables. All statistical tests were evaluat-
ed at the .05 significance level.
In 2006, 470 pregnant women were prospectively observed at the
Department of Obstetrics, University Hospital of Zurich. Venous blood
samples were taken for determination of hematological status and 3. Results
ferritin level between 16 and 20 weeks and for hemoglobin concen-
tration before delivery. The patients were asked for their consent to The demographic characteristics are shown in Table 1. A low level
participate in our study and the informed consent was obtained be- of education was observed in 81.1% (381/470). There was a significant
fore study enrolment. The study was approved by the hospital's Ethics difference in the level of higher education (secondary/technical or
Committee. All patients presented were singleton pregnancies. Exclu- University) between patients from Europe + North America and Yu-
sion criteria were; chronic renal disease, malignancies and having had goslavia (17.3% (27/156) vs. 2% (3/147; p = 0.001); and between pa-
a blood transfusion at least 3 months before enrolment in the study. tients from Europe + North America and developing countries (17.3%
Routine iron supplementation contained in vitamins was started in (27/156) vs. 1.8% (3/167; p = 0.001).
the first trimester. Patients with IDA received 80 mg/day of oral fer- The mean hemoglobin concentration at the baseline was 118 ±
rous sulphate (Gyno-Tardyferon®, Robapharm). 9 g/l and the median of serum ferritin was 34 μg/l (2–212 μg/l). Out
of 470 patients in the study, 49.8% (234/470) had normal hemoglobin
and normal ferritin concentration. The mean RBC was 3.99 ± 0.4
2.2. Study criteria x10 6/μl, HCT 34.1 ± 2.7%, MCV 85.5 ± 5.5 fl, MCH 29.5 ± 2.2 pg, RDW
13.5 ± 1.0%, CHr 32.1 ± 2.4 pg, microcytic erythrocytes (MRC) 2.0 ±
According to current guidelines based on recommendations of the 5.1%, and hypochromic erythrocytes (HRC) 0.8 ± 1.8%.
CDC, anemia in pregnancy is defined by a hemoglobin value less than
110 g/l in both the first and third trimester, and less than 105 g/l in
the second trimester [20]. Since we saw high intra-individual varia- Table 1
tions between 105 and 110 g/l, we chose Hb b110 g/l as the cut-off. Demographic characteristics. Data expressed as mean ± s.d. (range) or n (%).
Sufficient iron stores are defined as a serum ferritin >50 μg/l [3]. Se-
Maternal age (years) 29.2 ± 5.9 (16.1-43.3)
vere iron depletion was defined as a serum ferritin ≤15 μg/l and Gravidity (n) 2.3 ± 1.6 (1–14)
iron depletion as a serum ferritin b20 μg/l [21,22]. Anemia for other Parity (n) 1.8 ± 1.0 (1–6)
reason was defined as Hb b110 g/l and ferritin ≥20 μg/l. The category Gestational age at enrolment (week) 16 ± 3 (16–20)
anemia for other reason included the following; thalassemia and he- BMI (kg/m2) 23.9 ± 5.3 (15.4-50.9)
Origin of mother (%)
moglobinopathies, vitamin B12 deficiency anemia, folic acid deficien- Europe + North America 156/470 (33.2)
cy anemia, chronic inflammatory diseases (particularly HIV positive Former Yugoslavia 147/470 (31.3)
patients) etc. Developing countries 167/470 (35.5)
The patients were divided according to hemoglobin concentration Africa 30/470 (6.4)
Asia 61/470 (12.9)
and ferritin levels into patients with iron deficiency anemia (Hb
Middle East 46/470 (9.8)
b110 g/l and ferritin ≤15 μg/l) (Group 1), patients with decreased South America 30/470 (6.4)
iron stores without anemia (Hb ≥110 g/l and ferritin b20 μg/l) Education
(Group 2), patients with anemia for other reason (Hb b110 g/l and None or primary 381/470 (81.1)
ferritin ≥20 μg/l) (Group 3) and patients with normal status (Group Europe + North America 91/156
Former Yugoslavia 140/147
4). Decreased iron stores were further divided iron depletion and se- Developing countries 150/167
vere iron depletion. Secondary/ technical 18/470 (3.8)
Europe + North America 13/156
Former Yugoslavia 2/147
2.3. Laboratory assessment Developing Countries 3/167
University degree 15/470 (3.2)
Blood samples were collected by veinpuncture. Hb, red blood Europe + North America 14/156
cells (RBC), hematocrit (HCT), mean corpuscular volume (MCV), Former Yugoslavia 1/147
Missing value 56/470 (11.9)
percentage of red cells—microcytic, macrocytic, hypochromic and
Religion
hyperchromic erythrocytes, hemoglobin content of reticulocytes Muslim 152/470 (32.3)
(CHr) and red blood cell distribution width (RDW) were measured Christian 160/470 (34.1)
using an ADVIA® hematology analyser system (Bayer Diagnostics, Hindu 55/470 (11.7)
Undenominational 42/470 (8.9)
Leverkusen, Germany). Mean corpuscular hemoglobin (MCH) was
Missing value 61/470 (13.0)
automatically calculated from Hb and RBC. Ferritin was assessed by
 G. Bencaiova et al. / European Journal of Internal Medicine 23 (2012) 529–533 531

Table 2 There was a significant difference in IDA between patients from

Prevalence of IDA, decreased iron stores and anemia for other reason according to age, industrialised and developing countries (1.3% (2/157) vs. 7.7% (13/
parity and demographic background (%).
168); p = 0.006) as well as between pregnant women from indus-
Group 1 Group 2 Group 3 Group 4 All patients trialised countries and pregnant immigrants from former Yugosla-
Pregnant 29/470 149/470 58/470 234/470 470 via (1.3% (2/157) vs. 9.7% (14/145); p = 0.001) (Table 2).
women (6.2) (31.7) (12.3) (49.8) (100.0) Maternal age (women older than 30 years) and parity (women
Maternal with two or three children) were independent risk factors for de-
age
creased iron stores (Table 3). The logistic regression analysis
(years)
b 20 0/19 5/19 4/19 10/19 19/470 showed that being underweight was not a risk factor for anemia
(0) (26.3) (21.1) (52.6) (4.0) or decreased iron stores, and that parity was not a risk factor for
20–30 17/254 93/254 32/254 112/254 254/470 anemia for other reason. Origin of mother from former Yugoslavia
(6.7) (36.6) (12.6) (44.1) (54.1) was the highest risk factor for iron deficiency anemia OR 8.3 (1.9-
> 30 12/197 51/197 22/197 112/197 197/470
37.1, 95% CI) (Table 3).
(6.1) (25.9) (11.2) (56.9) (41.9)
Parity At the delivery, there were 382 patients for the statistical analysis;
=1 12/230 62/230 30/230 126/230 230/470 88 cases were excluded due to incomplete data. The mean hemoglo-
(5.2) (27.0) (13.0) (54.8) (48.9) bin level before delivery was 121 ± 12 g/l (79–154). The prevalence
2–3 13/212 79/212 24/212 96/212 212/470
of anemia before delivery was 9.7%; namely mild anemia in 8.8%
(6.1) (37.3) (11.3) (45.3) (45.1)
>4 4/28 8/28 4/28 12/28 28/470 and moderate anemia in 0.9% (Hb b90 g/l). The mean gestational
(14.3) (28.5) (14.3) (42.9) (6.0) age at delivery was 38.7 ± 2.9 weeks (25–42) and birth weight
Origin of 3320 ± 646 g (730–5250). Preterm delivery was observed in 7.6%
mother (%) (29/382), low birth weight in 8.1% (31/382) and perinatal mortality
Europe + North 2/157 49/157 13/157 93/157 157/470
in 0.5% (2/382).
America (1.3) (31.2) (8.3) (59.2) (33.4)
Former 14/145 54/145 17/145 60/145 145/470
Yugoslavia (9.7) (37.2) (11.7) (41.4) (30.9)
4. Discussion
Developing 13/168 46/168 28/168 81/168 168/470
countries (7.7) (27.4) (16.7) (48.2) (35.7)
In the present study, the prevalence of abnormal hemoglobin and
Group 1: Iron deficiency anemia.
abnormal iron status in mid-pregnancy was 50.2% (236/470); namely
Group 2: Decreased iron stores.
Group 3: Anemia for other reason. anemia in 18.5% (87/470) and decreased iron stores in 31.7% (149/
Group 4: Normal status. 470). Epidemiological surveys performed in European countries
showed a prevalence of decreased iron stores from 25% to 92% and
iron deficiency anemia from 6% to 30% in pregnant women [16]. Al-
The prevalence of decreased iron stores in the study population though routine iron supplementation is given during pregnancy in
was 31.7% (149/470); namely, severe iron depletion in 21.5% (101/ Switzerland, in our study a relatively high prevalence of decreased
470) and iron depletion in 10.3% (48/470) (Table 2). Anemia was iron stores (31.8%) and iron deficiency anemia (6.2%) was found
observed in 18.5% (87/470); consisting of iron deficiency anemia in early in the second trimester. The prevalence of decreased iron stores
6.2% (29/470) and anemia for other reason in 12.3% (58/470). In of 31.8% showed that every third woman does not have sufficient iron
the anemic patients, only mild anemia (Hb 90–109 g/l) was found. stores before pregnancy.
Hemoglobin between 90 and 99 g/l was observed in 31.1% (9/29) According to the WHO global database on anemia, only one study
of the group of patients with IDA and in 5.2% (3/58) of the patients was conducted on the prevalence of anemia during pregnancy in
with anemia for other reason. Hemoglobin concentration between Switzerland [24]. In this study, the prevalence of anemia was ob-
100 and 109 g/l was determined in 68.9% (20/29) of IDA and in served in 6% of the study group, iron deficiency anemia in 3% and
94.8% (55/58) of anemia for other reason. The prevalence of iron de- low serum ferritin (ferritin b12 μg/l) in 5%. Five years later, a 3–4
ficiency anemia and decreased iron stores was higher among women fold higher prevalence was determined in our study. The reason for
from former Yugoslavia (9.7% and 37.2%). The highest prevalence of this increase is a change in the population due to migration; namely
anemia for other reason in patients from developing countries was increased number of refugees and asylum seekers from former Yugo-
observed (16.7%). slavia and developing countries (67%). Apart from Luxembourg and

Table 3
Multivariate logistic regression analysis of the influence of maternal age, parity and origin of the mother on three anemia groups.

Iron deficiency anemia Decreased iron stores Anemia for other reason

OR (95% CI) Adj. OR (95% CI) OR (95% CI) Adj. OR (95% CI) OR (95% CI) Adj. OR (95% CI)

Maternal age (years)

20–30# 1 1 1 1 1 1
b 20 No cases No cases 0.62 (0.22–1.77) 0.77 (0.26–2.26) 1.85 (0.58–5.92) 1.77 (0.53–5.87)
> 30 0.90 (0.42–1.94) 1.36 (0.57–3.24) 0.60 (0.40–0.91)⁎ 0.58 (0.37–0.91)⁎ 0.87 (0.49–1.55) 0.90 (0.48–1.69)
Parity
= 1# 1 1 1 1 1 1
2–3 1.2 (0.53–2.68) 0.83 (0.36–1.92) 1.62 (1.08–2.43)⁎ 1.75 (1.15–2.68) 0.86 (0.48–1.2) 0.84 (0.46–1.53)
>4 3.03 (0.91–10.13) 2.21 (0.62–7.89) 1.08 (0.45–2.59) 1.24 (0.51–3.04) 1.11 (0.36–3.43) 1.19 (0.37–3.80)
Origin of mother (%)
Europe + North America# 1 1 1 1 1 1
Former Yugoslavia 8.28 (1.85–37.11)⁎ 10.04 (2.08–48.49)⁎ 1.31 (0.81–2.11 0.95 (0.56–1.61) 1.47 (0.69–3.15) 1.41 (0.62–3.19)
Developing countries 6.50 (1.44–29.28)⁎ 7.07 (1.54–32.42)⁎ 0.83 (0.52–1.34) 0.70 (0.43–1.14) 2.22 (1.10–4.45)⁎ 2.24 (1.10–4.56)⁎

(iron deficiency anemia: Hb b110 g/l and ferritin ≤15 μg/l; decreased iron stores: Hb ≥110 g/l and ferritin b20 μg/l; anemia for other reason: Hb b110 g/l and ferritin ≥20 μg/l).
Data are odds ratios (95% confidence intervals) and adjusted odds ratios (95% confidence intervals).
#
Baseline category.
⁎ p b 0.05.
532 G. Bencaiova et al. / European Journal of Internal Medicine 23 (2012) 529–533
Liechtenstein, Switzerland has 20.6% of the highest rate of migrants
among the general population in Western Europe [25]. Although mi-
gration has become an important concern in Western Europe [26],
there is no study observing health differences among particular eth-
nic groups.
Most epidemiological data on anemia and iron status in Europe-
an countries were published in the 80s and the beginning of the
90s. Some of these data are not valid because they are only based
on hemoglobin determination. However, hemoglobin concentration
is not thought to be a good indicator of iron deficiency, because
there can be a depletion of body iron stores in the presence of nor-
mal hemoglobin levels. Blood hemoglobin levels have been widely
used for this purpose, since the test is simple and inexpensive to
undertake [27]. Moreover, few data concern southern European
countries, in which a high frequency of genetic disorders may be
a confounding factor in assessment of the prevalence of iron defi-
ciency anemia, when based only on determination of hemoglobin
concentration [16]. The use of ferritin as the gold standard for
iron stores examination has been extensively studied in the last de-
cades, and in today's practice it is still considered the gold standard
[28]. In women, medians of serum ferritin levels vary according to
country, from 24 to 35 μg/l, corresponding to true levels of iron
stores of 240 to 350 mg [29]. In our study, the median of serum fer-
ritin levels was 34 μg/l and 78% of women had a serum ferritin
b50 μg/l, which underlines the fact that a large proportion of fe-
males do not have sufficient iron stores.
In Europe, with an average parity two or less children, the most
important risk factor of iron deficiency anemia is socio-demographic
background. In our study, the prevalence of iron deficiency anemia
was higher among women coming from former Yugoslavia and devel-
oping countries. Contrary to our study, in the study by Cemerlic-
Zecevic et al., which was carried out during the war in Sarajevo, it
was established that war and disruption of the food supply have not
had the expected negative impact of prevalence of anemia in hospita-
lised children [30].
In women, iron status is dependent mainly on the existence and
the magnitude of the menstrual blood losses, which are primarily de-
termined by genetic factors, and secondarily by the method of contra-
ception. The high prevalence of decreased iron stores in pregnant
women could be caused by the absence of contraception before preg-
nancy. Contraception prior to pregnancy reduces menstrual blood
loss by about 50% [31]. In the previous study, it was shown that the
frequency of iron depletion reached only 13.6% in menstruating
women using oral contraceptives [32]. The refusal to take contracep-
tion in our study population is probably based on religious grounds.
On the other hand, most women between 20 and 30 years of age
have a dietary iron intake that is too low to offset losses from men-
struation. In contrast to our study, young age was observed as a risk
factor of anemia in some studies [7,8,27].
The prevalence of anemia for other reason was twice as high in
comparison to IDA in the present population. In patients coming
from Africa and Asia, there is an increased incidence of anemia for
other reason, particularly HIV infection and hemoglobinopathies. In
these patients, with very low education and low economic status,
iron depletion and severe iron depletion were not significantly high.
The associations between iron status and infection may be
bidirectional-viral infection can alter iron metabolism and iron status
may alter severity of disease. No trials have been conducted on the ef-
fect of iron interventions on viral replication rates or severity of dis-
ease in HIV or hepatitis C. Paradoxically, decreased iron stores were
often observed in patients from industrialised countries (31.2% vs.
27.4% in patients from developing countries). Although this group
was not homogenous (Swiss and immigrants from other industria-
lised countries), it is likely that immigrants from culturally neigh-
bouring European countries share fewer socio-economic, nutritional
and religious differences.
Some studies showed a higher risk for women with 2 or more chil-
dren [4–7]. We did not confirm the correlation between parity and
abnormal hemoglobin concentrations. Our results are in accordance
with two previous studies [33,34]. The reason for this may be a rou-
tine iron supplementation given during pregnancy and the small
number of pregnant women with high parity in Western Europe. Dur-
ing pregnancy, anemia increases > 4-fold from the 1st to the 3rd tri-
mester, i.e. the prevalence in the third trimester is about 30-45%
[10,13,35]. Due to routine iron supplementation in Switzerland and
iron treatment in anemic pregnant women, the mean hemoglobin
level before delivery was 121 ± 12 g/l and the prevalence of anemia
before delivery was only 9.7% in the present study.
The limitation of our study is the absence of CRP determination,
since ferritin is a marker of inflammation. Consequently, high serum
ferritin could actually be false positive in patients with inflammation.
On the other hand, ferritin alone is a poor measure of iron status in
late pregnancy, because ferritin dynamics change in late pregnancy
and levels of ferritin fall even in iron-replete women. Therefore we
determined only Hb at the delivery.
Taking into account the deleterious effects of iron depletion on
health and its high prevalence, prevention of this disorder is particu-
larly relevant and may be implemented by different but complemen-
tary means; information about the advantages of using oral
contraceptives or intrauterine devices, information about appropriate
dietary habits, iron supplementation of pregnant women and iron
fortification of food [16]. It is possible to prevent and control anemia
and decreased iron stores by counselling individuals and families
about sound iron nutrition and about iron supplementation during
pregnancy; by screening persons on the basis of their risk for anemia
and decreased iron stores; and by treating and following up persons
with presumptive anemia and decreased iron stores. The necessity
of these precautions is underlined by the fact that every third
woman with iron deficiency anemia in the present study has hemo-
globin concentration between 90 and 99 g/l before physiological dilu-
tion. We suggest that patients should be screened for iron deficiency
anemia in the first trimester and given selective iron supplementation
when appropriate. This may help to reduce manifestations of iron de-
ficiency anemia and thus improve public health.
Learning points
• Decreased iron stores and iron deficiency anemia affect a large pro-
portion of pregnant women in industrialised countries.
• In patients coming from developing countries, a significant increase
of anemia for other reasons was observed and in patients older than
30 years, a significant increase of decreased iron stores.
• Pregnant women should be screened for decreased iron stores and
iron deficiency anemia in the first trimester and given selective
iron supplementation when appropriate. This may help to reduce
manifestations of iron deficiency anemia and thus improve public
health.
Conflict of interest statement
The authors state that they have no conflicts of interest.
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