Skip to main content
PLOS One logoLink to PLOS One
. 2024 Jul 10;19(7):e0306183. doi: 10.1371/journal.pone.0306183

Anaemia among adolescent girls, pregnant and lactating women in the southern rural region of Bangladesh: Prevalence and risk factors

Gulshan Ara 1,2,*, Rafid Hassan 1, Md Ahshanul Haque 1, Anika Bushra Boitchi 3, Samira Dilruba Ali 1, Kazi Sudipta Kabir 1, Riad Imam Mahmud 4, Kazal Ahidul Islam 4, Hafizur Rahman 4, Zhahirul Islam 5
Editor: Biswajit Pal6
PMCID: PMC11236138  PMID: 38985720

Abstract

Anaemia is a major public health concern in developing countries, particularly among children, adolescents, and women of reproductive age. The study aimed to assess the anaemia status among adolescent girls, pregnant, and lactating women with their contributing factors in the southern rural regions of Bangladesh. This cross-sectional study was conducted among 400 adolescent girls, 375 pregnant, and 375 lactating women using a multistage cluster-random sampling technique. Anaemia was measured through haemoglobin concentration in blood capillaries collected with a Hemocue 301 machine. Multinomial logistic regression was used to determine the factors associated with anaemia. The average age of pregnant and lactating women was 24 years and 15.2 years for girls. Overall, the prevalence of anaemia was 50% among pregnant women, 46% among lactating women, and 38% among adolescent girls. The risk of anaemia among adolescent girls was higher among non-Muslim (aOR = 2.13, 95%CI:1.05–4.31), belonged to families having >5 members (aOR = 2.24, 95%CI:1.16–4.31) while exposure to media reduced their risk (aOR = 0.33, 95%CI:0.15–0.74). Pregnant women who consumed a diversified diet, washed their hands after toilet, and received ≥4 ANC visits had a lower likelihood of developing anaemia. Lactating women who were employed, consumed a diversified diet, washed their hands before preparing food, and after toilet, had been exposed to media, received ≥4 ANC visits, and consumed ≥90 IFA, had a lower risk of developing anaemia. However, anaemia was more likely to be associated with lactating women who were non-Muslim (aOR = 3.75; 95%CI:1.26–11.22). The high prevalence of anaemia emphasizes the need to reconsider the existing strategy for the prevention and control of micronutrient deficiencies in Bangladesh.

Introduction

Anaemia is a global public health concern affecting almost one-third of the world’s population [1]. This adverse health condition arises when the red blood cells count or the concentration of haemoglobin within them falls below normal [2]. It can appear at any stage of the human life cycle, impairing the oxygen supply to tissues. However, the increased physiological demand for iron during growth, menstruation, and pregnancy of adolescent girls and reproductive-aged women makes them more vulnerable to anaemia [36]. The global prevalence of anaemia is 38% and 29% among pregnant women and reproductive-aged women, respectively. Although the prevalence is heterogeneously distributed across the world, low- and middle-income countries (LMICs) bear a greater burden of anaemia [7].

A multifaceted etiology encompasses the development of anaemia. However, iron deficiency anaemia accounts for around half of all anaemic cases among women across the globe. Inadequate consumption or absorption of iron-rich foods, increased need for iron during the course of growth and pregnancy, menstrual iron loss, and intestinal parasite infections contribute to iron deficiency [5]. In addition, deficiencies in certain nutrients, including vitamin B12, folate, riboflavin, vitamin A, vitamin C, and copper, as well as protein-energy malnutrition, may lead to anaemia [2,3,6]. Anaemia can also be caused by a number of hereditary diseases including thalassemia, sickle cell anaemia, chronic inflammation, a lack of glucose-6-phosphate-dehydrogenase, and ovalocytosis [2]. Infectious diseases such as intestinal worm infestation, malaria, tuberculosis, AIDS, schistosomiasis, and tropical sprue can also contribute to anaemia [2,3]. Nevertheless, a wide range of aspects encompassing social, economic, demographic, political, ecological, biological, anthropometric, and lifestyle factors play an important role in developing anaemia [1,3,4,79].

Anaemia has a detrimental impact on maternal and child health. It impairs cognitive development and motor function during the early stages of growth and development [3]. Individuals suffering from anaemia experience fatigue and loss of productivity, which eventually yields poor work performance, producing a substantial economic burden to the family and nation [2,3]. Furthermore, severe anaemia increases the risk of morbidity and mortality, especially among pregnant and perinatal mothers, resulting in miscarriages, stillbirths, prematurity, and low birth weight babies [2]. The intergenerational transfer of poor iron pools from iron-deficient pregnant women to their children increases the risk of developing iron deficiency and anaemia in infants [3].

Anaemia is highly prevalent among children and women living in South Asia and Central and Western Africa [6]. Bangladesh is a South Asian developing country with a long history of struggling with anaemia [8]. In Bangladesh, anaemia affected around half of the adolescent girls (52%) [4], pregnant (50%) and lactating (49%) women [10]. According to the National Micronutrient Survey 2011–2012, only 4.8% of nonpregnant and nonlactating women (15–49 years of age) and 1.8% of school-going children suffered from iron deficiency anaemia, with approximately one-fifth of anaemic persons experiencing this condition [11]. Although the dietary intake of iron only met 8–18% of the recommended dietary allowances of children and women of reproductive age, the presence of high groundwater iron may have a salutary effect in lowering iron deficiency anaemia [9,11]. This lower prevalence of iron deficiency anaemia suggests other possible factors that could explain the occurrence of anaemia in Bangladesh. However, there is a scarcity of recent evidence of anaemia and its determinants among adolescent girls, pregnant, and lactating women in rural community settings of Bangladesh, especially in the southern region. This area, being climate-vulnerable, is more susceptible to micronutrient deficiencies. While there were numerous national surveys and studies on anaemia in Bangladesh, the majority of them were outdated [1218], had methodological issues [13], and were hospital-based [1922]. However, only a small number of these studies examined the factors contributing to anaemia in adolescent girls [4], reproductive aged nonpregnant women [8,23,24], pregnant women [21,20,25], and lactating women, for whom there was no conclusive evidence. Therefore, the present study aimed to investigate the prevalence of anaemia and its determinants among adolescent girls, pregnant, and lactating women in the southern rural region of Bangladesh.

Methods

Study design and participants

Max Foundation has been implementing a healthy village campaign program in "Max Nutri-WASH" Program areas in 62 Unions of five districts- Patuakhali, Barguna, Khulna, Jessore, and Satkhira on water, sanitation, and hygiene, nutrition, adolescent and women reproductive health. This cross-sectional study was conducted from November to December 2021 among the beneficiaries who were enlisted in the "Max Nutri-WASH" program in three southern districts (Khulna, Patuakhali, and Satkhira) of Bangladesh. The participants of the study were subdivided into three groups: adolescent girls (10–19 years), pregnant, and lactating women.

Sampling procedure and sample size

A multistage cluster random sampling technique was used to obtain a representative population sample in the three districts of "Max Nutri-WASH" program zones. During the first stage of sampling, three districts from the Max Nutri-WASH program area were randomly selected. In the second stage, out of 24 upazilas in the selected three districts, eight upazilas consisting of 23 unions were randomly chosen. A list of adolescent girls, pregnant and lactating women was prepared by a door-to-door screening of the illegible subjects. The next stage involved selecting a predetermined number of participants from each target group using a systematic sampling technique from that list. Due to inconsistent findings on prevalence and a lack of recent data, the sample size was determined by assuming a 50% prevalence of anaemia (p). We considered 95% confidence interval, 6% margin of error (d), 1.2 design effect, and 10% non-response rate. A total of 352 participants was determined as the sample size for each group using the following formula:

n=(Zα/2)2p(1p)d2xdesigneffect

However, the final sample size for this study was 375 pregnant and lactating women within both categories and 400 adolescent girls.

Data collection tools and procedures

A standard structured questionnaire following the questionnaire of the National Micronutrient Survey of Bangladesh, Bangladesh Demographic Health Survey was formulated to collect data from the study participants. It was developed in English and later translated into Bengali, keeping the meaning unchanged. Data were collected on sociodemographic, dietary, WASH, and reproductive history-related information from the participants. The research team trained the field staff on the questionnaire and relevant interview skills before collecting the data. They received comprehensive training on the Hemocue 301- haemoglobin measurement device. Soon after finishing the training, they pretested the questionnaire at a neighbouring location before starting the actual data collection. Written consent was obtained from each participant before conducting the interviews. Participants provided information through face-to-face interviews with the field staff based on the pre-tested questionnaire.

Haemoglobin measurement

The haemoglobin concentration in blood capillaries was measured using a Hemocue 301 machine (Hemocue AB, Angleholm, Sweden) to detect anaemia. A disposable lancet was used to puncture the fingertip of the middle, ring, or index finger after disinfection with 0.5% chlorohexidine gluconate. The exact first drop of blood was discarded. Gentle pressure was applied to extract the second drop. Once the blood drop appeared, the micro cuvette was immersed into it to allow capillary action to refill it with the blood specimen. Excess blood was wiped out from the edges of the microcuvettes with a piece of cotton. After turning on the hemocue photometer, the micro cuvette holder was drawn out. The blood-filled microcuvette was placed onto the holder, and the holder was stabilized. After 10–20 seconds, haemoglobin values appeared on the digital display.

Variables of the study

The outcome variable of the study was anaemia status where the WHO threshold for haemoglobin concentration to be considered anaemic (Hb <11 g/dL for pregnant women and Hb <12 g/dL for nonpregnant women) [23]. Based on Hb levels, anaemia was further divided into mild, moderate, and severe categories for pregnant (10.0 to 10.9 g/dL, 7.0–9.9 g/dL, and 7.0 g/dL, respectively), and nonpregnant women (11.0–11.9 g/dL, 8.0–10.9 g/dL, and 8.0 g/dL, respectively) [23].

The independent variables were included in this study: age of the participants, religion (muslim, and non-muslim), educational status (primary, secondary, and higher), employment status (employed, and unemployed), family size (<5 members, and ≥5 members), dietary diversity (<5 food groups, and ≥5 food groups), toilet facilities (improved, and unimproved), handwashing before food preparation, and after toilet (occasional, and always), media exposure (yes, and no), region (Patuakhali Sadar, Rangabali, Galachipa, Batiaghata, Dumuria, Satkhira Sadar, Tala, and Kalaroa). In addition, pregnant and lactating women were interviewed to collect information about their pregnancy conditions including pregnancy trimesters (1st trimester, 2nd trimester, and 3rd trimester), no of antenatal care (ANC) visit (1–3 times, and ≥4 times), and iron and folic acid supplementation (IFA) (IFA ≤90, IFA >90) during their current and previous pregnancies. The Minimum Dietary Diversity-Women (MDD-W) indicator was used to assess their dietary diversity, which was developed based on a preceding 24-hour dietary recall from a list of ten selected food groups, including grains/roots/tubers, pulses/legumes, nuts/seeds, dairy, eggs, meat/poultry/fish, dark green leafy vegetables, other vitamin A-rich fruits and vegetables, other fruit, and other vegetables. A diet was considered diversified if anyone consumed at least five of the ten food groups [26]. Media exposure was constructed based on whether the participants watched television, or listened to the radio, or read the newspaper during the last week of the survey [10]. The wealth index was constructed based on principal component analysis (PCA) of the key socioeconomic variables and classified households into poorest, poorer, middle, richer, and richest [27].

Ethical considerations

The institutional review board (IRB) of icddr,b approved the study (protocol # PR-21124). Prior to the interview, informed written consent was taken in the local language from the study participants (>18 years). Assent was taken from the adolescent girls whose age was below 18 years and subsequently, consent was obtained from their parents and caregivers. Participants who were illiterate provided consent by thumb impression. The research team described to the participants about background and objectives of the study, the voluntary nature of participation, and the future use of data. They were given assurance that confidentiality would be maintained for all the gathered information. None other than the investigators of this research, the Ethical Review Committee of icddr,b, and any law-enforcing agency in the event of necessity would have access to the information.

Statistical analysis

Descriptive statistics were applied to collectively describe background characteristics. The effect of each independent variable on the anaemia outcome (no anaemia, mild anaemia, and moderate or severe anaemia) was determined through bivariate and multivariate analyses. In the multivariate analysis, multinomial logistic regression models were used where the independent variables (with p<0.25 in the bivariate analysis and low multicollinearity) were taken into consideration [28]. The results are presented as adjusted odds ratios (AORs) along with 95% confidence intervals (CIs). p<0.05 were considered statistically significant. STATA 15 was used for all statistical analyses.

Results

Background characteristics

Table 1 presents the socioeconomic and demographic characteristics of the study participants. The mean age of the adolescent girls, pregnant, and lactating women was 15.2, 24.2, and 24.6 years, respectively. Most of the participants were Muslim, unemployed, and acquired secondary level education. Only 10% of the pregnant, and lactating women were employed. The average dietary diversity score was approximately 3.3 among the participants. Approximately 80% of all participants did not consume a diversified diet (five or more food groups). An equal proportion of adolescent girls and lactating women (approximately 63%) had improved toilet facilities, whereas only half of the pregnant women could avail themselves of the same facility in their households. In case of handwashing practice, over half of the participants always washed their hands before preparing food, and approximately 90% always washed their hands after using the toilet. Approximately 80% of pregnant women were in the second or third trimester of pregnancy. Among all pregnant women, 75% received ANC 1–3 times, and 23.4% consumed >90 IFA tablets. Almost half of lactating women received ANC check-ups 1–3 times during their last pregnancy, and 54% of them consumed >90 IFA tablets.

Table 1. Background characteristics of the study participants.

Variables Adolescent girls, n (%) Pregnant women, n (%) Lactating women, n (%)
Age
Mean (SD) 15.2 (1.7) 24.2 (5.5) 24.6 (5.6)
Religion
Muslim 299 (74.7) 303 (80.8) 292 (77.9)
Non-Muslim 101 (25.3) 72 (19.2) 83 (22.1)
Educational status
Primary 25 (6.3) 75 (20.0) 74 (19.8)
Secondary 336 (84.0) 217 (57.9) 224 (59.7)
Higher 39 (9.7) 83 (22.1) 77 (20.5)
Employment status
Employed 12 (3.0) 40 (10.7) 34 (9.1)
Unemployed 388 (97.0) 335 (89.3) 341(90.9)
Family members
Mean (SD) 4.7 (1.6) 4.6 (2.0) 5.6 (2.1)
<5 members 215 (53.7) 224 (59.7) 115 (30.7)
≥5 members 185 (46.3) 151 (40.3) 260 (69.3)
Dietary diversity
Mean (SD) 3.3 (1.5) 3.5 (1.6) 3.3 (1.4)
<5 food group 321 (80.2) 282 (75.2) 310 (82.7)
≥5 food groups 79 (19.8) 93 (24.8) 65 (17.3)
Toilet facilities
Improved 252 (63.0) 186 (49.6) 237 (63.2)
Unimproved 148 (37.0) 189 (50.4) 138 (36.8)
Washed hand before food preparation
Occasionally 186 (46.5) 173 (46.1) 157 (41.9)
Always 214 (53.5) 202 (53.9) 218 (58.1)
Washed hand after toilet
Occasionally 45 (11.3) 45 (12.0) 42 (11.2)
Always 355 (88.7) 330 (88.0) 333 (88.8)
Media exposure
Yes 346 (86.5) 295 (78.7) 304 (81.1)
No 54 (13.5) 80 (21.3) 71 (18.9)
Pregnancy trimester
1st trimester - 73 (19.4) -
2nd trimester - 160 (42.7) -
3rd trimester - 142 (37.9) -
No. of ANC visit
1–3 times - 250 (75.8) 211 (51.3)
≥4 times - 80 (24.2) 164 (43.7)
No. of IFA intake
IFA ≤90 - 206 (76.6) 173 (46.1)
IFA >90 - 63 (23.4) 202 (53.9)
Wealth index
Poorest 80 (20.0) 92 (24.5) 72 (19.2)
Poorer 85 (21.2) 63 (16.8) 73 (19.5)
Middle 77 (19.3) 67 (17.9) 83 (22.1)
Richer 78 (19.5) 75 (20.0) 78 (20.8)
Richest 80 (20.0) 78 (20.8) 69 (18.4)
Region
Patuakhali Sadar 61 (15.3) 57 (15.2) 58 (15.5)
Rangabali 30 (7.5) 31 (8.2) 32 (8.5)
Galachipa 53 (13.3) 42 (11.2) 44 (11.7)
Batiaghata 23 (5.7) 16 (4.3) 20 (5.3)
Dumuria 142 (35.5) 118 (31.5) 129 (34.4)
Satkhira Sadar 34 (8.5) 53 (14.1) 17 (4.6)
Tala 44 (11.0) 43 (11.5) 56 (14.9)
Kalaroa 13 (3.2) 15 (4.0) 19 (5.1)

n, number; %, percentage.

- no observation.

Prevalence of anaemia among study participants

The prevalence of anaemia among adolescent girls, pregnant, and lactating women was approximately 38%, 50%, and 46%, respectively. Lactating women (28%) were more likely to suffer from mild anaemia than pregnant women (25%), and adolescent girls (23%). However, a higher prevalence of moderate or severe anaemia was found among pregnant women (25%) than lactating women (17%), and adolescent girls (15%) (Fig 1).

Fig 1. Prevalence of anaemia among the study participants.

Fig 1

Risk factors of anaemia among adolescent girls

The multiple multinomial logistic analyses in Table 2 show the factors associated with anaemia among adolescent girls in this study. Non-Muslim adolescent girls had 2.1 (aOR = 2.13, 95% CI: 1.05–4.31, p = 0.036) times higher odds of being mildly anaemic than those who practised Islam. Participants who lived in families having ≥5 members were 2.24 times (aOR = 2.24, 95% CI: 1.16–4.31, p = 0.016) more likely to be moderately/severely anaemic than those who had smaller families (<5 members). Exposure to media reduced the risk of developing moderate or severe anaemia among adolescent girls by 67% (aOR = 0.33, 95% CI: 0.15–0.74, p = 0.006). Adolescent girls residing in Rangabali (aOR = 0.21, 95% CI: 0.06–0.79, p = 0.021), Dumuria (aOR = 0.25, 95% CI: 0.09–0.67, p = 0.006), and Tala (aOR = 0.10, 95% CI: 0.02–0.48, p = 0.004) had lower odds of being moderate or severe anaemia. Similarly, girls who lived in Rangabali (aOR = 0.31, 95% CI: 0.09–1.00, p = 0.049) and Dumuria (aOR = 0.37, 95% CI: 0.16–0.87, p = 0.023) had a lower likelihood of being mildly anaemic.

Table 2. Factors associated with anaemia among adolescent girls in Bangladesh (n = 400).

Characteristics Mild Anaemia Moderate/severe Anaemia
aOR [95%CI] p-value aOR [95%CI] p-value
Religion
Muslim Ref Ref
Non-Muslim 2.13 [1.05–4.31] 0.036 1.24 [0.48–3.19] 0.653
Family members
<5 members Ref Ref
≥5 members 1.09 [0.65–1.84] 0.732 2.24 [1.16–4.31] 0.016
Dietary diversity
<5 food group Ref Ref
≥5 food groups 1.35 [0.73–2.50] 0.340 0.65 [0.26–1.64] 0.364
Toilet facilities
Unimproved Ref Ref
Improved 0.61 [0.37–1.02] 0.062 0.80 [0.43–1.52] 0.501
Washed hand before
food preparation
Occasionally Ref Ref
Always 1.35 [0.80–2.29] 0.260 0.84 [0.45–1.57] 0.576
Media exposure
No Ref Ref
Yes 0.58 [0.27–1.23] 0.157 0.33 [0.15–0.74] 0.006
Wealth index
Poorest Ref Ref
Poorer 0.71 [0.32–1.57] 0.397 0.99 [0.40–2.47] 0.984
Middle 0.73 [0.33–1.64] 0.447 0.51 [0.18–1.45] 0.206
Richer 0.89 [0.40–1.95] 0.767 0.81 [0.30–2.14] 0.667
Richest 0.70 [0.31–1.58] 0.386 0.83 [0.30–2.28] 0.718
Region
Patuakhali Sadar Ref Ref
Rangabali 0.31 [0.09–1.00] 0.049 0.21 [0.06–0.79] 0.021
Galachipa 0.54 [0.21–1.37] 0.195 0.38 [0.13–1.07] 0.068
Batiaghata 0.30 [0.08–1.15] 0.079 0.28 [0.06–1.34] 0.111
Dumuria 0.37 [0.16–0.87] 0.023 0.25 [0.09–0.67] 0.006
Satkhira Sadar 0.53 [0.18–1.56] 0.247 0.67 [0.22–2.11] 0.499
Tala 0.36 [0.13–1.00] 0.050 0.10 [0.02–0.48] 0.004
Kalaroa 0.89 [0.19–4.21] 0.878 1.50 [0.33–6.92] 0.602

aOR: Adjusted odds ratio; Ref: Reference; CI: Confidence interval.

Risk factors of anaemia among pregnant women

Table 3 presents the factors associated with anaemia among pregnant women. Women with higher educational attainment were more likely to have mild anaemia than those with primary education (aOR = 4.72, 95% CI: 1.58–14.11; p = 0.006). Pregnant women who consumed a diversified diet (≥5 food groups) had an 86% lower likelihood of being mildly anaemic (aOR = 0.14, 95% CI: 0.05–0.37, p<0.001). The pregnant women who always washed their hands after using the toilet had a lower risk of suffering from mild (aOR = 0.23, 95% CI: 0.08–0.68, p = 0.008) and moderate or severe (aOR = 0.16, 95% CI: 0.06–0.44, p<0.001) anaemia than the women who washed their hands occasionally. Furthermore, pregnant women in their second and third trimesters had around 10 times (aOR = 9.66, 95% CI: 2.88–32.41; p<0.001) and 13 times (aOR = 13.49, 4.02–45.21; p<0.001) higher chances of developing mild anaemia, respectively, compared to those in the first trimester. However, higher odds of moderate to severe anaemia were also observed among women in their second (aOR = 9.48, 95% CI: 2.89–31.03; p<0.001), and third trimesters (aOR = 10.28, 3.07–34.44; p<0.001). Additionally, individuals who received ANC at least four times had a 65% (aOR = 0.35, 95% CI: 0.16–0.77, p = 0.009), and 76% (aOR = 0.24, 95% CI: 0.10–0.56, p = 0.001) lower likelihood of experiencing mild and moderate or severe anaemia, respectively. Furthermore, pregnant women who were in the wealthiest quintile were more likely than those in the lowest quintile to have mild anaemia (aOR = 3.61, 95% CI: 1.25–10.41; p = 0.017). Pregnant women living in Satkhira Sadar (aOR = 0.22, 95% CI: 0.06–0.79, p = 0.02), and Tala (aOR = 0.09, 95% CI: 0.02–0.49, p = 0.005) were more likely to be moderate or severe anaemic compared to those who live in Patuakhali Sadar.

Table 3. Factors associated with anaemia among pregnant women in Bangladesh (n = 375).

Characteristics
Mild Anaemia Moderate/severe Anaemia
aOR [95%CI] p-value aOR [95%CI] p-value
Educational status
Primary Ref Ref
Secondary 1.16 [0.46–2.88] 0.756 0.62 [0.27–1.44] 0.270
Higher 4.72 [1.58–14.11] 0.006 1.43 [0.47–4.31] 0.530
Dietary diversity
<5 food group Ref Ref
≥5 food groups 0.14 [0.05–0.37] <0.001 0.67 [0.32–1.42] 0.294
Toilet facilities
Unimproved Ref Ref
Improved 0.63 [0.32–1.25] 0.190 0.65 [0.31–1.34] 0.246
Washed hand after toilet
Occasionally Ref Ref
Always 0.23 [0.08–0.68] 0.008 0.16 [0.06–0.44] <0.001
Pregnancy trimester
1st trimester
2nd trimester 9.66 [2.88–32.41] <0.001 9.48 [2.89–31.03] <0.001
3rd trimester 13.49 [4.02–45.21] <0.001 10.28 [3.07–34.44] <0.001
No. of ANC visit
1–3 times Ref Ref
≥4 times 0.35 [0.16–0.77] 0.009 0.24 [0.10–0.56] 0.001
Wealth index
Poorest Ref Ref
Poorer 1.73 [0.58–5.14] 0.322 1.21 [0.41–3.55] 0.728
Middle 2.42 [0.85–6.88] 0.097 1.56 [0.56–4.39] 0.398
Richer 3.61 [1.25–10.41] 0.017 2.03 [0.68–6.07] 0.203
Richest 2.83 [0.95–8.45] 0.063 2.10 [0.70–6.34] 0.188
Region
Patuakhali Sadar Ref Ref
Rangabali 0.70 [0.15–3.23] 0.646 0.36 [0.08–1.60] 0.180
Galachipa 0.80 [0.24–2.63] 0.712 0.40 [0.11–1.41] 0.153
Batiaghata 1.09 [0.21–5.59] 0.919 1.84 [0.42–8.06] 0.418
Dumuria 0.88 [0.33–2.39] 0.809 0.69 [0.26–1.77] 0.436
Satkhira Sadar 0.47 [0.14–1.56] 0.216 0.22 [0.06–0.79] 0.020
Tala 0.36 [0.10–1.32] 0.124 0.09 [0.02–0.49] 0.005
Kalaroa 0.98 [0.16–6.06] 0.981 1.10 [0.22–5.41] 0.908

aOR: Adjusted odds ratio; Ref: Reference; CI: Confidence interval.

Risk factors of anaemia among lactating women

The factors related to anaemia among lactating women are shown in Table 4. Employment status was related to anaemia prevalence, with working women exhibiting reduced risk of moderate to severe anaemia (aOR = 0.06, 95% CI: 0.01–0.61; p = 0.017). Lactating women who consumed foods from five or more food groups had 72% (aOR = 0.28, 95% CI: 0.12–0.65; p = 0.003) and 92% (aOR = 0.08, 95% CI: 0.02–0.36; p = 0.001) lower odds of experiencing mild and moderate to severe anaemia, respectively. Handwashing practices also played a role, as regular hand washing before food preparation was associated with lower risk of mild anaemia (aOR = 0.37, 95% CI: 0.20–0.67; p = 0.001) than those who washed their hands occasionally. Furthermore, lactating women had lower odds of being moderately or severely anaemic if they always washed their hands after toilet usage (aOR = 0.27, 95% CI: 0.09–0.78; p = 0.016). Exposure to media decreased the likelihood of moderate to severe anaemia among lactating mothers (aOR = 0.35, 95% CI: 0.15–0.85; p = 0.020). Both mild and moderate to severe anaemia was negatively associated with ANC visits and IFA intake. Lactating women who received four or more ANC visits during their last pregnancy had 70% lower odds of mild (aOR = 0.30, 95% CI: 0.17–0.55; p<0.001) and moderate to severe anaemia (aOR = 0.28, 95% CI: 0.13–0.58; p<0.001). In terms of their IFA intake, those who consumed more than 90 tablets had a 55% (aOR = 0.45, 95% CI: 0.25–0.79; p = 0.005) lower chance of having mild anaemia and an 81% (aOR = 0.19, 95% CI: 0.09–0.39; p<0.001) lower chance of having moderate or severe anaemia. Residence in certain areas also impacted anaemia prevalence among lactating women. Those residing in Rangabali, Galachipa, Dumuria, and Kalaroa had lower odds of mild anaemia, while Rangabali and Dumuria residents had higher odds of moderate to severe anaemia. Non-Muslim lactating women had 3.8 times (aOR = 3.75, 95% CI: 1.26–11.22; p = 0.018) higher likelihood of having moderate-to-severe anaemia than Muslim women. In addition, lactating women in the middle wealth quintile had 3.3 times (aOR = 3.26, 95% CI: 1.35–7.89; p = 0.009) higher odds of being mildly anaemic.

Table 4. Factors associated with anaemia among lactating women in Bangladesh (n = 375).

Characteristics
Mild Anaemia Moderate/severe Anaemia
aOR [95%CI] p-value aOR [95%CI] p-value
Educational status
Primary Ref Ref
Secondary 0.90 [0.41–1.99] 0.803 0.58 [0.23–1.46] 0.246
Higher 0.95 [0.34–2.65] 0.926 0.74 [0.22–2.43] 0.618
Employment status
Unemployed Ref Ref
Employed 0.64 [0.22–1.84] 0.407 0.06 [0.01–0.61] 0.017
Religion
Muslim Ref Ref
Non-Muslim 2.18 [0.92–5.14] 0.076 3.75 [1.26–11.22] 0.018
Family members
<5 members Ref Ref
≥5 members 1.40 [0.75–2.60] 0.287 0.88 [0.42–1.83] 0.725
Dietary diversity
<5 food group Ref Ref
≥5 food groups 0.28 [0.12–0.65] 0.003 0.08 [0.02-.0.36] 0.001
Toilet facilities
Unimproved Ref Ref
Improved 1.01 [0.56–1.82] 0.975 0.72 [0.35–1.46] 0.363
Washed hand before food preparation
Occasionally Ref Ref
Always 0.37 [0.20–0.67] 0.001 0.78 [0.37–1.65] 0.515
Washed hand after toilet
Occasionally Ref Ref
Always 0.72 [0.27–1.91] 0.514 0.27 [0.09–0.78] 0.016
Media exposure
No Ref Ref
Yes 0.72 [0.33–1.57] 0.405 0.35 [0.15–0.85] 0.020
No. of ANC visit
1–3 times Ref Ref
≥4 times 0.30 [0.17–0.55] <0.001 0.28 [0.13–0.58] 0.001
No. of IFA intake
IFA ≤90 Ref Ref
IFA >90 0.45 [0.25–0.79] 0.005 0.19 [0.09–0.39] <0.001
Wealth index
Poorest Ref Ref
Poorer 1.24 [0.51–3.05] 0.634 0.64 [0.21–1.94] 0.427
Middle 3.26 [1.35–7.89] 0.009 2.05 [0.70–6.05] 0.192
Richer 1.83 [0.70–4.79] 0.221 2.87 [0.93–8.89] 0.067
Richest 1.61 [0.58–4.52] 0.363 2.72 [0.79–9.37] 0.113
Region
Patuakhali Sadar Ref Ref
Rangabali 0.14 [0.04–0.50] 0.003 0.19 [0.05–0.81] 0.024
Galachipa 0.24 [0.08–0.71] 0.01 0.33 [0.09–1.16] 0.083
Batiaghata 2.51 [0.49–12.78] 0.268 2.31 [0.28–18.79] 0.435
Dumuria 0.24 [0.09–0.61] 0.003 0.16 [0.05–0.58] 0.005
Satkhira Sadar 0.29 [0.07–1.21] 0.089 0.36 [0.05–2.52] 0.306
Tala 0.45 [0.16–1.25] 0.126 0.69 [0.20–2.44] 0.568
Kalaroa 0.16 [0.03–0.82] 0.028 0.39 [0.07–2.18] 0.282

aOR: Adjusted odds ratio; Ref: Reference; CI: Confidence interval.

Discussion

Anaemia is still a major cause of public health concern in Bangladesh. The current study aimed to determine the prevalence of anaemia among adolescent girls, pregnant, and lactating women in the southern rural region of the country. Furthermore, it aimed to identify the potential risk factors associated with anaemia in these specific population groups. Anaemia was prevalent among 38% of adolescent girls, 50% of pregnant women, and 46% of lactating mothers. According to the study, the following factors were associated with anaemia: among adolescent girls, religion, family members, media exposure, and region; among pregnant women, dietary diversity, handwashing after using the toilet, pregnancy trimester, number of ANC visits, and region. Employment status, religion, dietary diversity, handwashing practices, media exposure, number of ANC visits, IFA intake, and region were found to be associated factors among lactating women.

The prevalence of anaemia among adolescent girls was nearly concordant with previous studies conducted in Bangladesh (43%) [4], and Nepal (38%) [29]. Conversely, this study found comparatively lower prevalence when compared to the prevalence rates reported in studies from Bangladesh (48–52%) [4,10], India (48–85%), Sri Lanka (58.1%) [4], Nepal (52–66%) [29]. In case of pregnant women, anaemia prevalence was almost comparable with the earlier findings, in Bangladesh (50–56%) [10,30]. However, the findings were in contrast to several studies conducted in Bangladesh (37%, 40%, 59%, 63%) [21], Ethiopia (23%) [31], Bhutan, Sri Lanka, Nepal (59–65%) [22], India (87%) [32]. Similarly, high prevalence of anaemia among lactating women was noticed in many studies conducted in Bangladesh (48%) [10], Sierra Leone (53%) [33], Mozambique (53%), Tanzania (46%), Kenia (44%) [3]. Conversely, a lower prevalence also observed in East Africa (36%), Rwanda (19%) [34], and Ethiopia (22%) [28]. Regarding the levels of anaemia status, moderate to severe anaemia was more prevalent among pregnant, and lactating women than adolescent girls. This finding was comparable with the recent Bangladesh Demographic Health Survey [10]. A difference in the prevalence of anaemia between and within countries has been shown. However, the variation might be due to differences in sociodemographic and cultural issues, dietary patterns, study design and methodology, and time differences of the studies [7,35].

Sociodemographic characteristics play a significant role in determining anaemia. Likewise, in other studies, lactating mothers who were employed had lower odds of having anaemia [28,34]. This might be due to their better decision-making autonomy resulting from their financial contributions to family, which empowered them to purchase a variety of foods and seek health facilities [28]. Besides, adolescent girls who had a family size of five and more were more likely to have moderate/severe anaemia, which was consistent with earlier studies [36,37]. The inability to afford micronutrient-rich foods in large families, coupled with low care, could be the possible cause [36]. This study also observed reduced likelihood of moderate to severe anaemia among adolescent girls and lactating women who had exposure to mass media. The importance of mass media was also acknowledged in earlier studies in reducing the risk of anaemia [38,39]. Mass media is considered a good source of receiving wider information regarding health-related programs which helps to increase nutrition knowledge and proper utilization of health care services and encourages women to intake diversified nutritious meals, and iron and folic acid supplements [39,40]. In our study, adolescent girls and lactating women from non-Muslim families had a considerably higher likelihood of developing anaemia than Muslims. This result was consistent with other studies conducted in Bangladesh [8], and India [32]. This difference in anaemia across religions may be due to different dietary practices and food taboos [32]. The bioavailability of dietary iron might fluctuate within particular religious communities due to distinct belief regarding food consumption, which limit their consumption of iron-rich foods [41]. The majority of non-Muslims in Bangladesh are Hindus, and most of them follow a vegetarian diet. In contrast, Muslims in this country consume more foods from animal sources than non-Muslims [8].

Inappropriate dietary habits may contribute to the development of anaemia, where low dietary diversity plays a significant role. In our study, anaemia among pregnant and lactating women was linked to the consumption of an inadequate diversified diet, which was consistent with earlier studies [31,42]. The physiological state of highly demanding nutrients during pregnancy and lactation suggests that women should consume a diversified diet to achieve nutrient adequacy to prevent the development of micronutrient-deficient anaemia [31].

Water, sanitation, and hygiene (WASH) practices are considered one of the interventions for the prevention and control of anaemia [7]. Particularly in Bangladesh, due to the tropical temperature, improper hand washing practices after excretion, before preparing meals or consuming food, and using unsanitary latrines could result in gastrointestinal parasitic infestation [8,39,4345]. Poor general health and/or chronic blood loss through gastrointestinal parasite infestation can be considered for the association of the unhygienic practice of using toilets with developing anaemia [8]. An earlier study revealed a higher prevalence of anaemia among adolescent girls, with approximately 32% of anaemic individuals found to be infected with intestinal parasites, compared to 30.6% of non-anemic cases [44]. A multi-country study among women of reproductive age in Bangladesh, Maldives, and Nepal found that access to safe drinking water seemed to be protective factor for lowering the cases of anaemia among women in Nepal, and Bangladesh [23]. In the current study, we found that frequent handwashing after using toilets and before food preparation decreased the likelihood of developing anaemia among pregnant and lactating women.

Align with earlier studies, our study found that pregnant and lactating women who received ANC ≥4 times during their pregnancy had a lower risk of being anaemic [42,46]. This may be due to a routine diagnosis of anaemia during the ANC visit and scheduled counselling on nutrition-related knowledge, supplementation and treatment [42]. We found a negative association between IFA intake and anaemia among lactating women during their preceding pregnancy. A study conducted in India found that IFA supplementation was similarly inversely related to the incidence of anaemia, with regular use of IFA or folic acid supplements in the preceding trimester leading to a 74% decreased risk of anaemia [47]. WHO strongly recommends daily supplementation of oral iron and folic acid to reduce the risk of anaemia during pregnancy and prevent the occurrence of low birth weight [2]. During pregnancy, anaemia can act as a risk factor and impose life-threatening consequences on the mother as well as the foetus [48]. This is likely because of the depletion of iron reserves as pregnancy develops, which further increases the requirement for iron, especially during the second and third trimesters [49]. During pregnancy, particularly after the first trimester, there is a need for the maternal blood volume to expand to support foetal growth. A previous study found that the prevalence of moderate to severe anaemia increased significantly after five months of gestation and that the risk was amplified in the later stages of pregnancy [38]. In the present study, women in the second and third pregnancy trimesters were more likely to be anaemic, which aligns with earlier studies conducted in Bangladesh [22], Cameroon [44], and Ethiopia [31].

However, the study has some limitations, including the inability to diagnose iron deficiency anaemia due to the lack of data on absolute dietary iron consumption or serum ferritin levels. Being cross-sectional in nature, the data should be utilized with caution when interpreting the temporal association between sociodemographic and anaemia. Additionally, we did not collect information on further health issues, including a family history of thalassemia, a malaria infection, an obstetrical issue, helminth infections, etc. Our understanding would be improved by supplementary research on these topics; therefore, extensive investigation into the causes of anaemia is required to identify the most appropriate measures. Attention must be paid to the high prevalence of anaemia in adolescent girls, pregnant and lactating women. To improve the status of anaemia in these vulnerable populations in the southern area of Bangladesh, dietary diversity, supplementation with multiple micronutrients, and social behaviour change communication should be advocated.

Conclusion

Our study acknowledges the importance of addressing anaemia as a major health concern among adolescent girls, pregnant and lactating women in Bangladesh. Socioeconomic conditions dietary diversity, pregnancy status, antenatal care, IFA intake, and WASH practices contribute to the development of anaemia. Even though the national strategy to control and prevent anaemia in Bangladesh encompasses a wide range of interventions, the implementation lacks strategic grounds. Thus, it is essential to understand the gap and introduce effective sustainable solutions to improve diet quality along with measures to control parasitic infestations in addition to running massive supplementation programs and awareness campaigns.

Supporting information

S1 File. Survey questionnaire.

(PDF)

pone.0306183.s001.pdf (816.3KB, pdf)
S1 Dataset. Dataset of adolescent girls.

(XLS)

pone.0306183.s002.xls (177.5KB, xls)
S2 Dataset. Dataset of pregnant women.

(XLS)

pone.0306183.s003.xls (183.5KB, xls)
S3 Dataset. Dataset of lactating women.

(XLS)

pone.0306183.s004.xls (178KB, xls)

Data Availability

All relevant data are within the paper and its Supporting Information files.

Funding Statement

Gulshan Ara received funding from Max Foundation, Bangladesh to conduct this study. The grant number was GR-02137. URL of funder website: https://maxfoundation.org/country/bangladesh/ The funders did not play any role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

References

  • 1.Sunuwar DR, Singh DR, Chaudhary NK, Pradhan PMS, Rai P, Tiwari K. Prevalence and factors associated with anemia among women of reproductive age in seven South and Southeast Asian countries: Evidence from nationally representative surveys. PLoS One. 2020. Aug 13;15(8):e0236449. doi: 10.1371/journal.pone.0236449 ; PMCID: PMC7425935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.World Health Organization. Global nutrition targets 2025: anaemia policy brief(WHO/NMH/NHD/ 14.4). Geneva: World Health Organization. 2014. [Google Scholar]
  • 3.Balarajan Y, Ramakrishnan U, Ozaltin E, Shankar AH, Subramanian SV. Anaemia in low-income and middle-income countries. Lancet. 2011. Dec 17;378(9809):2123–35. doi: 10.1016/S0140-6736(10)62304-5 Epub 2011 Aug 1. . [DOI] [PubMed] [Google Scholar]
  • 4.Mistry SK, Jhohura FT, Khanam F, Akter F, Khan S, Yunus FM, et al. An outline of anemia among adolescent girls in Bangladesh: findings from a cross-sectional study. BMC Hematol. 2017. Aug 22;17:13. doi: 10.1186/s12878-017-0084-x ; PMCID: PMC5568267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Tolentino K, Friedman JF. An update on anemia in less developed countries. Am J Trop Med Hyg. 2007. Jul;77(1):44–51. . [PubMed] [Google Scholar]
  • 6.World health organization. Worldwide prevalence of anemia 1993–2005. WHO Global Database on Anemia. Geneva: World health organization; 2008. [Google Scholar]
  • 7.Gautam S, Min H, Kim H, Jeong HS. Determining factors for the prevalence of anemia in women of reproductive age in Nepal: Evidence from recent national survey data. PLoS One. 2019. Jun 12;14(6):e0218288. doi: 10.1371/journal.pone.0218288 ; PMCID: PMC6561639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Kamruzzaman M, Rabbani MG, Saw A, Sayem MA, Hossain MG. Differentials in the prevalence of anemia among non-pregnant, ever-married women in Bangladesh: multilevel logistic regression analysis of data from the 2011 Bangladesh Demographic and Health Survey. BMC Womens Health. 2015. Jul 29;15:54. doi: 10.1186/s12905-015-0211-4 ; PMCID: PMC4517492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Rahman S, Ahmed T, Rahman AS, Alam N, Ahmed AS, Ireen S, et al. Determinants of iron status and Hb in the Bangladesh population: the role of groundwater iron. Public Health Nutr. 2016. Jul;19(10):1862–74. doi: 10.1017/S1368980015003651 Epub 2016 Jan 28. ; PMCID: PMC10270950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.NIPORT, Mitra and Associates, ICF International. Bangladesh Demographic and Health Survey, 2011. NIPORT, Mitra & Associates and ICF International, Dhaka, Bangladesh and Calverton, MD, USA. 2013. [Google Scholar]
  • 11.International Centre for Diarrheal Disease Research Bangladesh (icddr,b), United Nations Children’s Fund (UNICEF), Global Alliance for Improved Nutrition (GAIN), and Institute of Public Nutrition. National Micronutrients Status Survey 2011–12: Final Report. Dhaka, Bangladesh: Centre for Nutrition and Food Security, icddr,b. 2013. [Google Scholar]
  • 12.Ahmed F, Prendiville N, Narayan A. Micronutrient deficiencies among children and women in Bangladesh: progress and challenges. J Nutr Sci. 2017. Jan 3;5:e46. doi: 10.1017/jns.2016.39 ; PMCID: PMC5465809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Jamil KM, Rahman AS, Bardhan PK, Khan AI, Chowdhury F, Sarker SA, et al. Micronutrients and anaemia. J Health Popul Nutr. 2008. Sep;26(3):340–55. doi: 10.3329/jhpn.v26i3.1900 ; PMCID: PMC2740705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Ahmed F, Khan MR, Islam M, Kabir I, Fuchs GJ. Anaemia and iron deficiency among adolescent schoolgirls in peri-urban Bangladesh. Eur J Clin Nutr. 2000. Sep;54(9):678–83. doi: 10.1038/sj.ejcn.1601073 . [DOI] [PubMed] [Google Scholar]
  • 15.Ahmed F, Mahmuda I, Sattar A, Akhtaruzzaman M. Anaemia and vitamin A deficiency in poor urban pregnant women of Bangladesh. Asia Pac J Clin Nutr. 2003;12(4):460–6. . [PubMed] [Google Scholar]
  • 16.Hyder SZ, Persson Lk, Chowdhury A, Ekström EC. Anaemia among non-pregnant women in rural Bangladesh. Public Health Nutr. 2001. Feb;4(1):79–83. doi: 10.1079/phn200055 . [DOI] [PubMed] [Google Scholar]
  • 17.Hyder SM, Persson LA, Chowdhury M, Lönnerdal BO, Ekström EC. Anaemia and iron deficiency during pregnancy in rural Bangladesh. Public Health Nutr. 2004. Dec;7(8):1065–70. doi: 10.1079/PHN2004645 . [DOI] [PubMed] [Google Scholar]
  • 18.Bhargava A, Bouis HE, Scrimshaw NS. Dietary intakes and socioeconomic factors are associated with the hemoglobin concentration of Bangladeshi women. J Nutr. 2001. Mar;131(3):758–64. doi: 10.1093/jn/131.3.758 . [DOI] [PubMed] [Google Scholar]
  • 19.Rim MT, Ghosh A, Khatun AA, Awal MS. ANAEMIA AMONG THE ADOLESCENT, NON-PREGNANT AND PREGNANT WOMEN IN THE RURAL NORTHERN BANGLADESH. Bangladesh Journal of Multidisciplinary Scientific Research. 2022. Aug 12;5(1):21–30. [Google Scholar]
  • 20.Alam F, Khanum S, Jahan I, Ahmed JU. Prevalence and sociodemographic factors responsible for anaemia in pregnancy: experience in a military hospital in Bangladesh. BIRDEM Medical Journal. 2021;11(1):52–6. [Google Scholar]
  • 21.Sabina Azhar B, Islam MS, Karim MR. Prevalence of anemia and associated risk factors among pregnant women attending antenatal care in Bangladesh: a cross-sectional study. Prim Health Care Res Dev. 2021. Nov 3;22:e61. doi: 10.1017/S146342362100061X ; PMCID: PMC8569827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Chowdhury HA, Ahmed KR, Jebunessa F, Akter J, Hossain S, Shahjahan M. Factors associated with maternal anaemia among pregnant women in Dhaka city. BMC Womens Health. 2015. Sep 22;15:77. doi: 10.1186/s12905-015-0234-x ; PMCID: PMC4580087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Rahman MA, Rahman MS, Aziz Rahman M, Szymlek-Gay EA, Uddin R, Islam SMS. Prevalence of and factors associated with anaemia in women of reproductive age in Bangladesh, Maldives and Nepal: Evidence from nationally-representative survey data. PLoS One. 2021. Jan 7;16(1):e0245335. doi: 10.1371/journal.pone.0245335 ; PMCID: PMC7790421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Jana A, Chattopadhyay A, Saha UR. Identifying risk factors in explaining women’s anaemia in limited resource areas: evidence from West Bengal of India and Bangladesh. BMC Public Health. 2022. Jul 28;22(1):1433. doi: 10.1186/s12889-022-13806-5 ; PMCID: PMC9330636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Ahmed F, Khan MR, Shaheen N, Ahmed KMU, Hasan A, Chowdhury IA, et al. Anemia and iron deficiency in rural Bangladeshi pregnant women living in areas of high and low iron in groundwater. Nutrition. 2018. Jul-Aug;51–52:46–52. doi: 10.1016/j.nut.2018.01.014 Epub 2018 Feb 9. . [DOI] [PubMed] [Google Scholar]
  • 26.FAO. 2021. Minimum dietary diversity for women. Rome. doi: 10.4060/cb3434en [DOI]
  • 27.Vyas S, Kumaranayake L. Constructing socio-economic status indices: how to use principal components analysis. Health Policy Plan. 2006. Nov;21(6):459–68. doi: 10.1093/heapol/czl029 Epub 2006 Oct 9. . [DOI] [PubMed] [Google Scholar]
  • 28.Lakew Y, Biadgilign S, Haile D. Anaemia prevalence and associated factors among lactating mothers in Ethiopia: evidence from the 2005 and 2011 demographic and health surveys. BMJ Open. 2015. Apr 14;5(4):e006001. doi: 10.1136/bmjopen-2014-006001 ; PMCID: PMC4401847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Chalise B, Aryal KK, Mehta RK, Dhimal M, Sapkota F, Mehata S, et al. Prevalence and correlates of anemia among adolescents in Nepal: Findings from a nationally representative cross-sectional survey. PLoS One. 2018. Dec 14;13(12):e0208878. doi: 10.1371/journal.pone.0208878 ; PMCID: PMC6294609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Nessa Z, Rahman ML, Yesmin S, Rahman MH, Rahim CFMM. A study on prevalence of Anaemia in pregnancy among the women reporting for Antenatal care in combined Military Hospital, Dhaka Cantonment. J Dhaka Med Coll. 2017;26(2):103–10. doi: 10.3329/jdmc.v26i2.38824 [DOI] [Google Scholar]
  • 31.Lebso M, Anato A, Loha E. Prevalence of anemia and associated factors among pregnant women in Southern Ethiopia: A community based cross-sectional study. PLoS One. 2017. Dec 11;12(12):e0188783. doi: 10.1371/journal.pone.0188783 ; PMCID: PMC5724831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Lokare PO, Karanjekar VD, Gattani PL, Kulkarni AP. A study of prevalence of anemia and sociodemographic factors associated with anemia among pregnant women in Aurangabad city, India. Annals of Nigerian Medicine. 2012;6(1):30–4. [Google Scholar]
  • 33.Arinda IK, Sserwanja Q, Kamara K, Mukunya D, Agnes N, Edirisa Juniour N, et al. Anemia and Associated Factors Among Lactating Women in Sierra Leone: An Analysis of the Sierra Leone Demographic and Health Survey 2019. Nutr Metab Insights. 2022. Jun 16;15:11786388221105732. doi: 10.1177/11786388221105732 ; PMCID: PMC9208047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Abdelbagi OM, Hassan B, Eltayeb R, ALhabardi N, Adam I. Prevalence of anaemia and its associated factors among lactating mothers in eastern Sudan: a cross-sectional study. Trans R Soc Trop Med Hyg. 2022. Dec 2;116(12):1123–1128. doi: 10.1093/trstmh/trac037 . [DOI] [PubMed] [Google Scholar]
  • 35.Worku MG, Alamneh TS, Teshale AB, Yeshaw Y, Alem AZ, Ayalew HG, et al. Multilevel analysis of determinants of anemia among young women (15–24) in sub-Sahara Africa. PLoS One. 2022. May 9;17(5):e0268129. doi: 10.1371/journal.pone.0268129 ; PMCID: PMC9084531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Tesfaye M, Yemane T, Adisu W, Asres Y, Gedefaw L. Anemia and iron deficiency among school adolescents: burden, severity, and determinant factors in southwest Ethiopia. Adolesc Health Med Ther. 2015. Dec 15;6:189–96. doi: 10.2147/AHMT.S94865 ; PMCID: PMC4687608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Tirore LL, Mulugeta A, Belachew AB, Gebrehaweria M, Sahilemichael A, Erkalo D, et al. Factors associated with anaemia among women of reproductive age in Ethiopia: Multilevel ordinal logistic regression analysis. Matern Child Nutr. 2021. Jan;17(1):e13063. doi: 10.1111/mcn.13063 Epub 2020 Aug 5. ; PMCID: PMC7729796. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Perumal V. Reproductive risk factors assessment for anaemia among pregnant women in India using a multinomial logistic regression model. Trop Med Int Health. 2014. Jul;19(7):841–51. doi: 10.1111/tmi.12312 Epub 2014 Apr 7. . [DOI] [PubMed] [Google Scholar]
  • 39.Keokenchanh S, Kounnavong S, Tokinobu A, Midorikawa K, Ikeda W, Morita A, et al. Prevalence of Anemia and Its Associate Factors among Women of Reproductive Age in Lao PDR: Evidence from a Nationally Representative Survey. Anemia. 2021. Jan 15;2021:8823030. doi: 10.1155/2021/8823030 ; PMCID: PMC7822650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Chourasia A, Pandey CM, Awasthi A. Factors influencing the consumption of iron and folic acid supplementations in high focus states of India. Clin Epidemiol Glob Heal. 2017. Dec 1;5(4):180–4. doi: 10.1016/j.cegh.2017.04.004 [DOI] [Google Scholar]
  • 41.Madjdian DS, Azupogo F, Osendarp SJ, Bras H, Brouwer ID. Socio-cultural and economic determinants and consequences of adolescent undernutrition and micronutrient deficienceis in LMICs: a systematic narrative review. Ann N Y Acad Sci. 2018. Mar;1416(1):117–39. doi: 10.1111/nyas.13670 [DOI] [Google Scholar]
  • 42.Jugha VT, Anchang-Kimbi JK, Anchang JA, Mbeng KA, Kimbi HK. Dietary Diversity and Its Contribution in the Etiology of Maternal Anemia in Conflict Hit Mount Cameroon Area: A Cross-Sectional Study. Front Nutr. 2021. Feb 4;7:625178. doi: 10.3389/fnut.2020.625178 ; PMCID: PMC7889504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Siva PM, Sobha A, Manjula VD. Prevalence of Anaemia and Its Associated Risk Factors Among Adolescent Girls of Central Kerala. J Clin Diagn Res. 2016. Nov;10(11):LC19–LC23. doi: 10.7860/JCDR/2016/20939.8938 Epub 2016 Nov 1. ; PMCID: PMC5198362. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Banu H, Khanum H, Hossain MA. Relationships between anaemia and parasitic infections in adolescent girls of Bangladesh. Bangladesh J Zool. 2014;42(1): 91–103. doi: 10.3329/bjz.v42i1.23340 [DOI] [Google Scholar]
  • 45.Kothari MT, Coile A, Huestis A, Pullum T, Garrett D, Engmann C. Exploring associations between water, sanitation, and anemia through 47 nationally representative demographic and health surveys. Ann N Y Acad Sci. 2019. Aug;1450(1):249–267. doi: 10.1111/nyas.14109 Epub 2019 Jun 24. ; PMCID: PMC6771505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Mihiretu A. Factors associated with anemia among lactating mothers in subsistence farming households from selected districts of Jimma zone, south western Ethiopia: a community based cross-sectional study. Journal of Nutrition and Food Sciences. 2017;7(3). doi: 10.4172/2155-9600.1000595 [DOI] [Google Scholar]
  • 47.Varghese JS, Swaminathan S, Kurpad AV, Thomas T. Demand and supply factors of iron-folic acid supplementation and its association with anaemia in North Indian pregnant women. PLoS One. 2019. Jan 30;14(1):e0210634. doi: 10.1371/journal.pone.0210634 ; PMCID: PMC6353128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Pappas G, Akhtar T, Gergen PJ, Hadden WC, Khan AQ. Health status of the Pakistani population: a health profile and comparison with the United States. Am J Public Health. 2001. Jan;91(1):93–8. doi: 10.2105/ajph.91.1.93 ; PMCID: PMC1446517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Barrett JF, Whittaker PG, Williams JG, Lind T. Absorption of non-haem iron from food during normal pregnancy. BMJ. 1994. Jul 9;309(6947):79–82. doi: 10.1136/bmj.309.6947.79 ; PMCID: PMC2540564. [DOI] [PMC free article] [PubMed] [Google Scholar]

Decision Letter 0

Biswajit Pal

16 Jan 2024

PONE-D-23-35666Anaemia among adolescent girls, pregnant and lactating women in the south coastal region of Bangladesh: prevalence and risk factorsPLOS ONE

Dear Dr. Ara,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Please submit your revised manuscript by Mar 01 2024 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

  • A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.

  • A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.

  • An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Biswajit Pal, M.SC., Ph.D

Academic Editor

PLOS ONE

Journal Requirements:

When submitting your revision, we need you to address these additional requirements.

1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at 

https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and 

https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf

2. Note from Emily Chenette, Editor in Chief of PLOS ONE, and Iain Hrynaszkiewicz, Director of Open Research Solutions at PLOS: Did you know that depositing data in a repository is associated with up to a 25% citation advantage (https://doi.org/10.1371/journal.pone.0230416)? If you’ve not already done so, consider depositing your raw data in a repository to ensure your work is read, appreciated and cited by the largest possible audience. You’ll also earn an Accessible Data icon on your published paper if you deposit your data in any participating repository (https://plos.org/open-science/open-data/#accessible-data).

3.  In the online submission form, you indicated that [The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.]. 

All PLOS journals now require all data underlying the findings described in their manuscript to be freely available to other researchers, either 1. In a public repository, 2. Within the manuscript itself, or 3. Uploaded as supplementary information.

This policy applies to all data except where public deposition would breach compliance with the protocol approved by your research ethics board. If your data cannot be made publicly available for ethical or legal reasons (e.g., public availability would compromise patient privacy), please explain your reasons on resubmission and your exemption request will be escalated for approval. 

Additional Editor Comments:

The study was conducted in Max Nutri WASH program zones but the present title of the research generalizes the issue. Kindly reconsider the title.

Kindly address the issues raised by the reviewers.

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: No

Reviewer #2: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The manuscript is technically sound and written in a standard english. It is an important scientific research as anaemia is a serious public health problem among girls and women within reproductive age of the developing countries. The data also supported the conclusion and statistical analysis was done appropriately. There are some restricitions about the data availability. The author must be specified about the data availability statements. Need to revise the keywords and syntax error.

Reviewer #2: Introduction:

• Line 55-56: “Anaemia is determined by a decreasing red blood cell count below the cut-off point set by the World Health Organization”- is a wrong statement. What WHO says is- “Anaemia is a condition in which the number of red blood cells or the haemoglobin concentration within them is lower than normal”. Please use correct clinical terms to define a clinical condition like anaemia.

• Line 76: Reference missing.

• Line 86: Grammatically incorrect.

• Line 87: Reference missing.

• Line 92: Grammatically incorrect.

• What is the justification of conducting the survey in south coastal region of Bangladesh?

• In title, the region is mentioned as the south coastal region of Bangladesh whereas in line 101 the region is mentioned as rural southern region. Which one is correct? Please be consistent.

Methods:

• How is the “"Max Nutri-WASH" initiative connected to the reported study? This is unclear. Please detail this.

• Line 117: desired precision of what? Non-response rate of what? Please mention specifically.

• Line 123: standard or standardized? How did the authors standardize the questionnaire? Please clarify.

• Please add the English and Bangla versions of the questionnaire as supplementary files.

• Line 144-145: Reference missing.

• Ethical considerations, Line 164: “assent (<18 years) from their parents/caregivers”. But assent should be taken from the adolescents and that will be supported by subsequent consent taken from their caregivers. Please check and modify.

• Ethical considerations, Line 166-167: Giving assurance about maintaining confidentiality is important, but maintaining the confidentiality is more important. Was it maintained? Please mention.

• Statistical analysis: Predictors or explanatory variables or independent variables? Please use only one term consistently.

Results:

• Line 183. Five or more groups out of how many food groups? Please be specific and detail the MDD-W cut-off in the relevant section.

• Were all the clusters of same size? If not, were the reported proportions and the estimates weighted as proportional to size? Please explain.

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

**********

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

PLoS One. 2024 Jul 10;19(7):e0306183. doi: 10.1371/journal.pone.0306183.r002

Author response to Decision Letter 0


19 Feb 2024

Editor Comments: In the online submission form, you indicated that [The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.].

All PLOS journals now require all data underlying the findings described in their manuscript to be freely available to other researchers, either 1. In a public repository, 2. Within the manuscript itself, or 3. Uploaded as supplementary information.

This policy applies to all data except where public deposition would breach compliance with the protocol approved by your research ethics board. If your data cannot be made publicly available for ethical or legal reasons (e.g., public availability would compromise patient privacy), please explain your reasons on resubmission and your exemption request will be escalated for approval.

Response to Editor: All relevant data are attached within the manuscript and its Supporting Information files in the revised version.

Additional Editor Comments: The study was conducted in Max Nutri WASH program zones but the present title of the research generalizes the issue. Kindly reconsider the title. Kindly address the issues raised by the reviewers.

Response to Editor: The participants of the study were the beneficiaries of the Max Nutri WASH program and the program was implemented in southern region. Therefore, in the title we mentioned southern region. In the response to the reviewer sections, we addressed all the issues raised by the reviewers.

Review Comments to the Author

Reviewer #1 comments: The manuscript is technically sound and written in a standard english. It is an important scientific research as anaemia is a serious public health problem among girls and women within reproductive age of the developing countries. The data also supported the conclusion and statistical analysis was done appropriately. There are some restrictions about the data availability. The author must be specified about the data availability statements. Need to revise the keywords and syntax error.

Response to Reviewer #1: Thank you for your constructive feedback. In the revised version, all relevant dataset is attached. Additionally, we carefully revise the keywords and address the syntax error.

Reviewer #2 comments: Introduction: Line 55-56: “Anaemia is determined by a decreasing red blood cell count below the cut-off point set by the World Health Organization”- is a wrong statement. What WHO says is- “Anaemia is a condition in which the number of red blood cells or the haemoglobin concentration within them is lower than normal”. Please use correct clinical terms to define a clinical condition like anaemia.

Response to Reviewer #2: In line 55-56: We revised the definition of anaemia according to the reviewer’s suggestion- “This adverse health condition arises when the red blood cells count or the concentration of haemoglobin within them falls below normal.”

Reviewer #2 comments: Line 76: Reference missing.

Response to Reviewer #2: In the revised version, reference is added to this line.

Reviewer #2 comments: Line 86: Grammatically incorrect.

Response to Reviewer #2: Sorry for this inconsistency. We have corrected the grammatical issue. The revised line 86: In Bangladesh, anaemia affected around half of the adolescent girls (52%) [4], pregnant (50%) and lactating (49%) women.

Reviewer #2 comments: Line 87: Reference missing.

Response to Reviewer #2: In the revised version, reference is added to this line.

Reviewer #2 comments: Line 92: Grammatically incorrect.

Response to Reviewer #2: Sorry for this inconsistency. We have corrected the grammatical issue. The revised line 92: This lower prevalence of iron deficiency anaemia suggests other possible factors that could explain the occurrence of anaemia in Bangladesh.

Reviewer #2 comments: What is the justification of conducting the survey in south coastal region of Bangladesh?

Response to Reviewer #2: The study was conducted in Max Nutri-WASH programme area. The programme is mainly focused southern rural part of Bangladesh. The southern part has both coastal and non-coastal areas. Our study participants were from both coastal and non-coastal areas. Therefore, we revised the title as “southern rural region”. The study was funded by Max-Foundation, they wanted to measure the anaemia situation of the beneficiaries of Max Nutri-WASH programme. Besides, there is a scarcity of recent evidence of anaemia and its determinants among adolescent girls, pregnant, and lactating women in rural community settings of Bangladesh, especially in the southern region. This area, being climate-vulnerable, is more susceptible to micronutrient deficiencies. Therefore, this study was conducted in this region.

Reviewer #2 comments: In title, the region is mentioned as the south coastal region of Bangladesh whereas in line 101 the region is mentioned as rural southern region. Which one is correct? Please be consistent.

Response to Reviewer #2: The study was conducted in Max Nutri-WASH programme area. The programme is mainly focused southern rural part of Bangladesh. The southern part has both coastal and non-coastal areas. Our study participants were from both coastal and non-coastal areas. Therefore, we revised the title as “southern rural region” and it was kept consistent throughout the manuscript.

Reviewer #2 comments: Methods: How is the “"Max Nutri-WASH" initiative connected to the reported study? This is unclear. Please detail this.

Response to Reviewer #2: Reproductive age women and children are more vulnerable to micronutrient malnutrition, especially anemia. Inadequate sanitation increases the probability of parasitic diseases, which generates iron deficiency, and WASH conditions may influence the prevalence of anemia. Max Foundation has been implementing healthy village campaign program in "Max Nutri-WASH" Program areas in 62 Unions of five districts- Patuakhali, Barguna, Khulna, Jessore, and Satkhira on water, sanitation, and hygiene, nutrition, adolescent and women reproductive health. This cross-sectional study was conducted among the beneficiaries who were enlisted to the "Max Nutri-WASH" program in three southern districts (Khulna, Patuakhali, and Satkhira) of Bangladesh.

Reviewer #2 comments: Line 117: desired precision of what? Non-response rate of what? Please mention specifically.

Response to Reviewer #2: Desired precision or margin of error was 6%. Non-response was considered to 10% which refers to participants who were not willing to provide blood samples for haemoglobin measurement or did not continue the full interview session.

Reviewer #2 comments: Line 123: standard or standardized? How did the authors standardize the questionnaire? Please clarify.

Response to Reviewer #2: We apologies for this inconsistency. It would be standard not standardized. The line was revised as: A standard structured questionnaire following the questionnaire of the National Micronutrient Survey of Bangladesh, Bangladesh Demographic Health Survey was formulated to collect data from the study participants.

Reviewer #2 comments: Please add the English and Bangla versions of the questionnaire as supplementary files.

Response to Reviewer #2: The English and Bangla versions of the questionnaire are added as a supplementary file.

Reviewer #2 comments: Line 144-145: Reference missing.

Response to Reviewer #2: In the revised version, reference is added to this line.

Reviewer #2 comments: Ethical considerations, Line 164: “assent (<18 years) from their parents/caregivers”. But assent should be taken from the adolescents and that will be supported by subsequent consent taken from their caregivers. Please check and modify.

Response to Reviewer #2: We modified the Ethical considerations in the revised version. It was written as: The institutional review board (IRB) of icddr,b approved the study (protocol # PR-21124). Prior to the interview, informed written consent was taken in the local language from the study participants (>18 years). Assent was taken from the adolescent girls whose age was below 18 years and subsequently, consent was obtained from their parents and caregivers. Participants who were illiterate provided consent by thumb impression. The research team described to the participants about background and objectives of the study, the voluntary nature of participation, and the future use of data. They were given assurance that confidentiality would be maintained for all the gathered information. None other than the investigators of this research, the Ethical Review Committee of icddr,b, and any law-enforcing agency in the event of necessity would have access to the information.

Reviewer #2 comments: Ethical considerations, Line 166-167: Giving assurance about maintaining confidentiality is important, but maintaining the confidentiality is more important. Was it maintained? Please mention.

Response to Reviewer #2: We assured that the privacy, anonymity and confidentiality of data/information identifying the study subjects was strictly maintained. We kept all the collected information and results of the clinical tests performed on confidential, under lock and key. None other than the investigators of this research, the Ethical Review Committee of icddr,b and any law-enforcing agency in the event of necessity would have an access to the information.

Reviewer #2 comments: Statistical analysis: Predictors or explanatory variables or independent variables? Please use only one term consistently.

Response to Reviewer #2: In the revised version, independent variables is consistently used.

Reviewer #2 comments: Results: Line 183. Five or more groups out of how many food groups? Please be specific and detail the MDD-W cut-off in the relevant section.

Response to Reviewer #2: A diet was considered diversified if anyone consumed at least five of the ten food groups. It was elaborated in the methods section. The revised lines: The Minimum Dietary Diversity-Women (MDD-W) indicator was used to assess their dietary diversity, which was developed based on a preceding 24-hour dietary recall from a list of ten selected food groups, including grains/roots/tubers, pulses/legumes, nuts/seeds, dairy, eggs, meat/poultry/fish, dark green leafy vegetables, other vitamin A-rich fruits and vegetables, other fruit, and other vegetables. A diet was considered diversified if anyone consumed at least five of the ten food groups.

Reviewer #2 comments: Were all the clusters of same size? If not, were the reported proportions and the estimates weighted as proportional to size? Please explain.

Response to Reviewer #2: Yes, all the clusters were same in size. Here, the cluster was union and equal number of participants from each target group was chosen using a systematic sampling technique.

Decision Letter 1

Biswajit Pal

13 Jun 2024

Anaemia among adolescent girls, pregnant and lactating women in the southern rural region of Bangladesh: prevalence and risk factors

PONE-D-23-35666R1

Dear Dr. Ara,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. Please make sure your user information is up-to-date by logging into Editorial Manager at Editorial Manager® and clicking the ‘Update My Information' link at the top of the page. If you have any questions relating to publication charges, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Biswajit Pal, M.SC., Ph.D

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Authors have adequately addressed the comments raised in a previous round of review and this manuscript is now acceptable for publication.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

**********

Acceptance letter

Biswajit Pal

1 Jul 2024

PONE-D-23-35666R1

PLOS ONE

Dear Dr. Ara,

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team.

At this stage, our production department will prepare your paper for publication. This includes ensuring the following:

* All references, tables, and figures are properly cited

* All relevant supporting information is included in the manuscript submission,

* There are no issues that prevent the paper from being properly typeset

If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks to review your paper and let you know the next and final steps.

Lastly, if your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

If we can help with anything else, please email us at customercare@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Biswajit Pal

Academic Editor

PLOS ONE

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 File. Survey questionnaire.

    (PDF)

    pone.0306183.s001.pdf (816.3KB, pdf)
    S1 Dataset. Dataset of adolescent girls.

    (XLS)

    pone.0306183.s002.xls (177.5KB, xls)
    S2 Dataset. Dataset of pregnant women.

    (XLS)

    pone.0306183.s003.xls (183.5KB, xls)
    S3 Dataset. Dataset of lactating women.

    (XLS)

    pone.0306183.s004.xls (178KB, xls)

    Data Availability Statement

    All relevant data are within the paper and its Supporting Information files.


    Articles from PLOS ONE are provided here courtesy of PLOS

    RESOURCES