Tropical Medicine and International Health

volume 9 no 4 pp 486–490 april 2004

Maternal anaemia and its impact on perinatal outcome

Farah Wali Lone1, Rahat Najam Qureshi1 and Faran Emanuel2

1 Department of Obstetrics and Gynecology, Aga Khan University, Karachi, Pakistan

2 Department of Community Health Sciences, Aga Khan University, Karachi, Pakistan

Summary objective To find out the relationship between maternal anaemia and perinatal morbidity and
mortality.
method A cohort of 629 pregnant women was studied from October 2001 to October 2002. Of these,
313 were anaemic (haemoglobin <11 g/dl in labour and on two previous occasions in current preg-
nancy). A total of 316 women had haemoglobin >11 g/dl at all times in pregnancy and were labelled as
non-anaemic. Perinatal outcomes included preterm delivery, low birth weight (LBW) at delivery,
intrauterine growth restriction, perinatal mortality, APGAR score at 1 and 5 min, intrauterine foetal
demise (IUD).
results The risk of preterm delivery and LBW among exposed group was 4 and 1.9 times higher
among anaemic women, respectively. Newborns of anaemic mothers had 1.8 times increased risk of
having an APGAR score of <5 at 1 min and the risk of IUD was 3.7 times higher for anaemic women.
conclusion Low maternal haemoglobin levels are associated with increased risk of preterm delivery,
LBW babies, APGAR score <5 at 1 min and IUD.

keywords anemia, low birthweight, IUGR, IUD, premature birth, perinatal mortality

is commonly considered a risk factor for poor pregnancy

Introduction
Anaemia is one of the most prevalent nutritional deficiency
problems afflicting pregnant women (Thangaleela &
Vijayalakshmi 1994a). The extent to which maternal
anaemia affects maternal and neonatal health is still
uncertain. It has long been recognized that anaemia is a
major public health problem especially among poorer
segments of the population in developing countries such as
India, Pakistan and Bangladesh (World Health Organiza-
tion 1992). Anaemia that complicates pregnancy threatens
the life of both the mother and the foetus. The World
Health Organization defines anaemia in pregnancy as
‘haemoglobin levels of 11 g/dl or less’ (Thangaleela &
Vijayalakshmi 1994b). There is a lot of variability owing to
differences in socioeconomic conditions, lifestyles and
health-seeking behaviours across various cultures. Prior
research in Pakistan documents iron deficiency as the
leading cause of anaemia in pregnancy (Karim et al. 1994).
The effects of anaemia in terms of pregnancy outcomes
have not been evaluated systematically in randomized,
prospective intervention trials that include a sufficient
number of iron deficient women, while controlling for
possible confounding factors.
The pattern of anaemia in Pakistan and other Asian
countries shows a trend that appears to be one of the areas
of public health that requires attention. Maternal anaemia
outcome (Gregory & Taslim 2001). Some studies have
demonstrated a strong association between low haemo-
globin before delivery and adverse outcomes (Kathleen &
Rasmussen 2001). However, others have not found a
significant association. Thus, there is insufficient informa-
tion to asses the overall adverse impact of anaemia during
pregnancy. Our aim was to determine the relationship
between maternal anaemia and perinatal outcome.
Material and methods
In this cohort study, the association of multiple effects of
anaemia with perinatal outcome was studied among
pregnant women in the Obstetrics Department of the Aga
Khan University Hospital Karachi, Pakistan, from October
2001 until October 2002.
A total number of 2975 women were delivered during
the study year. Of these, we included all the women who
fulfilled the inclusion criteria, i.e. attended outpatient care
before 16 weeks of gestation; age 16 years and older;
singleton pregnancy with a complete medical record.
Women with a past history of preterm delivery, obstetrical
complications or medical illnesses except anaemia were
excluded in order to control for confounding factors. As
preterm delivery can recur in the next pregnancy, a past
history of preterm delivery per se can cause preterm

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Tropical Medicine and International Health volume 9 no 4 pp 486–490 april 2004

F. W. Lone et al. Maternal anaemia and perinatal outcome

delivery, rather than anaemia. Only 629 women fulfilled Table 1 Comparison of the demographic and socioeconomic
the inclusion criteria. Most of the exclusions were women characteristics of the anaemic and non-anaemic groups
who had three or fewer antenatal visits and therefore only
Non-anaemic
one haemoglobin test during their pregnancy. Variable Anaemic group group P value
The anaemic group was defined as having haemoglobin
levels below 11 g/dl in labour and on two previous Age (mean ± SD) 26.85 ± 4.77 27.08 ± 4.65 0.005*
occasions during the current pregnancy. The non-anaemic BMI (mean ± SD) 23.62 (3.65) 24.15 (3.89) 0.039*
group included those women whose haemoglobin level was Respondent’s education, n (%) 0.004*
>11 g/dl at all times during pregnancy. Women were Up to grade 10 264 (84.3) 288 (91)
interviewed in Urdu, on the day after delivery and the data Above grade 10 49 (15.7) 28 (9.0)
were recorded on a pre-designed questionnaire that recor- Employment status, n (%) 0.548
ded BMI, haemoglobin estimation at first antenatal visit, at Employed 265 (84.7) 263 (83.2)
House wives 48 (15.3) 53 (16.8)
28–32 weeks, at 33–37 weeks and in labour, gestational
age at delivery, perinatal outcome (live birth, stillbirth, Family structure, n (%) 0.058
intrauterine foetal demise, IUD), intrauterine growth Joint 202 (64.5) 184 (58.2)
Nuclear 110 (35.1) 132 (41.8)
restriction (IUGR) and the type of IUGR. Gestational age
was calculated from first day of last menstrual period. Monthly income in Rupees, n (%) 0.004*
IUGR was defined as the foetal growth (measured by (1US$ ¼ 58 Rupees)
Up to 20 000 114 (36.4) 118 (37.3)
ultrasound) less than the 10th centile for that gestational
20 000–30 000 99 (31.6) 117 (37.0)
age. Preterm delivery was defined as delivery after 24 and 30 000–50 000 82 (26.2) 70 (22.2)
before 37 completed weeks of gestation. IUD was defined >50 000 18 (5.8) 11 (3.5)
as foetus without cardiac activity, confirmed on ultra-
sound, at any time after 24 weeks of pregnancy. Stillbirth * P < 0.005 shows the difference is statistically significant.
was defined as the death of a live foetus during the birth
process. The weight of newborns and their APGAR score i.e. 23.62 (SD ¼ 3.65) among anaemic women compared
at 1 and 5 min were recorded. to 24.15 (SD ¼ 3.89) among the non-anaemic women.
One month after delivery, we repeated the interview Most women in both groups were Muslims, urban dwellers
with the mother and reviewed the medical records of the and spoke the national language Urdu. The majority of the
neonate, documenting its health status, perinatal mortality women (84.3% in the anaemic group and 91% in the non-
(PNM) and its cause. PNM was defined as death of a foetus anaemic group) had attended school to grade 10 or less.
after 24 weeks of pregnancy until 1 week after delivery. More than 83% were housewives in both groups. About
64.5% in the anaemic group and 58.2% of non-anaemic
women lived in a joint family, i.e. with parents, grand-
Data analysis
parents and siblings in addition to husband and children.
The data was analysed in spss version 7.5. Frequencies were As the family income is divided among many people, the
determined, Levene’s test was applied to measure equality of share of nutrition decreases accordingly. Household
variances and t-test was used to compare means. Univariate monthly income is also given. The results in the two groups
analysis was carried out. For further evaluation of data, (from statistical analysis) revealed that the two samples
multivariate analysis was done to control for confounding were well matched and there was no statistically significant
factors using multiple logistic regression for dependent difference among the two groups.
variables. Results are expressed as means (SD), adjusted Table 2 outlines the univariate analysis of perinatal
relative risk and 95% confidence interval (95% CI). outcome variables in the two groups. Risk of preterm
delivery (<37 weeks) was four times higher among anaemic
women with a statistical significant association (95%
Results
CI ¼ 2.5–6.3). There was a 2.2 times increased risk of
A total of 629 women fulfilled the inclusion criteria, LBW in the anaemic group (95% CI ¼ 1.3–3.7) and a 1.9
313 anaemic and 316 non-anaemic. Twenty-two women times increased risk among anaemic women of giving birth
were lost to follow-up. Table 1 shows the demographic to IUGR babies (95% CI ¼ 1.1–3.3). The risk of PNM was
and socioeconomic characteristics of the two groups. The 3.2 times higher among anaemic women (95% CI ¼ 0.7–
mean age of anaemic women was 26.85 (SD ¼ 4.77) years 14.6). The risk of an APGAR score <5 at 1 min and <7 at
against 27.08 (SD ¼ 4.65) years among non-anaemic 5 min was 2.1 and 1.7, respectively (95% CI ¼ 1.2–3.7
women. The BMI of women in both groups was similar, and 1.0–3.1) for anaemic women. They also were at

ª 2004 Blackwell Publishing Ltd 487

Tropical Medicine and International Health volume 9 no 4 pp 486–490 april 2004

F. W. Lone et al. Maternal anaemia and perinatal outcome

Table 2 Univariate analysis of perinatal outcomes among the LBW in the anaemic population was 1.9 times higher (95%
two groups CI ¼ 1.0–3.4). The risk of the anaemic population of
giving birth to babies with an APGAR score <5 at 1 min
Anaemic Non-anaemic Adjusted
Variable group, n group, n relative risk 95% CI (95% CI ¼ 1.2–3.7) was 1.8 times higher. The risk
association of IUD was 3.7 times higher among anaemic
Premature birth women (95% CI ¼ 0.86–14.6).
Yes 79 20 4.0 2.5–6.3
No 234 296 1.0
Low birth weight Discussion
Yes 42 19 2.2 1.3–3.7 Anaemia is a common problem in pregnant women in
No 271 292 1.0
developing countries. Pregnancy outcomes vary depending
IUGR upon the type of anaemia. Studies have demonstrated
Yes 41 18 1.9 1.1–3.3
differences in outcomes between iron deficiency and
No 297 268 1.0
physiological anaemia of pregnancy (Duthie et al. 1991).
Perinatal mortality Also, the relationship between maternal anaemia and
Yes 6.0 2.0 3.2 0.7–14.6
perinatal outcomes such as increased risk of perinatal
No 306 313 1.0
death, preterm delivery, LBW and low APGAR score at
Low APGAR 1 min is not clear.
at 1 min
The risk of prematurity and LBW is higher in anaemic
Yes 32 16 2.1 1.2–3.7
No 272 299 1.0 women. In populations in which the rate of anaemia is
low among non-pregnant women, the primary cause of
Low APGAR
at 5 min
anaemia during pregnancy is likely to be plasma volume
Yes 27 17 1.7 1.0–3.1 expansion, and this anaemia is not associated with
No 280 298 1.0 negative birth outcomes (Whittaker et al. 1996). Mater-
IUD nal haemoglobin values during pregnancy are associated
Yes 5.0 2.0 2.5 0.7–13.0 with birth weight and preterm birth in a U-shaped
No 308 314 1.0 relationship with high rates of babies who are small at
low and high concentrations of maternal haemoglobin.
However, some of this association may result from using
Table 3 Multivariate analysis of perinatal outcomes among ‘lowest haemoglobin’ rather than a haemoglobin value
anaemic and non-anaemic groups controlled for the stage of pregnancy. A similar U-shaped
association is likely to be present between maternal
Variable ARR 95% CI
haemoglobin concentration and PNM, but the data to
Premature birth establish this association remain insufficient (Verma &
Yes 4.0 2.5–6.3 Dhar 1976).
No 1.0 As it is estimated that about 7.3 million perinatal
Low birth weight deaths occur annually in the world, most of these in
Yes 1.9 1.0–3.4 developing countries especially Asia (Shazia et al. 1994),
No 1.0 one could assume many of these could be prevented by
Low APGAR at 1 min correcting maternal anaemia. Prematurity and birth
Yes 1.8 1.2–3.7 anoxia are the main causes of perinatal deaths in
No 1.0 Pakistan. In the studied population, prematurity was the
IUD leading cause of perinatal death but less frequent than in
Yes 3.7 0.86–14.6 other hospitals in Pakistan (Saad 1990; Rana 1994),
No 1.0 indicating poor resuscitation facilities and neonatal care
in the country.
Severe anaemia (<8 g/dl) is associated with birth weight
2.5 times increased risk of IUD compared to the normal values that are 200–400 g lower than in women with
population (95% CI ¼ 0.7–13.0). higher (>10 g/dl) haemoglobin values, but these researchers
Table 3 shows the multivariate analysis of the study generally have not excluded other factors that might also
population. Anaemic women were at four times increased have contributed to both LBW and the severity of anaemia
risk of preterm delivery (95% CI ¼ 2.5–6.3). The risk of (Steer et al. 1995).

488 ª 2004 Blackwell Publishing Ltd

Tropical Medicine and International Health
F. W. Lone et al. Maternal anaemia and perinatal outcome
The complication of preterm labour and pregnancy-
related infections has also been shown to have a causal
relationship with each other. Maternal infections during
pregnancy are a well-known risk factor for preterm
labour and the examination of amniotic fluid or placental
membranes has shown the presence of bacteria or inflam-
matory cytokines (Amici et al. 1999). The relationship of
anaemia and infections may be due to adverse effect on
immune function, by altering the proliferation of T and B
lymphocytes, reducing the bactericidal activity of phago-
cytes and neutrophils (Hooton et al. 1996). Lymphocyte
stimulation indices are also lower in anaemic women
(Stamey & Timothy 1975).
Anaemia is considered one of the main nutritional
deficiency disorders affecting a large fraction of the
population not only in developing but also in developed
countries. Poverty, gender bias and lack of education
about the importance of intake of balanced and iron-rich
diet contribute to it, rendering anaemia a continuing
challenge for change and intervention at an early age
in women. The high prevalence of iron and other
micro-nutrient deficiencies among women before and
during pregnancy calls for interventions such as
periodic supplementation (Cutner et al. 1999). This
may help to reduce manifestation of iron deficiency,
2 Obstetrics and Gynecology 102, 523–527.
improve public health and thus reduce maternal
morbidity and mortality.
Our study was conducted in a tertiary care hospital
which is not a representative of the country. Since most
women in Pakistan deliver at home, the burden of
anaemia can be expected to be much higher outside the
hospital setting. Studying the impact of maternal anaemia
on quality of life could have strengthened the study and
would have added more to our knowledge. Other
nutritional deficiencies have also been proposed to have
an impact on maternal and foetal outcome, e.g. niacin
and zinc deficiency. These need to be studied in detail so
that when further research is being done on iron
deficiency anaemia, the affect of such confounders can be
ameliorated.
Conclusions
The results show the association of maternal anaemia in
pregnancy with increased risk of delivery of premature
and LBW babies, IUD, low APGAR score at 1 min and
PNM. Deaths were commonly due to prematurity and
sepsis. In developing countries, maternal anaemia remains
a cause of considerable PNM and morbidity (Cutner et al.
1999). The improvements achieved in the developed
world are due largely to more effective diagnosis and
treatment.
ª 2004 Blackwell Publishing Ltd
volume 9 no 4 pp 486–490 april 2004
We therefore propose that routine iron supplementation
should be given during pregnancy and postpartum to
cover losses during delivery and lactation. Obstetricians
have an important role to play by making women aware
of the iron content in a balanced diet, especially in green
leafy vegetables. Iron supplementation may improve
lymphocyte stimulation and thus decrease the risk of
intrapartum and postpartum infection. Additional studies
on pregnant women are needed evaluating immune
function in response to iron supplementation. Pregnant
women should be counselled regarding the risks of adverse
pregnancy outcomes with anaemia. Little is known
concerning the effects of maternal iron status during
pregnancy on the infant’s subsequent health and develop-
ment and on the quality of life of the mother. These areas
warrant detailed research.
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Authors
Farah Wali Lone, H. No. NE 38/A, Aziz Manzil, Tipu Road, Rawalpindi, Pakistan. E-mail: farahwali21@yahoo.com
(corresponding author).
5 Rahat Najam Qureshi, Aga Khan University Hospital, Stadium Road, New Town, Karachi, Pakistan. E-mail: rahat.qureshi@aku.edu
Faran Emanuel, Aga Khan University Hospital, Stadium Road, New Town, Karachi, Pakistan. E-mail: faran.emanuel@aku.edu

490 ª 2004 Blackwell Publishing Ltd