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Tropical Medicine and International Health

doi:10.1111/tmi.12312

volume 19 no 7 pp 841851 july 2014

Reproductive risk factors assessment for anaemia among


pregnant women in India using a multinomial logistic
regression model
Vanamail Perumal
Department of Obstetrics and Gynaecology, All India Institute of Medical Sciences, New Delhi, India

Abstract

objective To assess reproductive risk factors for anaemia among pregnant women in urban and
rural areas of India.
method The International Institute of Population Sciences, India, carried out third National Family
Health Survey in 20052006 to estimate a key indicator from a sample of ever-married women in the
reproductive age group 1549 years. Data on various dimensions were collected using a structured
questionnaire, and anaemia was measured using a portable HemoCue instrument. Anaemia
prevalence among pregnant women was compared between rural and urban areas using chi-square
test and odds ratio. Multinomial logistic regression analysis was used to determine risk factors.
results Anaemia prevalence was assessed among 3355 pregnant women from rural areas and 1962
pregnant women from urban areas. Moderate-to-severe anaemia in rural areas (32.4%) is
significantly more common than in urban areas (27.3%) with an excess risk of 30%. Gestational age
specific prevalence of anaemia significantly increases in rural areas after 6 months. Pregnancy
duration is a significant risk factor in both urban and rural areas. In rural areas, increasing age at
marriage and mass media exposure are significant protective factors of anaemia. However, more
births in the last five years, alcohol consumption and smoking habits are significant risk factors.
conclusion In rural areas, various reproductive factors and lifestyle characteristics constitute
significant risk factors for moderate-to-severe anaemia. Therefore, intensive health education on
reproductive practices and the impact of lifestyle characteristics are warranted to reduce anaemia
prevalence.
keywords anaemia, pregnant women, reproductive risk factors, multinomial logistic regression, India

Introduction
Anaemia caused by nutritional deficiency at the level of
<11 g/dl is one of the major risk factors for maternal
mortality, infant mortality, low birthweight and preterm
birth. WHO (2008) estimates the global prevalence of
anaemia (19932005) among pregnant women at 42%
(95% CI: 4044), that is, 56 million (95% CI: 5459). In
south-east Asian countries, anaemia prevalence among
pregnant women is significantly higher at 48% (95%CI:
4453%), affecting 18 million (95% CI: 1620) women.
Anaemia prevalence among pregnant women is estimated
to be 14% in developed and 51% in developing countries
(WHO 2004). In India, it is 6575%, the highest in
South Asian countries, and constitutes an important public health problem. Indias share of maternal deaths due
to anaemia in South Asia is an alarming 80% (Ezzati
et al. 2002).

2014 John Wiley & Sons Ltd

Numerous epidemiological studies have established the


major causes of anaemia as poor dietary intake, poor dietary iron intake, HIV/AIDS, malaria, infectious diseases,
bacterial infections and helminthic infections. Among
pregnant women, reproductive behaviours such as parity
status, gestational age, history of pregnancy complications, age at marriage, pregnancy interval between two
births and frequency of antenatal check-ups aggravate the
anaemia status even further. Anaemia in pregnant women
is likely to reduce the resistance to blood loss during
delivery and cause death. For the growth of the foetus
and of the placenta, an adequate amount of circulating
blood in the expectant mother and an increased supply of
nutrients, particularly iron and folic acid, are necessary.
However, due to short birth intervals and frequent terminations of pregnancies, the majority of women in developing countries start pregnancy with depleted body stores
of these nutrients and need to compensate for even higher
841

Tropical Medicine and International Health

volume 19 no 7 pp 841851 july 2014

V. Perumal Reproductive risk factors of anaemia in pregnant women

requirements than usual. This alarming situation in rural


areas requires the immediate attention of national programmes.
A number of epidemiological studies (Lobel et al.
2000; Mart-Carvajal & Pe~
na Marti 2004; Agarwal et al.
2006; Lawrence et al. 2007; Bharati et al. 2008; Maria
et al. 2010; Mosha Theobald & Philemon 2010; Samuel
et al. 2013) were carried out to determine the risk or
associated factors for anaemia status through logistic
regression or multiple linear regression analyses. In contrast, this study attempted to determine significant reproductive risk factors for anaemia separately among
pregnant women in rural and in urban areas of India. As
there are differences in lifestyle, food habits, cultural
behaviours with respect to reproduction, health-seeking
facilities and communication systems between urban and
rural areas, the factors causing anaemia may differ, and
identifying them separately for the two environments may
be helpful in devising an appropriate control strategy.

Materials and methods


Study area
Third National Family Health Survey (NFHS-3) was conducted under the stewardship of the Ministry of Health
and Family Welfare (MOHFW), Government of India,
with the collaborative efforts of a large number of
research organisations. The International Institute for
Population Sciences (IIPS), Mumbai, was designated by
MOHFW as the nodal agency for the project. NFHS-3
covered 99% of Indias population in 29 states; it collected information from a representative sample of
109 041 households: 124 385 women aged 1549 years
and 74 369 men aged 1554 years between November
2005 and August 2006. Salient findings of the study are
available on IIPS websites (http://www.nfhsindia.org/
india2.html; http://www.measuredhs.com/pubs/pdf/
FRIND3/FRIND3-VOL2.pdf). The database on women
was obtained from IIPS, Mumbai, and also downloaded
from the Demographic Health Survey site http://www.
measuredhs.com/data/dataset/India_Standard-DHS_2006
on the understanding that any publication from the data
will be duly acknowledged and a copy of the publication
will be added to the site.

estimating the key indicators from a sample of evermarried women in the reproductive ages of 1549 years.
Accordingly, the target sample size for each state was estimated in terms of the number of ever-married women of
reproductive age to be interviewed. In each state, in rural
areas, two-stage sampling was adopted: Initially, villages
were selected as primary sampling unit (PSUs) with probability proportional to population size (PPS); subsequently,
a random selection of households within each village was
taken. In urban areas, a three-stage procedure was adopted
with ward as PSU based on PPS, random selection of one
census enumeration block (CEB) in each PSU and finally
random selection of at least 15 and at most 60 households
in each CEB. All selected households were visited during
the main survey. If a particular PSU was inaccessible, a
replacement PSU with similar characteristics was selected
by the main nodal agency IIPS.
All pregnant women surveyed in the age group 15
49 years with their anaemia status were taken as inclusion criteria for the present analysis, and the remaining
data were considered as exclusion criteria. Stage by stage
sample size and the data considered for the final analysis
are described in Flow chart 1.
Data collection
Respondents were briefed about the purpose of the survey in the local language and verbal consent was
obtained. A structured questionnaire was used to collect
Number of women surveyed in
1519 years age from 29 states
124 385

Anaemia level measured


from 28 states
112 714

Anaemia level not measured


3896 from one state (Nagaland)
7775 due to technical reasons
(excluded)
Number of non-pregnant women
107 397 (excluded)
Number of pregnant women
5317 (included)

Sampling design and sample size


Sampling design and sample size determination are
explained in detail on the IIPS website (http://www.nfhsin
dia.org/india2.html). In brief, a census in 2001 was the
sampling frame for the NFHS-3, conducted with an aim of
842

Numbers in rural areas


3355

Numbers in urban areas


1962

Flow chart 1 Flow chart showing sampling design and sample


size for anaemia prevalence assessment.

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Tropical Medicine and International Health

volume 19 no 7 pp 841851 july 2014

V. Perumal Reproductive risk factors of anaemia in pregnant women

various indicators for different dimensions from all the


women aged 1549 years who were usual residents of
the sample household. The questionnaire was designed to
cover background characteristics (age, marital status,
caste/tribe, religion, education, employment status, mass
media exposure, place of residence and husbands background), reproductive behaviour and intentions (dates
and survival status of all births, current pregnancy status,
pregnancy losses, use of ultrasound for recent pregnancies
and future childbearing intentions), marriage and cohabitation (duration of marriage and cohabitation, number of
times married) and lifestyle characteristics. Data on other
issues were also collected; details can be found at http://
www.nfhsindia.org/india2.html. To assess the nutritional
level of everyone, body mass index (BMI) was calculated
from height and weight. Anaemia prevalence was
assessed using the haemoglobin level measured with a
portable HemoCue instrument (manufactured by HemoCue AB, Angelholm, Sweden) that provides the test result
in <1 min.
Data coding and analysis
While carrying out data analyses, variables were classified
and coded and in the present analysis, also same classifications and coding were maintained. Accordingly, education was classified as no education (0), primary (1),
secondary (2) and higher (3). Various indicators of
wealth assessment of each household were collected, and
the wealth index of each household was derived based on
the factor analysis score. It was classified and coded as
poorest (1), poorer (2), middle (3), richer (4) and richest
(5). Reproductive variables considered for the present
analysis were age at first marriage (years), termination of
pregnancy (no = 0; yes = 1), age at first birth (years),
number of children ever born, number of living children,
number of children under five years, number of births in
the last five years, number of births in the last three
years, number of births in the past year, current pregnancy duration (months) and household size. Variables
considered for lifestyle characteristics were smoking habit
(no = 0; yes = 1) and alcohol consumption (no = 0;
yes = 1). BMI was classified into four categories based on
the WHO criteria: underweight (<18.5 kg/m2), normal
weight (18.524.9 kg/m2), overweight (25.029.9 kg/m2)
and obesity (>29.9 kg/m2). A mass media exposure variable was created based on scores of three indicators
(reading newspaper: 0never, 1occasionally and 2daily;
listening to radio: 0never, 1occasionally and 2daily;
and watching television: 0never, 1occasionally and
2daily), and total score for each individual was expected
to be between zero and six.

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Haemoglobin levels were classified as normal (11.0 g/


dl), mild anaemia (10.010.9 g/dl), moderate anaemia
(7.09.9 g/dl) and severe anaemia (<7.0 g/dl). Present
analysis was carried out by considering three categories
of anaemia level (normal = 0, mild = 1, moderate to
severe = 2).
Descriptive statistics such as mean and standard deviation (SD) were calculated for continuous variables and
compared between rural and urban areas using Students
t-independent test. Similarly, using univariate analysis,
anaemia prevalence by background characteristics, reproductive variables and lifestyle characteristics was compared between rural and urban areas using chi-square
test. Multinomial logistic regression analysis was carried
out to determine the relationship between the anaemic
status of pregnant women (dependent variable) and various socio-demographic and reproductive variables (independent variables) (Hosmer & Lemeshow 2000). In brief,
multinomial logistic regression is used to analyse relationships between a non-metric dependent variable and metric or dichotomous independent variables. Multinomial
logistic regression compares multiple groups through a
combination of binary logistic regressions. As multinomial logistic regression does not make any assumptions
of normality, linearity and homogeneity of variance for
the independent variables, it is preferred to discriminant
analysis when the data do not satisfy these assumptions.
The overall fit of the model is based on the reduction in
the likelihood values for a model which does not contain
any independent variables and the model that contains
the independent variables. The difference in likelihood
follows a chi-square distribution and is referred to as the
model chi-square. The significance test for the final model
chi-square is the statistical evidence of the presence of a
relationship between the dependent variable and the combination of the independent variables. Significant variables for the model were assessed based on statistical
significance of individual coefficients using Wald statistics. A standard error that increased an amount of 10%
from its coefficient value was taken as indication of multicollinearity among independent variables. The model
was fitted again after dropping suspected collinearity
variables. Finally, the utility of the best fitted model was
determined. A more useful measure to assess the utility is
classification accuracy, which compares predicted group
membership based on the logistic model to the actual
known group membership, which is the value for the
dependent variable. The benchmark that is used to characterise a multinomial logistic regression model as useful
is a 25% improvement over the rate of accuracy achievable by chance alone. This is referred to as by chance
accuracy or the proportional by chance accuracy rate,
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V. Perumal Reproductive risk factors of anaemia in pregnant women

which is computed by calculating the proportion of cases


for each group in the Case Processing Summary, and
then squaring and summing the proportion of cases. A
forward stepwise procedure was used to select an adequate model based on overall fit, statistical significance of
individual coefficient and the proportional by chance
accuracy rate. In the forward stepwise procedure, the
score chi-square statistic is computed for each independent variable not in the model and examines the largest
of these statistics. If it is significant at some entry levels,
the corresponding variable is added to the model. Once a
variable is entered in the model, it is never removed from
the model. The process is repeated until none of the
remaining variables meet the specified level for entry. For
all the statistical tests, level of significance P < 0.05 was
considered, and Statistical Package for Social Sciences
(SPSS) IBM version 19.0 was used for data analyses.

Results
Basic-characteristics
The distribution of pregnant women by various study
characteristics and residential status is shown in Table 1.
We found significant (P < 0.05) variation in wealth
index, education level and nutritional status between
rural and urban areas. In rural areas, the percentage of
women who smoke (11.1%) or drink alcohol (3.9%) is
significantly (P < 0.05) higher than in urban areas (6.3%
and 1.3%, respectively). Similarly, in rural areas, mean
(SD) age (17.7  3.5 years) at first marriage and age
(19.3  3.3 years) at first child birth are significantly
(P < 0.05) younger than in urban areas (Table 1). Mean
(SD) number of children ever born (1.6  1.8), number
of living children (1.4  1.6), number of births
(0.8  0.8) in the last five years and number of births
(0.5  0.6) in the last three years are significantly
(P < 0.05) higher among pregnant rural than urban
women. The mean (SD) number of persons per household (6.2  3.2) in rural areas is significantly (P < 0.05)
higher than in urban areas (5.8  3.2). The mean (SD)
duration of current pregnancy (5.5  2.3 months) among
rural women is significantly (P < 0.05) longer than that
of urban women (5.3  2.2).
Anaemia prevalence status
Prevalence of mild and moderate-to-severe anaemia for
the entire country is 24.1% (95% CI: 23.025.3%) and
30.5% (95% CI: 29.331.8%), respectively. Moderateto-severe anaemia prevalence has significantly (v2 = 23.8;
P < 0.001) increased from 26.3% (95% CI: 25.227.5%)
844

observed in the NFHS-2 survey of 19981999 (IIPS


1999; Bharati et al. 2008). While the prevalence of mild
anaemia in rural (23.8%; 95% CI: 22.425.3%) and
urban (24.5%; 95% CI: 22.726.5%) areas do differ
markedly, moderate-to-severe anaemia prevalence in rural
areas (32.4%; 95% CI: 30.834.0%) is significantly
(v2 = 14.8; P < 0.001) higher than in urban areas
(27.3%; 95% CI: 25.429.3%) with crude odds ratio
(OR) of 1.3 (95% CI: 1.11.4), implying that
rural women are about 30% more likely to have moderate-to-severe anaemia than urban women.
Mild and moderate-to-severe anaemia prevalence by
age at first marriage is depicted in Figure 1. While mild
anaemia prevalence does not show any significant trend
over age, moderate-to-severe anaemia prevalence reveals
a significant (v2-trend in proportion = 89.0; P < 0.001)
decreasing trend over age; the risk is reduced by about
50% at age >20 years compared with 20 years. In rural
areas, moderate-to-severe anaemia prevalence among
those married at <20 years of age is 34.6%, significantly
(v2 = 8.4; P < 0.01) higher than the 30.0% in urban
areas. Those married at <20 years in rural areas are at
about 1.2 times (OR = 1.2; 95% CI: 1.11.4) the risk as
their counterparts in urban areas.
Anaemia prevalence by the number of children born
during the last five years is shown in Figure 2. While
mild anaemia prevalence is independent of births in the
last five years, moderate-to-severe anaemia prevalence
increases significantly with the number of births (v2-trend
in proportion = 62.0; P < 0.001). Those who had 3 or
more births in the last five years have twice the risk as
those who had none. In rural areas, moderate-to-severe
anaemia prevalence (41.3%) among those who had more
than two births in the last five years is significantly
(v2 = 4.1; P = 0.043) higher than in urban areas
(34.0%): rural women are at 1.4 times (OR = 1.4; 95%
CI: 1.11.9) the risk as their urban counterparts.
Anaemia prevalence by period of gestation is shown
in Figure 3. While mild anaemia prevalence remains
almost static throughout the pregnancy period, moderate-to-severe anaemia exhibits a significant (v2-trend in
proportion = 12.4; P < 0.01) increasing trend with the
gestation period and the risk doubles in the late stage of
pregnancy. In rural areas, moderate-to-severe anaemia
prevalence (38.7%) among the women of more than 6month gestation is significantly (v2 = 5.5; P = 0.02)
higher than in urban areas (34.0%); the risk in rural
areas is 1.2 times (95% CI: 1.11.5) of that in urban
areas. Based on univariate cross-tabulation analysis, the
significant variables that are associated with anaemia
prevalence are presented in Table 2 for both urban and
rural areas.

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Tropical Medicine and International Health

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V. Perumal Reproductive risk factors of anaemia in pregnant women

Table 1 Distribution of pregnant women by study characteristics and residential status


Residential area
Socio-economic characteristics
Wealth Index (%)
Poorest
Poorer
Middle
Richer
Richest
Educational status (%)
No education
Primary
Secondary
Higher
BMI status (%)
Under weight (<18.5 kg)
Normal weight (18.524.9)
Pre-obese (25.029.9)
Obesity (> = 30)
Smoking habit (%)
Alcohol habit (%)
Mean (SD) age (years) at first marriage
Terminated pregnancy (%)
Mean (SD) age (years) at first birth
Mean (SD) number of children ever born
Mean (SD) number of living children
Mean (SD) number of children under 5 years
Mean (SD) number of births in the last 5 years
Mean (SD) number of births in the last 3 years
Mean (SD) number of births in the past year
Mean (SD) household size
Mean (SD) duration (months) of current pregnancy

Urban (n = 1962)

Rural (n = 3355)

Chi-square/t-value

3.1
7.0
15.2
31.9
42.8

25.6
24.2
23.3
18.4
8.5

1388.0

0.000

22.2
11.1
50.8
15.9

45.8
16.6
34.2
3.5

533.1

0.000

15.5
67.0
14.2
3.3
6.3
1.3
19.4 (3.9)
17.4
20.5 (3.5)
1.2 (1.4)
1.0 (1.3)
0.5 (0.8)
0.7 (0.7)
0.4 (0.5)
0.04 (0.2)
5.8 (3.2)
5.3 (2.2)

19.8
72.9
6.6
0.7
11.1
3.9
17.7 (3.5)
17.0
19.3 (3.3)
1.6 (1.8)
1.4 (1.6)
0.5 (0.8)
0.8 (0.8)
0.5 (0.6)
0.05 (0.2)
6.2 (3.2)
5.5 (2.3)

144.6

0.000

P-value

32.9
29.6
16.7
0.15
9.9
9.3
8.4
0.6
6.7
4.6
1.7
4.7
2.5

0.000
0.000
0.000*
>0.05
0.000*
0.000*
0.000*
>0.05*
0.000*
0.000*
>0.05*
0.000*
0.012*

SD, Standard deviation.


*Based on Students t-independent test.

45

Mild

Prevalence (%)

40

Moderate/Severe

35
30
25
20
15
10
5
0

Figure 1 Prevalence (%) of anaemia by


age at first marriage.

<=15

16

Multinomial logistic regression analyses


The combined effect of all significant variables identified in
univariate analysis was assessed using multinomial logistic
regression analysis with forward stepwise procedure.

2014 John Wiley & Sons Ltd

17

18

19
20
21
22
Age at marriage (years)

23

24

25

>25

The analysis was carried out separately for urban and rural
areas after adjusting for education level and wealth
index. Anaemia status was taken as the dependent variable
(1normal, 2mild and 3moderate-to-severe), and all the

845

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V. Perumal Reproductive risk factors of anaemia in pregnant women

45
40
Prevalence (%)

35
30
25
20
15
10
5
0

Mild
0

Moderate/Severe
>=3

Number of births in the last five years

measured reproductive variables and lifestyle characteristics were taken as independent variables. Among the set of
independent variables, education, wealth index, BMI,
smoking habit, alcohol consumption and termination of
pregnancy were taken as categorical variables and the
remaining variables were treated as continuous variables.
Model fitting for urban areas showed that the probability
of the overall model v2 value 120.0 (df = 16) was significant (P < 0.001), indicating that there was a relationship
between the dependent variable and the set of independent
variables. The proportional by chance accuracy rate in the
present analysis was 35.9%, and 30% improvement was
taken as the criterion for an adequate model. The fitted
model yielded 48.6% as classification accuracy, and it is
more than the criteria (46.7%) fixed. Therefore, the overall
fitted model is adequate, and parameter estimates of significant independent variables are presented in Table 3a. Pregnancy duration is the only reproductive variable found to
be a significant risk factor for mild anaemia.
The relative risk ratio (adjusted odds ratio) for mild
anaemia category compared with normal anaemia category is 1.08 (95% CI: 1.021.14). Similarly, the risk due
to pregnancy duration for moderate-to-severe anaemia is
significantly (P < 0.001) increased by 23% (95% CI: 17
30%) over the normal anaemia category. The pregnant
woman in the BMI category of underweight would be at
the risk of getting moderate-to-severe anaemia by the factor 3.57 (95% CI: 1.528.38) compared with normal
anaemia category. The pregnant women in the BMI category of normal weight would be at the risk of getting
moderate-to-severe anaemia about 2.44 (95% CI: 1.08
5.48) times compared with normal anaemia category.
Similarly, having up to secondary-level education, the
likelihood that a pregnant woman would be at the risk of
getting moderate-to-severe anaemia by 1.44 (secondary)
to 2.38 (no education) times compared with normal
anaemia category.

846

Figure 2 Prevalence (%) of anaemia by


number of children born during last five
years.

Model fitting for rural areas showed that the probability of the overall model v2 value 249.5 (df = 20) was significant (P < 0.001). The proportional by chance
accuracy rate in the present analysis was 34.7% and the
fitted model yielded 47.6% as classification accuracy,
which exceeded the 30% improvement criterion fixed.
Therefore, the overall fitted model is adequate and the
coefficient of significant independent variables is presented in Table 3b. While mass media exposure is a significant protective factor (adjusted odds ratio = 0.93;
95% CI: 0.871.00) for mild anaemia, alcohol consumption (adjusted odds ratio = 1.89; 95% CI: 1.143.13)
and increase in pregnancy duration (adjusted odds
ratio = 1.08; 95% CI: 1.041.12) are significant risk factors over normal category.
Significant protective factors for moderate-to-severe
anaemia are increase in age at first marriage (adjusted
odds ratio = 0.96; 95% CI: 0.930.98) and higher mass
media exposure (adjusted odds ratio = 0.91; 95% CI:
0.850.97). A pregnant woman in the wealth categories
of poorest and poor would be at 2.07 (95% CI: 1.36
3.14) and 1.57 (95% CI: 1.052.35) times greater risk of
developing moderate-to-severe anaemia, respectively, over
normal category.) Other significant risk factors for moderate-to-severe anaemia are smoking (adjusted odds
ratio = 1.44; 95% CI: 1.081.92), alcohol consumption
(adjusted odds ratio = 1.66; 95% CI: 1.022.68), increasing pregnancy duration (adjusted odds ratio = 1.18; 95%
CI: 1.141.23) and increase in number of births in the
last five years (adjusted odds ratio = 1.28; 95% CI: 1.14
1.44).
Discussion
This study reveals that due to lack of knowledge on
reproductive process and prevailing cultural marriage
practices, there is significant variation in age at first

2014 John Wiley & Sons Ltd

Tropical Medicine and International Health

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V. Perumal Reproductive risk factors of anaemia in pregnant women

Table 2 Univariate analysis showing significant variables associated with anaemia prevalence by residential status
Anaemia prevalence (%) in
rural areas

Anaemia prevalence (%) in


Urban areas

Variables

Nil

Wealth Index
Poorest
31.2
Poorer
36.7
Middle
42.6
Richer
44.2
Richest
52.4
Educational status
No education
37.9
Primary
47.7
Secondary
47.1
Higher
55.8
BMI status
Under weight
44.4
Normal weight
45.1
Pre-obese
54.5
Obesity
51.6
Alcohol use (No)
46.7
Alcohol use (Yes)
36.0
No. of children born
Nil
49.2
12 Children
46.8
>2 Children
37.2
No. of living children
Nil
49.3
12 Children
46.2
>2 Children
37.1
No. of births in the last 5 years
Nil
49.5
One Child
44.9
More than one Child
40.4
No. of births in the last 3 years
Nil
48.2
One Child
43.8
More than one child
44.4
Mass media exposure level
Nil
35.8
12 score
43.8
34 score
48.3
>4 score
53.0
Smoking (No)
47.0
Smoking (Yes)
39.3

Mild

Moderate/
Severe

Chi-square
(P-value)

Nil

Mild

Moderate/
Severe

Chi-square
(P-value)

29.5
26.6
22.8
27.2
25.1

39.3
36.7
34.6
28.6
22.4

36.8 (0.000)

31.7
38.9
43.8
50.3
56.8

25.6
25.5
25.2
24.1
24.6

42.7
35.6
31.0
25.6
18.6

105.4 (0.000)

24.1
25.7
26.7
24.7

37.9
26.6
26.2
19.6

38.5 (0.000)

35.7
42.5
47.6
61.5

25.5
23.7
25.4
24.8

38.8
33.8
27.0
13.7

75.0 (0.000)

24.7
26.1
22.6
35.9
25.9
12.0

30.9
28.8
22.9
12.5
27.5
52.0

18.3 (0.006)

44.8
40.7
44.6
52.2
42.5
23.8

24.6
25.5
22.5
21.7
24.9
31.5

30.6
33.8
32.9
26.1
32.6
44.6

6.0 (0.428)

26.1
24.8
27.5

24.7
28.4
35.3

14.8 (0.005)

48.1
42.1
32.1

25.9
24.2
25.9

26.0
33.7
42.0

64.4 (0.000)

25.7
25.4
26.8

25.0
28.4
36.2

13.5 (0.009)

48.2
40.8
32.1

25.3
24.6
25.8

26.5
34.6
42.1

60.0 (0.000)

25.9
25.4
25.6

24.6
29.7
34.0

12.5 (0.014)

48.3
38.4
35.6

24.5
26.7
22.8

27.2
34.9
41.6

54.9 (0.000)

26.5
24.5
22.3

25.3
31.8
33.3

9.8 (0.045)

44.4
38.3
43.2

24.7
26.4
13.6

30.9
35.4
43.2

20.3 (0.000)

24.8
26.3
25.3
25.8
25.7
25.4

39.4
29.9
26.3
21.2
27.3
35.2

23.7 (0.001)

34.6
40.4
49.8
58.7
42.9
31.8

25.4
25.6
24.6
22.2
25.1
25.5

40.0
33.9
25.6
19.1
32.0
42.7

80.6 (0.000)

marriage, age at first child birth and number of children


born during the last five and three years between rural
and urban areas. Because mean age at first marriage
and mean age at first birth are significantly younger in
rural areas (Table 1), rural women are susceptible to
pregnancy-related complications as the reproductive
organs are not properly developed at young age. All
pregnant women are at the risk of becoming anaemic as

2014 John Wiley & Sons Ltd

7.8 (0.020)

4.1 (0.131)

18.1 (0.000)

19.7 (0.000)

they need more iron and folic acid than usual. However, the risk is higher due to pregnancy at young age
and short birth intervals. Smoking and alcohol consumption are significantly more common in rural areas.
As smoking reduces absorption of essential nutrients
and alcohol consumption leads to poor nutrition, these
lifestyle characteristics are likely to aggravate severe
anaemia in rural areas.
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V. Perumal Reproductive risk factors of anaemia in pregnant women

Table 3 Significant reproductive risk factors for mild and moderate- to-severe anaemia among pregnant women in (a) urban areas and
(b) rural areas
95%
Confidence
limits
Anaemia
category*
(a) Urban areas
Mild

Moderate/
severe

(b) Rural areas


Mild

Moderate/
severe

Independent variables

Coefficient

Standard
error

Intercept
Education level- No
education
Primary
Secondary
Higher
BMI-under weight
Normal weight
Over weight
Obesity
Alcohol consumption
Pregnancy duration
Intercept
Education level- No
education
Primary
Secondary
Higher
BMI-under weight
Normal weight
Over weight
Obesity
Alcohol consumption
Pregnancy duration

0.95
0.32

0.33
0.19

0.19
0.23
1.00 (ref)
0.16
0.19
0.55
1.00 (ref)
0.54
0.07
2.96
0.87

Intercept
Wealth index Poorest
Poorer
Middle
Richer
Richest
Alcohol consumption
Smoking-yes
Age at first marriage
No. of births in the last five
years
Pregnancy duration
Mass media exposure
Intercept
Wealth index Poorest
Poorer
Middle
Richer
Richest
Alcohol consumption
Smoking-yes
Age at first marriage
No. of births in the last five
years
Pregnancy duration
Mass media exposure

Wald
statistics

Pvalue

Adjusted Odds
Ratio

Lower

Upper

8.10
2.79

0.004
0.095

1.38

0.95

2.01

0.22
0.16

0.74
1.97

0.389
0.161

1.21
1.25

0.78
0.91

1.87
1.72

0.32
0.29
0.32

0.24
0.42
3.03

0.627
0.515
0.081

0.85
0.83
0.57

0.45
0.47
0.31

1.60
1.46
1.07

0.68
0.03
0.45
0.19

0.62
7.87
42.49
20.01

0.430
0.005
0.000
0.000

0.58
1.08

0.15
1.02

2.23
1.14

2.38

1.63

3.49

0.40
0.36
1.00 (ref)
1.27
0.89
0.42
1.00 (ref)
0.75
0.21

0.23
0.17

3.02
4.36

0.082
0.037

1.49
1.44

0.95
1.02

2.35
2.03

0.43
0.41
0.43

8.55
4.66
0.95

0.003
0.031
0.330

3.57
2.44
1.53

1.52
1.08
0.65

8.38
5.48
3.58

0.46
0.03

2.63
58.51

0.105
0.000

2.12
1.23

0.85
1.17

5.26
1.30

0.80
0.26
0.14
0.08
0.01
1.00 (ref)
0.64
0.15
0.01
0.08

0.36
0.21
0.20
0.19
0.18

5.10
1.53
0.52
0.21
0.001

0.024
0.216
0.470
0.648
0.976

1.29
1.15
1.09
1.00

0.86
0.78
0.76
0.70

1.94
1.70
1.57
1.44

0.26
0.16
0.01
0.06

6.10
0.81
0.49
1.57

0.014
0.367
0.482
0.211

1.89
1.16
0.99
1.08

1.14
0.84
0.96
0.96

3.13
1.59
1.02
1.23

0.07
0.07
0.95
0.73
0.45
0.37
0.22
1.00 (ref)
0.50
0.37
0.04
0.25

0.02
0.03
0.35
0.21
0.21
0.20
0.20

13.68
4.03
7.18
11.59
4.85
3.60
1.26

0.000
0.045
0.007
0.001
0.028
0.058
0.261

1.08
0.93

1.04
0.87

1.12
1.00

2.07
1.57
1.45
1.25

1.36
1.05
0.99
0.85

3.14
2.35
2.14
1.83

0.25
0.15
0.01
0.06

4.23
6.26
8.62
16.92

0.040
0.012
0.003
0.000

1.66
1.44
0.96
1.28

1.02
1.08
0.93
1.14

2.68
1.92
0.98
1.44

0.17
0.09

0.02
0.03

76.00
7.52

0.000
0.006

1.18
0.91

1.14
0.85

1.23
0.97

*The reference category is normal.

848

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V. Perumal Reproductive risk factors of anaemia in pregnant women

The risk of developing moderate-to-severe anaemia is


20% higher among pregnant women in rural areas and
who married at <20 years than in urban areas (Figure 1).
Similarly, among the rural women who had more than
two child births in last five years, the risk is 40% higher
(Figure 2). Anaemia prevalence by gestation months
(Figure 3) indicates that there is a significant increase in
moderate-to-severe anaemia prevalence after 5 months of
gestation and that the risk doubles in the later stages of
pregnancy. During pregnancy, maternal blood volume
needs to increase to support the growth of the foetus,
particularly after the first trimester. If there is a lack of
iron or certain other nutrients, the pregnant woman
might not be able to produce the amount of red blood
cells needed to make this additional blood.
Multinomial logistic regression analysis showed that
for moderate-to-severe anaemia prevalence among pregnant women of urban areas, the variables such as BMI
category of underweight, normal weight and education
level up to secondary are significant risk factors. Among
reproductive and lifestyle variables, pregnancy duration is
the only risk factor for anaemia. However, in rural areas,
the most significant risk factors are smoking, alcohol
consumption, number of births in the last five years,
pregnancy duration and wealth index below middle category. Age at first marriage and mass media exposure are
significant protective factors. Socioeconomic factors
undoubtedly play a larger role in women empowerment
for health-seeking behaviour. However, poor women are
less likely to have formal education than wealthy women
and are less likely to be in good health. In almost all
societies, women are a socially disadvantaged group and
this universal social stigma, particularly in developing
countries such as India, cannot be wiped out in a short
time. Therefore, health education on the consequences of
early marriage and pregnancy should be strengthened at
the community level. Impact of health education through

45
40

available resources had been demonstrated in different


aspects. Ramesh et al. (1996) concluded that systematic
exposure to electronic media has a large effect on contraceptive use. Upadhyay et al. (2011) showed that calendars and video films are effective in increasing nutrition
knowledge of illiterate hill women. Long-term use of
mass media programmes is a prerequisite to combat the
nutritional problems of rural communities in India.
Although the National Anaemia Control Programme
(NACP) is fighting anaemia prevalence with multipronged strategies at national level, anaemia continues
to be a public health problem (WHO 2001) in India.
The increasing trend of moderate-to-severe anaemia may
not be fully due to non-availability and non-compliance
of Iron and Folic Acid tablets as highlighted in an
earlier study (Kalaivani 2009); it might be due to mushrooming of fast food and junk food eateries at least in
the last 10 years, particularly in urban areas. The
expansion of information technology created many
employment opportunities, and changes in working patterns (night/day shift) have become inevitable. Both factors together may lead people to consume food without
adequate iron content.
Pregnant women in rural areas may be unable to
attend regular antenatal check-up (ANC) at primary
health centres due to they cannot afford it, lack transport
or anticipate long waiting times. Pregnant women should
be registered at an early stage of pregnancy and health
personnel in the area should regularly conduct safe motherhood camps to counsel the women on proper diet and
provide them with supplemental iron tablets or syrup.
The strength of the present study is that it is based
on national sample representing 28 states of the country
and covering 94.5% of the target sample. The data
were collected by adopting rigorous sampling techniques
with a uniform method. Even though many studies
(Roy & Chakravorty 1992; Thangaleela &

Chi-square trend in proportion = 12.4; P < 0.01; OR = 1.6

Prevalence (%)

35
30
25
20
15
10
5

Mild

0
Figure 3 Prevalence (%) of anaemia by
gestation period.

2014 John Wiley & Sons Ltd

<=3

5
6
7
Gestation period (months)

Moderate/Severe
8

>=9

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V. Perumal Reproductive risk factors of anaemia in pregnant women

Vijayalakshmi 1994; Kapil et al. 1999; Toteja et al.


2006; Gautam et al. 2010; Panghal & Boora 2010;
Bisoi et al. 2011; Viveki et al. 2012) assessed the risk
factors for anaemia prevalence, they were either site
specific or had smaller samples. They also assumed that
socioeconomic status and cultural reproductive behaviours are similar between rural and urban areas, which
is not the case. Therefore, due to limitation of sample
sizes, their results varied vary widely. This study is a
robust and contemporary analysis of reproductive risk
factors quantified in terms of relative risk ratio.
Limitations of this study are that it was not possible to
assess the risk factors for anaemia due to other complications such as obstetrics/gynaecological related diseases,
malaria infection, soil-transmitted helminthic infections,
deworming status, history of blood transfusions, acute
febrile illnesses, cardiac disease, family history of thalassaemia and non-compliance to iron supplements.
Conclusion
The major root causes of anaemia early marriage leading to teenage pregnancy, short birth intervals, too many
child births, alcohol consumption and smoking habits
may be overcome through proper health education focusing on:
Stating the extent and effects of anaemia (dire consequences for reproductive health);
Using mass media, street plays and documentary film
to demonstrate how anaemia can be overcome;
Publicising success stories, preferably from the local
area.
Incorporating these in the existing NACP programme
and implementing the safe motherhood campaigns at the
door step are likely to reduce the anaemia prevalence
among pregnant women.
Acknowledgement
I am grateful to Dr. Alka Kriplani, Professor and HOD
of Obstetrics and Gynaecology, All India Institute of
Medical Sciences, New Delhi, for her support and
encouragement. The Director, IIPS, Mumbai, India, is
acknowledged for providing data to the present analysis.
I am also grateful for the support given by the authorities
of MEASURE DHS, ICF International, USA.
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Corresponding Author Vanamail Perumal, Department of Obstetrics and Gynaecology, All India Institute of Medical Sciences,
New Delhi 110029, India. E-mail: pvanamail@gmail.com

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