Introduction

The burden of adverse pregnancy outcomes (APOs), which includes both preterm births and low birth weights [1,2], is substantial in both developed and developing countries [1–3]. More than 60% of preterm births take place in south Asia and sub-Saharan Africa [3]. A recent study estimated that 12.8 million babies were born small for gestational age in India alone in the year 2010, a prevalence of 47% of all births [1]. Preterm birth and low birth weight are critical determinants of child survival, disabilities, stunting, and long-term adverse consequences for the onset of non-communicable diseases in the life course and demand appropriate public health interventions [1,4]. Despite India’s impressive economic growth in the last two decades, access to improved sanitation services in rural and vulnerable communities is extremely limited.

The World Health Organization (WHO) defines a birth weight of <2,500 g as low birth weight and a delivery before 37 completed weeks of gestation as preterm birth [5]. We adopted the WHO guidelines that define an APO as an event of low birth weight, preterm birth, stillbirth, or abortion. APO is a complex, multifactorial, physiological outcome in women, and despite decades of research, a clear causal mechanism for APOs has not been established. Studies have reported numerous risk factors for APOs such as malaria [6], infection [7–12], anaemia [13–16], obesity [17], hypertension [18], hyperglycaemia [19], diabetes [20], periodontal disease [21], endometriosis [22], history of abortion [23], antenatal complications [24], antenatal care (ANC) [24], environmental pollution [25–29], violence [30], and other socio-economic disparities [31–33]. In many low- and middle-income countries, access to improved sanitation facilities is limited, but the link between sanitation and APOs has not been explored.

The WHO/UNICEF Joint Monitoring Programme for Water Supply and Sanitation (JMP) defines an improved sanitation facility as a facility that hygienically separates human excreta from human contact, such as a flush toilet, piped sewer system, septic tank, flush/pour flush to pit latrine, ventilated improved pit latrine, pit latrine with slab, or composting toilet [34]. Similarly, the JMP defines unimproved sanitation facilities as flush/pour flush to elsewhere, pit latrine without slab, bucket, hanging toilet or hanging latrine, no facilities, or bush or field. Globally, 1.1 billion people still practices open defecation, of which 638 million are in India [34]. Poor sanitation, alongside unsafe drinking water and hygiene, are responsible for a considerable proportion of the global burden of disease [35,36]. Water, sanitation, and hygiene (WASH) interventions have been linked to improvements in a number of important health outcomes, including diarrhoeal diseases [37], helminth infections [38,39], and childhood stunting [40,41]. Recent studies in India have failed to show that programmes to improve sanitation in India lead to health gains in children aged under 5 y, although critical in these findings were the low levels of improved sanitation use among the population [42,43]. Although little work has been done to evaluate the effects of WASH interventions on APOs, a recent review identified over 60 biological and social mechanisms linking poor WASH practices to various maternal and reproductive health outcomes [44].

At least some of these identified plausible mechanisms linking open defecation to APOs are supported by existing evidence. For example, there is good evidence that poor sanitation can promote hookworm infestation [39], which is a risk factor for maternal anaemia [10,45,46], which, in turn, is directly linked to APOs [16,47]. In India, the prevalence of anaemia and chronic energy deficiency (measured as low body mass index [BMI]) in women aged 15–49 y is as high as 55.3% and 35.6%, respectively [48,49].

Exposure to unsafe water, unimproved sanitation, and poor waste management during pregnancy may increase the risk of infection, causing downstream effects such as low birth weight and preterm delivery. A recent systematic review [50] and a conceptual framework [44] concluded that a lack of improved sanitation facilities appears to be associated with maternal mortality, and highlighted the paucity of primary studies assessing the impact of water and sanitation practices on pregnancy outcomes [44,50].

To the best of our knowledge, this is the first rigorous attempt to quantify the risk of APOs with access to improved sanitation and practice using a population-based cohort, with specific aims to quantify the prevalence of open defecation among pregnant women and its association with APOs.

Methods

Study Design

We conducted a population-based prospective cohort study. Assuming a 20.0% prevalence of APOs [24,56–58], we calculated that the sample size needed to be 582 to detect a relative risk (the difference in incidence of APOs between women with and without improved sanitation) of 1.5 with 95% confidence at 80% power. All pregnant women satisfying the eligibility criteria in the study population were recruited into the study. Estimating an anticipated 15% dropout rate, our final target sample size was 670. There were 708 eligible pregnant women in the two study settings (coastal and inland). A random number generator selected the 670 geocoded households/women who were enrolled through a household visit by the CHV. A schematic diagram of the study design is shown in Fig 1. Baseline assessment at recruitment and three home visits (one in the second trimester and two in the third trimester) were designed to ensure retention and learn about study outcomes during the course of pregnancy, followed by a home visit at birth to document pregnancy outcomes. Sanitation exposures measured at baseline were used to estimate the risks of pregnancy outcomes.

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Fig 1. Study design and sampling scheme.

https://doi.org/10.1371/journal.pmed.1001851.g001

Results

Of the 670 women recruited, 667 completed the study, of which 172 (28.2%) experienced APOs (Fig 1). Among these women, 130 (19.4%) had preterm births, 95 (14.2%) gave birth to babies with low birth weight, 11 (1.6%) had spontaneous abortions, and six (0.9%) had stillbirths. Detailed socio-demographic, anthropometric, and clinical characteristics of study participants stratified by APO are shown in Table 1. In our study population, about 85% of the women were 20–29 y-old, 72% had normal BMI (range 18.5–24.9 kg/m²), 36.1% did not have anaemia (Hb ≥ 110 g/l), 35.4% were primiparous, and 15.1% had no formal education (Table 1).

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Table 1. Pregnant women’s selected socio-demographic, anthropometrics, and clinical characteristics stratified by adverse pregnancy outcome (n = 667).

https://doi.org/10.1371/journal.pmed.1001851.t001

Table 2 provides the prevalence of sanitation access and practices with unadjusted ORs for APOs. Of the 667 women, 388 (58.2%) had no access to a latrine and reported open defecation at recruitment. About half (45.8%) of the pregnant women living in a household with latrine access used the latrine on a regular basis, and 32% reported rare use of the facility. The majority (72.4%) of the latrine facilities were simple pit latrines. About 60% of the latrines had a water source in or at the latrine, and 21.5% of the latrines had visible faecal contamination on the latrine floor (an indication of poor sanitation practice). About half of the households had a hand-washing station with soap at or near the latrine. In our population, 58% of pregnant women did not wash their hands with soap or detergent after defecation. Only 14.7% of participants in our study used piped water for bathing or body washing.

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Table 2. Pregnant women’s sanitation access and use with unadjusted odds ratios for adverse pregnancy outcomes.

https://doi.org/10.1371/journal.pmed.1001851.t002

Unadjusted bivariate associations of each of these sanitation factors with APOs are presented in Table 2. Compared to latrine access, open defecation was associated with higher odds of APO (OR: 2.53; 95% CI: 1.72–3.71), preterm birth (OR: 2.36; 95% CI: 1.54–3.62), and low birth weight (OR: 2.00; 95% CI: 1.24–3.23). Risk of APO (OR: 3.92; 95% CI: 1.80–8.52) was also considerably higher for women who used a latrine only occasionally. Water not being available at the latrine was also associated with an increased odds of APO (OR: 4.07; 95% CI: 2.07–8.02). Women who reported bathing or body washing with an open source of water such as a pond, river, or canal also had significantly higher odds of APO (Table 2).

Table 3 shows the results of the multivariable model adjusted for covariates that were selected using a priori criteria, as related to latrine access and APOs. The model estimate in the multivariable analysis for the association of open defecation with APO (AOR: 2.38; 95% CI: 1.49–3.80) was minimally attenuated (Table 3). We also observed that higher wealth index was not associated with a reduction in the odds of APOs (AOR: 0.97; 95% CI: 0.80–1.18); however, higher education was found to be associated with a reduction in the odds of APO (AOR: 0.68; 95% CI: 0.59–0.79). Higher haemoglobin in the first trimester was found to be significantly associated with lower odds of APOs (AOR: 0.50; 95% CI: 0.31–0.81) (Table 3). We further investigated the association between latrine use and APOs among participants with latrine access (Table 4). Our results specifically demonstrate that latrine access alone is not associated with a reduction in the burden of APOs; however, latrine use is. Our model estimated 7-fold higher odds of APOs among pregnant women who had access to a latrine but used it only rarely (AOR: 7.10; 95% CI: 2.18–23.11) compared to women who used a latrine often/daily. The association of poor sanitation practices with APOs was independent of poverty in our study settings.

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Table 3. Multivariable adjusted models for the association between sanitation characteristics and adverse pregnancy outcomes (n = 667).

https://doi.org/10.1371/journal.pmed.1001851.t003

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Table 4. Association between sanitation use and adverse pregnancy outcomes among participants with latrine access (n = 279).

https://doi.org/10.1371/journal.pmed.1001851.t004

Discussion

In this prospective study, we examined the relationship between maternal sanitation behaviour and APOs. After adjusting for socio-demographic, anthropometric, and other sanitation-related behaviours, we observed that women who reported poor sanitation practices in the early phase of pregnancy (10–12 wk of gestation) were more likely to experience an APO, independent of the established confounding factors of poverty and caste. To our knowledge, this is the first community-based prospective study to demonstrate that practicing open defecation is associated with a higher risk of APOs. Using a large existing population-based cohort, all pregnancies could be enrolled and followed longitudinally from the first trimester to pregnancy. The diverse nature of our study sites also allowed us to enrol a representative rural Indian sample including individuals of different castes, class, religion, and socio-economic status, with a range of sanitation-related practices.

Population-based data on the prevalence of APOs as reported here are uncommon in India. Among our cohort, we found that 19.5% of births were preterm and 14.2% of babies had low birth weight during the study period. Studies from south India (Tamil Nadu) have reported a prevalence of low birth weight and preterm birth of 17.0% and 12.3%, respectively, although the prevalence of low birth weight has also been estimated to be as high as 30%–40% in India [57]. The rate of preterm delivery (<37 wk) in neighbouring Bangladesh [24] was 22.3% in a setting similar to India. In sub-Saharan Africa, the prevalence of preterm birth and low birth weight in an urban setting was 19.9% and 10.2%, respectively [56].

Given the paucity of research linking open defecation to APOs, it is difficult to assess our findings in the context of other study findings. A hospital-based study in sub-Saharan Africa found a higher risk of preterm birth, but not low birth weight, among babies born to mothers using shared sanitation facilities (OR: 1.26; 95% CI: 1.07–1.48) [56].

Our study reports a protective role of maternal haemoglobin (Hb ≥ 110 g/l) in regards to the risk of APOs among the study populations which is in line with other findings. A recent systematic review and meta-analysis showed a significantly higher risk of low birth weight (OR: 1.29; 95% CI: 1.09–1.53) and preterm birth (OR: 1.21; 95% CI: 1.13–1.30) with anaemia in the first or second trimester [47]. The same study also estimated that each 1-g/l increase in mean haemoglobin corresponded to birth weight being increased by 14.0 g (95% CI: 6.8–21.8). Another study in India revealed 30% of women to be anaemic (Hb < 110 g/dl), and maternal anaemia predicted a 2.4-fold greater risk of preterm delivery (p < 0.01) and an increased risk of low birth weight (p = 0.05) [16]. We observed that higher haemoglobin was associated with low odds (AOR: 0.50; 95% CI: 0.31–0.81) of APOs among women in the multivariable model.

Another important finding of our study was that education remained a key determinant of APOs in the multivariable model. We observed higher education to be associated with lower odds (AOR: 0.68; 95% CI: 0.59–0.79) of APOs among women in the multivariable model. This finding is consistent with numerous research findings of higher education being predictive of lower likelihood of APOs [31,61]. A Canadian study showed that not having a high school diploma was associated with low birth weight (OR: 3.20; 95% CI: 2.61–3.91). The inverse association of education with APOs could be attributed to many socio-behavioural factors related to the overall impact of higher levels of education. Education can improve knowledge about safe hygiene practices and assimilation of health-related information and good hygiene behaviour [62,63]. Similarly, an educated person may be more likely to appreciate the positive effect of sanitation and hygiene practices, resulting in sustained healthy behaviour [64].

We adjusted our estimates to account for socio-economic factors by constructing a household wealth index. Poverty is highly correlated with a lack of sanitation access, and both factors have been linked to increased risks regarding maternal health [31,32], stunting [41], and stress. While it is intuitive to expect that individuals with low economic status are more likely to experience APOs because of many concomitant negative determinants of pregnancy, our results demonstrate that open defecation poses significant health risks that are not explained by poverty.

In our study, although we adjusted our estimates for a priori covariates and considered several biological plausibilities, we did not adjust for many potential risk factors for APOs such as maternal smoking, alcohol use, history of sexually transmitted diseases, history of antenatal complications, history of abortions, etc. Whereas each of these factors has been associated with an increased risk of APOs, we are unaware of any data suggesting that these variables are associated with defecation practice. Hence, we considered these variables unlikely to be confounders in our analysis [60]. Several questions remained unanswered in this study, and we have not been able to address the biological or behavioural basis of these findings. One mechanism may be related to the adverse outcomes of restricting food and water intake to cope with sanitation challenges. It has been shown that women, when confronted with poor sanitation choices, may choose to limit their intake of food and water to avoid the need to use the toilet. Another potential mechanism may be related to community-level or household-level coverage and use of sanitation and the resulting increase in disease prevalence associated with environmental contamination in drinking water or in food. The pathogenesis of each of the adverse birth outcomes is unique and potentially independent, and we have not identified the specific exposure pathways (such as incidence of bacterial vaginosis) that may play a role in our observed outcomes. A third potential mechanism may be related to the lack of sanitation and psycho-social stress. Women throughout their life course may experience tangible threats to physical health as a result of sanitation insecurity, a mechanism currently being explored as part of this study.

This study indicates that, in the context of maternal and child health promotion research, sanitation is an important dimension of women’s health and distinct from poverty and caste. Additional research is warranted that addresses the underlying mechanisms of sanitation-related APOs.

Supporting Information

Acknowledgments

The authors wish to thank the other members of our research consortium: Belen Torondel, Bethany Caruso, Kristyna Rae Solawetz Hulland, Krushna Chandra Sahoo, Padmalaya Das, Pravas Ranjan Misra, and Robert Dreibelbis. Also, we are indebted to the programme manager, supervisors, data entry personnel, and many field staff who administered the surveys and collected measurements for this study. We would like to express our appreciation for the support from study participants, and for the Anganwadi workers and Accredited Social Health Activists for assisting in this project.