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ISSN: 1476-7058 (print), 1476-4954 (electronic)
J Matern Fetal Neonatal Med, 2014; 27(9): 887891
! 2014 Informa UK Ltd. DOI: 10.3109/14767058.2013.845161

ORIGINAL ARTICLE

Prevalence of anemia in pregnant women and its effect on neonatal

outcomes in Northeast India
Reeta Bora1, Corey Sable2, Julian Wolfson2, Kanta Boro1, and Raghavendra Rao3
1

Neonatal Unit, Department of Pediatrics, Assam Medical College, Dibrugarh, Assam, India, 2Division of Biostatistics, School of Public Health, and
Division of Neonatology, Department of Pediatrics, University of Minnesota, Minneapolis, MN, USA

Abstract

Keywords

Objectives: To determine the prevalence of anemia in pregnant women and characterize its
effect on neonatal outcome in Northeast India.
Patients and methods: Four hundred and seventy mothers and their newborn infants during
a one month period were included. The association between maternal hemoglobin (Hb) at
delivery and neonatal outcomes were determined.
Results: Anemia (Hb5110 g/L) was present in 421 (89.6%) mothers with 35 (8.3%) having severe
anemia(Hb570 g/L). After adjusting for maternal and neonatal variables, each 10 g/L decrease
in maternal Hb was associated with 0.18 week decrease in gestational length (p 0.003)
and 21 g decrease in birth weight (p 0.093). Severe maternal anemia was associated
with 0.63week (95% CI, 0.031.23week) shorter gestation, 481 g (95% CI, 305658 g) lower
birth weight and 89% increased risk of small-for-gestation (OR 1.89, 95% CI, 1.252.86)in the
offspring, compared with those born to mothers without anemia (p50.001).
Conclusion: Maternal anemia was highly prevalentin this population. Lower gestational age and
birth weight, and increased risk of small-for-gestation were associated with maternal anemia,
especially when maternal Hb was 580 g/L. Maternal anemia needs urgent attention to improve
neonatal outcome in this population.

Low birth weight, maternal anemia,

prematurity

Introduction
Maternal anemia during pregnancy, defined by the World
Health Organization as hemoglobin (Hb) concentration
5110 g/L [1], bodes poorly to the mother and the fetus. The
adverse effects depend upon the severity and duration of
anemia and the stage of gestation. Women with chronic mild
anemia, where anemia is well compensated, may go through
pregnancy and labor without any adverse consequences [2].
Maternal morbidity and mortality increases with worsening
severity of anemia[3]. Antepartum and post-partum hemorrhage, pregnancy induced hypertension and sepsis may lead to
maternal death in women with Hb of 7089 g/L [2]. In women
with Hb 550 g/L even 200 mL blood loss in the third stage of
labor may produce shock and death [2]. Similarly, neonatal
mortality and morbidity increases with severe maternal
anemia [46]. Maternal Hb 580 g/L is associated with low
birth weight [LBW] due to prematurity and intrauterine
growth restriction [3,7,8]. Perinatal mortality rate increases
23 folds when maternal Hb is 580 g/L and 810 folds when
maternal Hb is 550 g/L [3,7].

Address for correspondence: Reeta Bora, M.D, D.M., Associate

Professor, Neonatal Unit, Department of Pediatrics, Assam Medical
College, Dibrugarh, Assam, India. Tel: 91-373-2300167. Fax: 91-3732302227. E-mail: rbora_amc@yahoo.co.in

History
Received 26 July 2013
Accepted 26 August 2013
Published online 23 October 2013

Anemia is highly prevalent in India. Pregnant women and

preschool children are particularly affected with a prevalence
rate of 6575%, in comparison to 14% in developed countries
[912]. The inter-regional variations in the prevalence of
maternal anemia in India has not been well studied. The
institution where the study was conducted caters health care
to rural farming population and tea garden workers within
a catchment area of 200 km radius in Northeast India. The
population habitually consumes a plant-based diet rich in
phytates and polyphenols that inhibit absorption of dietary
non heme iron [13] by forming insoluble complexes [14,15].
The problem is further compounded by the habit of
consuming large quantities of black tea with meals, especially
among the tea garden workers [16]. Additional causes of
anemia in this population include helmithic infections, sickle
cell disease in tea garden worker community, and hemoglobinopathies, such as hemoglobin E disease in those of
Assamese ethnicity [17,18].
The State of Assam, where the institution is located has a
high neonatal mortality rate of 37/1000 live births [11].
Several special care newborn units have been established
in the state, along with implementation of programs, such as
Integrated Management of Neonatal and Childhood Illnesses
program [19], to promote institutional births. The ultimate
goal of these programs is to substantially reduce infant
mortality rate from present 58/1000 live births to 30/1000 live

888

R. Bora et al.

births by 2015 [20]. A better understanding of factors,

particularly those that can be modified, is urgently needed for
achieving this goal. The aims of the present study were to
(1) determine the prevalence of anemia among pregnant
women attending the institution for delivery and (2) characterize its effect on neonatal outcome. Our purpose was to
determine whether prevention and treatment of maternal
anemia during pregnancy needs urgent attention for reducing
the high neonatal mortality rate in this region.

Patients and methods

Study population
The study was approved by the ethics committee of Assam
Medical College. Mothers who delivered a live newborn
infant during the one month period from 8 July 2010 to
8 August 2010 were eligible. Mothers were enrolled soon
after admission for delivery and after obtaining verbal
consent.
Variables and outcome measures
Maternal age, parity, ethnicity, obstetrical problems, delivery
mode and Hb at the time of delivery were recorded. Maternal
anemia was defined as Hb5110 g/L [1]. The gestational age
(GA) of the infant was calculated from the first day of the
last menstrual period and confirmed by physical exam after
birth using the New Ballard Score [21]. Birth weight was
recorded to the nearest 5 g using an electronic scale. LBW
was defined as birth weight 52500 g. Birth weight percentiles
were calculated using Lubchencos growth chart [22]. Infants
with birth weight below third percentile for gestation were
classified as small-for-gestation (SGA). Birth asphyxia was
defined as Apgar score 56 at 5 min. Infants were observed
for respiratory distress and signs of sepsis. The mothers
and infants were followed until discharge or death. In case of
death, the cause of mortality was recorded.
Statistical analysis
Subjects were classified based on their Hb level into No
anemia (Hb  110 g/L) and Anemia (Hb5110 g/L) groups.
The severity of anemia was classified as mild anemia (Hb,
100109 g/L), moderate anemia (Hb, 7199 g/L) and severe
anemia (Hb570 g/L) using the World Health Organization
criteria [1]. Intergroup differences were tested using unpaired
t-tests for continuous variables, and Pearson Chi-square and
Fishers Exact tests for categorical variables. The distribution
of Apgar at 1 min was skewed, therefore, Wilcoxon rank sum
test was applied for this outcome.
To isolate the effects of anemia independent of potential
confounders, multiple linear regression models were used to
predict continuous outcomes such as gestational length and
birth weight. Logistic regression models were employed
to predict categorical outcomes such as neonatal death and
SGA. The regression models included the main effect of Hb
as a continuous variable. In all models, two-way interactions
between (continuous) Hb and all other potential predictors
were tested and forward selection procedures were used to
identify covariates and interaction terms for inclusion in
regression models. Because of their potential confounding

J Matern Fetal Neonatal Med, 2014; 27(9): 887891

influence, maternal age and occupational status were included

as covariates in all regression models regardless of statistical
significance.
Analyses were carried out using the R statistical software
package (version 2.14.1). Data are presented as mean  SD.
All p values reported are two-tailed, with significance defined
as p50.05.

Results
Sample characteristics
Five hundred sixty five mothers delivered 580 live newborn
infants (551 singleton, 13 pairs of twins and 1 set of triplets)
during the study period. Fourteen non-singleton mothers and
their 29 infants were excluded from the study to avoid the
influence of multiple pregnancy on outcome measures.
Additionally, 81 mothers whose Hb level was not available
and their singleton newborn were excluded. Of these
40 (49.4%) were ethnic Assamese, 24 (29.6%) tea garden
workers, and the rest, non Assamese. Four mothers died after
delivering a live born infant. They and their infants were
included in the analysis. Thus, the final analysis included 470
mothers and 470 newborn infants.
Mean maternal age of the cohort was 24.0  3.8 years
(range: 1640 years; median 23 years). Most (57%) were
primigravida (n 267), 38% were second or third gravida
(n 179), and 5% were4third gravida (n 24). Ninety
(19.1%) mothers were from the tea garden worker community.
The mode of delivery was spontaneous vaginal delivery in
269 (57.2%), caesarean section in 189 (40.2%) and forcepsassisted delivery in 12 (2.6%).
Mean maternal Hb was 91.4  15.1 g/L (range: 30149 g/L;
median, 91 g/L). Four hundred twenty one (89.6% of the
sample) mothers were anemic as defined by Hb5110 g/L.
Only 49 mothers (10.4% of the sample) were non-anemic
(Hb  110 g/L). The maternal and neonatal characteristics
of the No anemia and Anemia groups are given in Table 1.
Within the Anemia group, 91 (21.6%) had mild anemia
(Hb, 100109 g/L), 295 (70.1%) had moderate anemia (Hb,
7099 g/L) and 35 (8.3%) had severe anemia (Hb570 gm/
L).The Hb levels of the four mothers who died were (g/L) 73,
80, 80 and 92, and all were from the moderate anemia
group. Excluding these four cases, the mean Hb for the other
466 mothers was 91.5  15.1 g/L. Maternal age and parity did
not have an effect on Hb level.
Table 2 compares selected key neonatal outcomes across
levels of anemia. The following sections describe the effect
of maternal Hb on these outcomes in greater detail.
Effect of maternal Hb on gestational age
The mean gestational age of infants in the cohort was
38.1  1.9 week (range: 2840 week; median, 38 week).
Mean gestational age was 0.38 and 0.63 weeks shorter
(p 0.007 and p 0.04, respectively) in the moderate and
severe anemia group when compared with the No anemia
group. After adjusting for maternal age, occupation, and
gravidity, each 10 g/L decrease in maternal Hb was associated
with a 0.179 week decrease in gestational length (p 0.003).
The effect of Hb on gestational length did not differ by

Maternal Anemia and Neonatal Outcome

DOI: 10.3109/14767058.2013.845161

889

Table 1. Maternal and neonatal variables in the no anemia and anemia groups.
No anemia group
(N 49)

Variable
Maternal variables
Age (y), mean (SD)
Tea garden worker, number (%)
Primigravida, number (%)
Mode of delivery, number (%)
Vaginal vertex delivery
Cesarean section
Forceps-assisted delivery
Breech delivery
Hemoglobin (g/L), mean (SD)
Neonatal variables
Gestation (week), mean (SD)
Birth weight (g), mean (SD)
Length (cm), mean (SD)
Head circumference (cm), mean (SD)
Chest circumference (cm), mean (SD)
Apgar score, mean (SD)
1 min
5 min
Neonatal Complications, count (%)
Birth asphyxia
Respiratory distress
Sepsis
Hypoglycemia
Death

Anemia group
(N 421)

24.3 (3.9)
0 (0.0)
31 (63.3)
19
26
3
1
118.1

(38.8)
(53.1)
(6.1)
(2.0)
(8.9)

38.6
2869.6
48.0
33.5
31.4

(1.1)
(395.1)
(1.6)
(1.1)
(1.1)

1
3
1
7
0

24 (3.8)
90 (19.1)
236 (56.1)

0.62
50.001
0.42

244
163
9
5
88.3

(57.9)
(38.7)
(2.2)
(1.2)
(12.4)

0.02
0.07
0.12
0.49
50.001

(2.0)
(504.3)
(3.5)
(1.7)
(2.0)

0.09
0.01
0.06
0.07
50.001

38.1
2709.5
47.5
33.2
30.5

7.6 (0.8)
8.6 (0.5)

Unadjusted p

50.001
50.001

7.0 (1.3)
8.3 (1.1)

(2.0)
(6.1)
(2.0)
(14.3)
(0.0)

17
21
21
49
9

(4.0)
(5.0)
(5.0)
(11.6)
(2.1)

0.77
0.99
0.57
0.76
0.63

Table 2. Neonatal outcomes by severity of maternal anemia.

Mild anemia (versus no anemia)
Diff

95% CI

p value

Moderate anemia (versus no anemia)

Severe anemia (versus no anemia)

Diff

Diff

Gestational age (weeks)

0.05
0.38
0.28 0.78
Birth weight (g)
153.60 291.40 15.69 0.03
Birth weight percentile
7.55 15.82
0.72 0.07
Chest circumference (cm)
0.79
1.22 0.36 50.001
Head circumference (cm)
0.59
1.04 0.13 0.01
Length (cm)
1.26
2.29 0.23 0.02
Apgar, 1 minute
0.58
0.92 0.23 0.01

0.38
88.49
0.88
0.49
0.03
0.19
0.65

OR

OR

SGA (BW%53%)

1.23

95% CI
0.36

p value
4.26

0.74

1.16

95% CI
0.66
206.30
8.31
0.84
0.38
0.75
0.91

p value

0.11
29.30
6.56
0.15
0.31
0.37
0.40

95% CI
0.67

0.01
0.14
0.81
0.01
0.86
0.50
50.001
p value

2.00

0.59

95% CI

p value

0.63
1.23
0.03 0.04
481.70 658.30 305.00 50.001
21.14 29.86 12.42 50.001
1.80
2.47
1.13 50.001
1.03
1.64
0.43 0.001
1.67
2.52
0.82 50.001
0.73
1.04
0.42 50.001
OR
1.89

95% CI
1.25

p value
2.86

0.002

Bold values denote differences and odds ratios that are statistically different from 0 (1) at the 5% level.
BW birth weight; SGA small-for-gestation.

maternal age, occupation, or gravidity. On average, a 10 g/L

decrease in Hb increased the odds of prematurity (gestational
length 537 weeks) by 33% (p 0.008).
Effect of maternal Hb on birth weight
The mean  SD birth weight of the newborn infants was
2726  496 g (range: 8703860 g). Birth weight was significantly lower in the mild (153.6 g, p 0.03) and severe
(481.7 g, p50.001) anemia groups as compared with the No
anemia group. After adjusting for maternal age, occupation,
gravidity, and gestational length, a 10 g/L decrease in
maternal Hb was associated with a 21 g decrease in birth
weight (p 0.093). However, unlike the effect of Hb on
gestational length, the effect of Hb on birth weight was not
linear. Statistical changepoint analyses [2326] using several
different functions from the changepoint package in R were
performed to identify the level of Hb at which the association

between Hb and birth weight changed most substantially. All

of these analyses suggested that the association changed when
Hb was between 80 and 82 g/L. The effect of Hb on birth
weight did not vary by maternal age, occupation, gravidity or
length of gestation. Birth weight percentiles were 21% lower
in the severe anemia group than the Non- anemia group
(p50.001). The odds of SGA were 90% higher in the severe
anemia group than the No anemia group (p 0.002), but not
significantly different when comparing the moderate or mild
anemia groups with the No anemia group.
Effect of maternal Hb on other neonatal outcomes
Apgar scores at 1 min were lower at all three levels of anemia
as compared to the no anemia group, ranging from a decrease
of 0.58 (p 0.01) in the mild anemia group to a decrease of
0.73 (p50.001) in the severe anemia group. Chest circumference was also significantly lower across all three anemia

890

R. Bora et al.

levels, with the largest decrease in the severe anemia group

(1.8 cm, p50.001). Head circumference and length were
significantly lower in the mild and severe anemia groups.
Several of these findings appeared to be associated with
Hbs effect on gestational age: In regression models adjusted
for gestational age, there was no association between
continuous Hb level and length, chest circumference or
Apgar score at 1 min.
There were nine neonatal deaths, all in the Anemia group
(three in the mild anemia group, five in the moderate anemia
group and 1 in the severe anemia group). Five deaths were
due to birth asphyxia that failed to respond to resuscitation.
The remaining four were due to sepsis. The mean Hb of
the mothers (88.6  15.6 g/L; range: 60 to 105 g/L) of these
infants was not different from the rest of the sample
(88.3  12.3 g/L; range: 30 to 149 g/L).

Discussion
Our study demonstrates that anemia is highly prevalent
among pregnant women of rural farming population in this
region of Northeast India. The prevalence rate of almost 90%
is higher than national average of 6570% [3]. Moreover,
unlike a previous study from India [27], moderate anemia
(Hb, 7099 g/L), rather than mild anemia (Hb, 100109 g/L)
was more common. Multiple factors likely contributed to
the high prevalence of maternal anemia, among which iron
deficiency was potentially the major factor [1315]. In
addition to the risk factors (plant-based diet, helmiths and
malaria) common with the rest of India [15,16,28], the habit
of consuming large quantities of tea that is known to inhibit
dietary iron absorption[8,29,30]was likely responsible for the
higher prevalence and severity of anemia in our population.
The universal occurrence of anemia in the tea garden worker
community supports this contention. Beyond iron deficiency,
sickle cell disease and hemoglobinopathies were potential
risk factors for anemia in this population [18].
Our data show that maternal anemia has negative effects
on neonatal outcomes. Gestational length progressively
decreased with worsening severity of maternal anemia.
The shorter gestational length also appears to mediate the
observed association between Hb and LBW. However, unlike
previous studies [31,32], there was a strong association
between Hb and birth weight that was independent of
gestational length at lower maternal Hb levels. Surprisingly,
unlike mild and severe anemia, moderate anemia did not
influence birth weight and other growth parameters. One
possibility is that most (84%) mothers in the moderate anemia
group had Hb481 g/L, which may have skewed the results.
Previous studies [7,8,33] and our change-point analyses
confirm 80 g/L as the threshold below which low Hb levels
have the greatest influence on birth weight. Another possibility is that hemodilution due to plasma expansion was partly
responsible for the low Hb in the moderate anemia group.
Such plasma expansion is thought to have beneficial
effects on placental circulation and fetal growth [34]. Future
studies are necessary to confirm our findings and explain
the discrepant results. The strongest effect on birth weight
independent of gestational age (i.e. SGA) was seen only with
severe maternal anemia (Hb570 g/L), which is consistent

J Matern Fetal Neonatal Med, 2014; 27(9): 887891

with previous studies [35,36]. Morphological changes in

placenta leading to inadequate nutrient transport and
chronic hypoxia, stress-induced cortisol secretion, oxidative
stress, enhanced risk of infection and inflammation are
potentially responsible for the risk of SGA in severe maternal
anemia [31].
Beyond gestational age and birth weight, maternal anemia
did not influence neonatal outcomes, presumably because
very few mothers were severely anemic [3739]. However,
this does not negate the possibility of other long-term
sequelae in these infants. Preterm as well as LBW infants
are prone to a wide range of long-term problems in physical
growth, metabolic and cardiovascular health, and neurodevelopment. Infants of anemic mothers are also at increased
risk for developing anemia during infancy [4042]. Severe
maternal anemia [Hb570 g/L] adversely affects cord blood
and breast milk iron concentration [42]. Iron deficiency
during early infancy is associated with long-term cognitive
deficits that persist despite iron supplementation [43].
Our study has some limitations. Maternal Hb was
determined during admission for delivery. In the absence
of longitudinal assessment throughout gestation, it is not
possible to know the effect of duration of maternal anemia for
our results. Additional limitations are lack of information
on the cause of anemia, maternal nutritional intake and
the hematological indices in the newborn infants. However,
as a first step for devising prevention strategies to improve
maternal-child health, the study identifies the population
at greatest risk. With additional data on the cause and course
of anemia, specific preventive strategies tailored to this
community could be developed. One such strategy is delaying
tea drinking by at least an hour after a meal or limiting tea
drinking to between meals to minimize its inhibitory effect
on dietary iron absorption [37]. Another strategy is parenteral
iron administration for severe maternal anemia, which is
known to improve neonatal outcomes [44].
Conclusion
In view of the high prevalence of maternal anemia in
pregnancy and its adverse neonatal consequences, prevention
and treatment of maternal anemia is of high priority in this
region of India. Our study demonstrates that most adverse
effects occur when maternal Hb is 580 g/L. Hence, greater
emphasis should be given for achieving and maintaining
maternal Hb480 g/L during the third trimester. Mandatory
screening for anemia in the clinic and home settings by
community health care providers may help. A well designed,
prospective study is necessary to address the long-term effects
of maternal anemia on maternal and neonatal health and
to devise strategies beyond routine iron and folic acid
supplementation.

Declaration of interest
The authors report no conflict of interest

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