Predictors of Anemia Among Pregnant Women of Under-privileged Ethnic Groups Attending Antenatal Care at Provincial Level Hospital of Province 2, Nepal

Background: This study aims to determine the predictors of anemia among pregnant women of underprivileged ethnic groups attending antenatal care at provincial level hospital of Province 2. Methods: A hospital based cross-sectional study was carried out in Janakpur Provincial Hospital of Province 2, Southern Nepal. 287 pregnant women from underprivileged ethnic groups attending antenatal care were selected and interviewed. Face to face interviews using structured questionnaire was undertaken. Anemia status was assessed based on hemoglobin levels determined at the hospital’s laboratory. Bivariate and multiple logistic regression analyses were used to identify the predictors of anemia. Analyses were performed using IBM SPSS version 23 software. Results: The overall anemia prevalence in the study population was 66.9% (95% CI 61.1-72.3). The women from most under-privileged ethnic groups (Terai Dalit, Terai Janajati and Muslims) were twice more likely to be anemic than Madhesi women. Similarly, women having education lower than secondary level were about 3 times more likely to be anemic compared to those with secondary level or higher education. Women who had not completed four antenatal visits were twice more likely to be anemic than those completing all four visits. The odds of anemia were three times higher among pregnant women who had not taken deworming medication compared to their counterparts. Furthermore, women with inadequate dietary diversity were four times more likely to be anemic compared to women having adequate dietary diversity.

women from most under-privileged ethnic groups (Terai Dalit, Terai Janajati and Muslims) were twice more likely to be anemic than Madhesi women. Similarly, women having education lower than secondary level were about 3 times more likely to be anemic compared to those with secondary level or higher education. Women who had not completed four antenatal visits were twice more likely to be anemic than those completing all four visits. The odds of anemia were three times higher among pregnant women who had not taken deworming medication compared to their counterparts. Furthermore, women with inadequate dietary diversity were four times more likely to be anemic compared to women having adequate dietary diversity.
Conclusions: The prevalence of anemia is a severe public health problem among the pregnant women of under-privileged ethnic groups in Province 2. Being Dalit, Janajati and Muslim, having lower education, less frequent antenatal visits, not receiving deworming medication and having inadequate dietary diversity are found to be the signi cant predictors. The present study highlights the need of improving the frequency of antenatal visits and coverage of deworming program in ethnic populations. Furthermore, promoting a dietary diversity at the household level would help lower the prevalence of anemia. The study ndings also imply that the nutrition interventions to control anemia must target and reach pregnant women from most-marginalized ethnic groups and those with lower education.

Background
Anemia, a condition with low blood hemoglobin concentration and/or red blood cells (RBCs), is a global public health problem that mostly affects low and middle income countries (LMICs) 1 . Anemia in pregnancy poses greater risk for low birth weight, preterm birth, and perinatal and neonatal mortality 2 .
Besides, severity of anemia is associated with higher rates of maternal mortality 3 . Anemia affects over half a billion women of reproductive age worldwide. It is estimated to affect 38% (32.4 million) of pregnant women globally with highest prevalence in the World Health Organization (WHO) regions of South-East Asia (48.7%) and the Africa (46.3%) 4 . Evidences from various low and middle income countries suggest that anemia is disproportionately concentrated in low socio-economic-group 5 with poorest, ethnically disadvantaged and least educated at the greatest risk.
In Nepal, 41 percent of reproductive age women are anemic with highest prevalence in the Province 2 (58%) 6 . The anemia prevalence in women is disproportionately higher among Terai Dalit (so-called untouchable Terai inhabitants), Terai Janajati (indigenous Terai people), Terai/Madhesi Brahmin Chhetri (upper caste-Terai inhabitants) and Muslims 7 . These ethnic groups constitute over three-fourth of the population in the Province 2 8 . Yet, they are historically marginalized and have performed poorly as measured by indicators of poverty, health, nutrition, education and women's empowerment. The utilization of health services by Terai Dalit, Terai Janajati, Muslim and Madhesi are consistently poor for the past many years 7 . Furthermore, studies have also shown that Terai women are more likely to be anemic than women in other regions [9][10][11] .
Reducing anemia prevalence among women and children have been a long standing priority for Nepal. remarkable efforts to reduce anemia in women through activities such as universal, daily iron-folic acid (IFA) supplementation to pregnant and lactating women; deworming program to reduce the burden of parasitic infections and mandatory forti cation of wheat our with iron, folic acid and vitamin A 12,13 . Yet, anemia is still a public health problem in Nepal. This is more challenging as women from the poorest and marginalized groups are the most affected 7 .
The 2030 agenda for sustainable development has urged countries to place special emphasis on those left furthest behind and the most excluded with a strong focus on leaving no one behind. This agenda also requires the country to reach its goals and targets for all people and all segments of the society 14 .
The national strategy for reaching the unreached (2016-30) has also clearly highlighted that the reduction of health and nutrition inequalities and achievement of a universal health coverage in the country can only be realized if unreached populations are systematically targeted 15 . In this context, nutrition programs, actions and strategies are necessary that target the most-vulnerable communities bearing disproportionate burden of anemia 11 . This warrants an appropriate investigation among marginalized ethnic groups and those furthest behind. Although a wide range of research studies in Nepal have attempted to examine the factors associated with anemia, majority of these analyses are speci cally limited to general population such as women, children and adolescents. Disaggregated analysis involving key sub-populations particularly the ethnic groups which are underprivileged and have greater vulnerability to anemia have not yet been available for Nepal. It is against this background that this study was conducted. The study aimed to assess the predictors of anemia among pregnant women of underprivileged ethnic groups who attended antenatal care at the provincial level hospital of Province 2.
Better understanding of the local determinants of anemia are considered crucial to identify and implement evidence-based and contextually appropriate strategies 5 .

Study Design and Settings
This was a hospital based cross-sectional study conducted at Janakpur Provincial Hospital, located at the Janakpurdham, the capital of Province-2, Nepal. The Province 2, one of the seven provinces consists of eight districts that extends in the south-eastern at plains (Terai region) of Nepal. Despite its ecological richness, Province 2 fares poorly in various socio-economic and health indicators including but not limited to literacy, teenage pregnancy, nutrition, contraceptive use, immunization coverage, and exposure to domestic violence. As per the Nepal Demographic Health Survey, the prevalence of anemia among women of reproductive age was reported the highest in the Province 2 6 . Janakpur Provincial Hospital is the largest referral level public hospitals in the Province 2 offering wide range of health care services including antenatal, maternal and newborn care. This hospital receives patients and clients largely from Dhanusha and surrounding four districts (Siraha, Mahaottari, Sarlahi and some parts of Sindhuli).

Study Population
This study was carried out among pregnant women who attended antenatal care (ANC) in the Janakpur Provincial Hospital. Women in the second and third trimester of pregnancy and belonging to the underprivileged ethnic groups were included in the study. The underprivileged groups in this study constituted of Terai Dalit, Terai Janajati, Muslim and Madhesi. These groups have historically suffered oppression, discrimination and social-segregation and are politically, economically and socially backward 16,17 . They are often unable to enjoy social services and facilities and face signi cant inequalities in the utilization of health care 7,18 . Terai dalits are ascribed the lowest position in the casteethnicity hierarchical structure and represent the most depressed category among all ethnic groups. They have suffered from acute landlessness, caste-based discrimination, including untouchability 16,19 .
Madhesi caste group grips a relatively better advantage as compared to the other three groups 20 .

Study Design and Sampling Procedure
The sample size was calculated using Epi Info StatCalc software assuming 95% level of con dence, 0.06 margin of error and 57.8% anemia prevalence among reproductive age women of Province-2 6 . A minimum sample of 261 was estimated and it was increased to 287 considering the non-response rate of 10%. The study participants attending antenatal care between 10 am to 4 pm were consecutively enrolled until the planned sample size was achieved.

Data Collection
A structured questionnaire was developed based on the study objectives. Standard food and dietary recall questionnaire developed by Food and Nutrition Technical Assistance (FANTA) Project was used to assess the dietary diversity status 21 . The questionnaire was divided in four broad sections: socio-demographic information; preventive health practices; dietary practices; and hemoglobin level (Additional le 1). Data collection was carried out between November and December 2017 using face to face interview with the pregnant women at the antenatal care (ANC). Interviews were conducted in a separate room after the participants received their antenatal services. The interview was administered by the rst author who could speak both Nepali and Maithili (local) languages. In order to determine the status of anemia, blood was drawn from each participant with the help of a certi ed lab technician. The blood samples were collected and tested in the laboratory of Janakpur Provincial Hospital. The collected blood samples were checked for hemoglobin level using cyanmethemoglobin method.

Dietary Diversity Status
This was a dichotomous indicator of whether or not women have consumed at least ve out of ten de ned food groups within 24 hours. In order to determine this, we used a 24-hour dietary recall questionnaire gathering information on all foods and beverages consumed by the participants in the previous day and night. The foods consumed were aggregated into 10 recommended food groups: starchy staples, pulses (beans, peas and lentils), nuts and seeds; dairy; meat, poultry and sh; eggs, dark green leafy vegetables; vitamin A rich fruits and vegetables; other vegetables; and other fruits. For each food group the pregnant women consumed from, a score of 1 was provided and 0 otherwise. The scores from all ten food groups were added to obtain the total dietary diversity score ranging from 0 to 10. The dietary diversity score thus obtained was categorized into 2 groups to derive a dietary diversity status for pregnant women. The dietary diversity score of ve or more was considered adequate (coded as 1) and the score below ve was inadequate (coded as 0) 21,23 .
Ethnicity A caste/ethnicity classi cation used by the Health Management Information System (HMIS) of the Ministry of Health and Population, Nepal was adapted for this study. This system uses six caste-groups; Dalits, Janajati, Muslim, Madhesi, Brahmin/Chhetri and Others, of which the rst four groups (Table 1) were taken as they are considered belonging to the underprivileged groups. Among Dalit and Janajati, only Terai Dalits and Terai Janajati were present during the period of data collection.

Characteristics of the Study Population
The age of the women ranged from 18-37 years. The mean age of the respondents was 22.6 years (SD = 3.9 years). Majority of the women were in the age group 20-24 years (45.6%), were Madhesi (65.2%) and followed Hinduism (90.2%). Only one-fourth of pregnant women (27.2%) had completed their secondary level education. Greater majority of the pregnant women lived in joint and extended families (81.5%) and were homemaker (89.9%). At the time of interview, 41.5 and 58.5 percent were in their second and third trimesters of pregnancy respectively. More than half (53.7%) of the pregnant women were multi-gravida. About one in ten (9.4%) pregnant women had a history of miscarriage/abortion (Table 2). Preventive health practices In our study, only about a fourth of pregnant women (28.8%) had their four ANC visits completed. More than four in ve women had consumed iron folic acid (88.1%) and deworming medicine (81.8%). All pregnant women (100%) used mosquito net while sleeping (Table 3).  The overall prevalence of anemia (hemoglobin < 11.0 g/dl) was 66.9% (95% CI 60.3%-71.2%). In terms of severity, mild anemia was 64.8% (95% CI 59.0%-70.3%), moderate anemia was 1.7% (95% CI 0.57%-4.02%) and one women was severely anemic (Table 5).

Predictors of anemia
The anemia status of pregnant women was compared with socio-demographic characteristics, preventive health practices and dietary diversity status. In the bivariate analyses, a statistically signi cant association was found with ethnicity (p < 0.01), religion (p = 0.008), education (p < 0.001), place of residence (p = 0.019), gravida (p = 0.006), frequency of antenatal visits (p < 0.0 01), consumption of iron folic acid (p = 0.032) and deworming medicines (p = 0.001) and dietary diversity status (p < 0.001).
However, the association was not statistically signi cant for age, occupation, family type, history of miscarriage/abortion, and practice of food avoidance (Table 6).

Discussion
In the present study two in three pregnant women (66.9%) were anemic, signifying a severe public health problem 25 . This gure is more than two times higher than the prevalence reported among pregnant women from mid-western Nepal (28.3%) 26 . The anemia prevalence in our study is also higher than both the national (41%) and provincial estimates (58%) for the women of reproductive age 6 . The discrepancies in the prevalence might be due to hospital based study setting, inclusion of only the women from underprivileged ethnic groups, different study periods and regional variations in the socio-economic status and dietary practices. Being a referral level hospital, it is also possible that some of the pregnant women attending ANC at the study hospital were referred from peripheral health facilities after being suspected for pregnancy related complications including anemia. However, such information was not explored in this study. The anemia prevalence in our study was comparable with the study conducted among pregnant women in similar setting 27 . The PoSHAN community studies baseline report had also reported similar ndings among the pregnant women in the Terai region 28 .
In our study the factors associated with anemia among underprivileged pregnant women were ethnicity, education, intake of deworming medication, antenatal visits and dietary diversity status. Based on the available evidences from Nepal, it is clear that pregnant women from underprivileged or disadvantaged ethnic groups are more likely to be anemic compared to the upper caste groups. Our study further revealed that the burden of anemia is unevenly distributed even within the underprivileged ethnic groups.
The odds of anemia in pregnancy was two times higher among the most-marginalized groups (Terai Dalit, Terai Janajati and Muslims) compared to Madhesi women. This nding is quite obvious as Terai Dalits and Muslims occupy the lowest position in the human development and poverty indices 29,30 and suffer caste based discriminations much higher than other groups. The underlying structural factors such as poor literacy, caste-based discriminations, lesser autonomy in decision making and other cultural restrictions might have predisposed these women towards greater anemia risks. Furthermore, both the per capita consumption expenditure and land ownership are reported to be lowest among the terai Dalit caste-groups 31 suggesting their limited capacity to consume diverse foods. This nding warrants the need for special targeting to women from the most-disadvantaged ethnic groups with nutritional programs and interventions in order to "leave no one behind" as pledged in the 2030 agenda 14 .
Our study found signi cantly higher odds of anemia among pregnant women with lower education levels.
Women who had education below the secondary level were about three times more likely to be anemic than others. This is consistent with the ndings of similar studies where anemia was inversely associated with maternal education [32][33][34][35] . This is perhaps due to the bene ts associated with education. For example, higher education can contribute to higher productivity and earnings which in turn might have positive in uences in women's dietary practices. Studies have also documented positive impact of educational attainment on the quality of women's diet 36 . Women's education might also be associated with women's autonomy and empowerment. Autonomous women are likely to obtain more information and make better decisions regarding their nutrition, improve health-care seeking, and in uence intrahousehold food distribution 37,38 . Bene ts of completing secondary education on the nutritional status of women must therefore be recognized.
Low dietary diversity signi cantly predicted anemia in our study population. Pregnant women who did not have adequate diversity in their diet were four times more likely to be anemic compared to women whose dietary diversity was adequate. A number of previous studies from Nepal and other LMICs have also con rmed association of low dietary diversity with anemia [39][40][41][42] . The role of dietary diversity in ensuring adequate hematological status of pregnant women and thus its contribution in reducing the likelihood of anemia has been well documented 43 . Nonetheless, the anemia prevalence in our study was higher although more than two-thirds of pregnant women were found having an adequate dietary diversity. This might be because although the pregnant women reported consuming items from diverse food groups, they might have been consumed in low frequency and small portion sizes 28,[44][45][46] . Women often suffer the most from inequitable intra-household food distribution and are often the last in the household serving order [44][45][46] . Furthermore, one study conducted among Tharu and Musahar populations (indigenous groups of terai) revealed that the diet in Terai are dominated by rice (cereals) with only tiny portions of side-dishes such as lentils and vegetables which are insu cient to meet the recommended dietary allowance for micro-nutrients 47 . Although green vegetables and other diverse foods are readily grown and available in the terai region, people do not regard them as food items that should be consumed in large amounts 47 . This highlights the need for strong targeted behavior change communication (BCC) intervention that not only promotes dietary diversity but also the nutritional value of locally available foods and need for optimal intake of diets from each group (dietary adequacy).
Additionally, the possibility that lower dietary diversity in our study population might have been in uenced by household food insecurity cannot be undermined. Results of a national survey data found signi cantly higher odds of experiencing household food insecurity by dalit women 48 . The interventions to reduce micronutrient de ciency in the region should therefore aim to address dietary diversity, dietary adequacy and food security targeting the ethnically disadvantaged populations.
Evidences show that low coverage of deworming medications during pregnancy results in increased parasitic infections 49,50 and is associated with higher rates of anemia in pregnant women. Not having a deworming medication was one of predictors of anemia among our study population. Respondents who had not taken deworming medicines in their current pregnancy had three times higher odds of anemia than their counterparts. This is comparable with the evidence from previous studies 41, 51,52 . Further in our study, fewer ANC visits was associated with increased chances of anemia among the study population.
This can be explained by the fact that late and infrequent ANC visits might deny women with or delay the provision of iron-folic acid supplementation, deworming medication and/or malaria prophylaxis.
Whereas, women who seek ANC frequently are more likely to bene t from counseling and advices concerning nutrition, preventive health behaviors and healthful dietary practices. Our nding is consistent with previous studies which have reported an association between infrequent ANC visits and anemia 32,41,53 . Promoting the coverage and frequency of antenatal visits are therefore considered vital to reducing anemia in pregnant women.
There are some notable limitations which must be taken into account while interpreting the results of the study. First, cross-sectional nature of our study makes it di cult to establish the temporal relationships.
Second, the assessment of dietary diversity status was based on 24-hour dietary recall, which may not always represent the actual intake. Moreover, the possibility of recall bias also cannot be ruled out completely. Third, our prevalence estimate was based on participants enrolled in the hospital-based setting, which may differ from that of community based studies. Lastly, it is important to recognize that underprivileged ethnic groups from hill/mountain such as hill Dalit and hill Janajati could not be represented in this study as they were not present at ANC during the data collection period.

Conclusions
The prevalence of anemia is a severe public health problem among the pregnant women of underprivileged ethnic groups in Province 2. Being Dalit, Janajati and Muslim, having lower education, less frequent antenatal visits, not receiving deworming medication and having inadequate dietary diversity are found to be the signi cant predictors. The present study highlights the dire need of improving the frequency of antenatal visits and coverage of deworming program in ethnic populations. Furthermore, promoting a dietary diversity at the household level would help lower the prevalence of anemia. The study ndings also imply that the nutrition interventions to control anemia must target and reach pregnant women from most-marginalized ethnic groups and those with lower education.