Background
In Ethiopia, approximately 40% of children under five suffer from chronic undernutrition [
1]. To address this issue among rural populations that face poor physical and financial access to healthy diets, agricultural approaches have been promoted as one potential way to support nutrition [
2,
3]. Specifically, the production of animal source foods (ASF) has been recognized as a promising enterprise that can potentially empower women—who are often responsible for raising small animals—while also diversifying household diets and incomes, and increasing access to micronutrient-rich foods [
4‐
6].
However, there are concerns that small-scale animal production may increase a household’s exposure to contamination, especially in areas with suboptimal water, sanitation, and hygiene conditions [
7,
8]. Contamination of houses and yards with animal feces can lead to the spread of pathogens in water, food, and hands, resulting in the ingestion of fecal matter that leads to infection and, consequently, threats to the health and nutrition of infants and young children [
7,
9]. The main pathways through which exposure to animal contamination can harm child nutritional status are through the transmission of zoonotic pathogens that cause diarrhea, through parasitic infections such as worms, and through a subclinical condition known as environmental enteric dysfunction (EED), which triggers low-level inflammation and poor nutrient absorption [
7,
9,
10]. Thus, increased ownership of animals may be associated with increased exposure to fecal matter [
11] which has been associated with a higher prevalence of child growth faltering [
10‐
13].
Recent research has attempted to address these concerns of animal ownership and contamination by conducting observational, experimental, and qualitative studies. Some methods to explore these relationships have included “spot checks” of cleanliness around a household [
11]; direct observations of infants and young children to document instances of exposure to contamination [
13,
14]; direct measurement of pathogens and their transmission to humans, animals, and objects [
14‐
17]; measurement of biomarkers of EED [
18]; randomized trials to limit exposure to contamination [
19‐
21]; description of the factors predicting chicken corralling practices by households [
22]; qualitative research to understand perceptions surrounding the adoption of animal corrals [
23,
24]; and a combination of these methods [
14,
25]. However, we are not aware of any studies that quantitatively describe the chicken management practices used by households and then assess them qualitatively for ground-truthing purposes, especially in the context of Ethiopia. Moreover, our mixed methods include the use of in-depth interviews, which provide a detailed perspective on decision-making processes and justification for the use of husbandry practices by households.
Due to the recent push towards nutrition-sensitive livestock [
3], it is important to evaluate whether rural, resource-constrained households can safely integrate animals into their environments. Thus, as part of the baseline household survey of the Agriculture-to-Nutrition (ATONU) trial, an intervention designed to increase the production and consumption of chickens in rural Ethiopia, we collected a number of indicators describing chicken management practices and the households’ interaction with animals. Based on previous research showing a high degree of exposure of young children to environmental health risks [
11,
14], additional data triangulation through direct observations and in-depth interviews was necessary in order provide a more validated view of chicken management practices in this context.
The aims of this paper were to:
1)
Show the relationship between chicken management practices and distal measures of sanitation, using quantitative baseline data from the ATONU trial;
2)
Describe the pathways of chicken-child interactions using qualitative direct observation data collected during the midline of the ATONU trial; and.
3)
Investigate the beliefs and barriers underlying the adoption of different chicken management practices by households through qualitative in-depth interviews with woman caregivers of young children.
Discussion
Both our quantitative and qualitative findings support that children’s physical exposure to chickens is high among households raising chickens in these two regions of Ethiopia, and that specific chicken husbandry practices were linked to increased exposure to environmental contamination. The frequency and proximity of exposure pose substantial health risks for this population, and especially for households with young children, who are most vulnerable to adverse health and nutrition consequences.
To synthesize our findings, first, our quantitative results demonstrated that as the number of chickens raised increased, exposure to animal feces actually decreased. While having any chicken coop increased the risk of observing animal feces—likely because this was a proxy for raising enough chickens to warrant a coop—it was clear that not all coops were equally protective. Thus, while more animals can potentially equate to increased levels of contamination, it also appears that this may be somewhat compensated by increased measures of protection. This trend was supported by both phases of our qualitative research. Household observations and interviews revealed that if there were fewer chickens, or after high rates of chicken mortality, households often abandoned the use or upkeep of a coop and instead kept chickens inside the home. From this interpretation, having fewer chickens could potentially be associated with higher exposure to contamination, if it is accompanied by more informal animal husbandry. However, it is worth noting that this study selected for small-scale chicken producers (the median number of chickens owned was 6), so we have fewer observations to determine the full spectrum of this relationship, and whether it is truly negative or possibly U-shaped.
Second, we found that the type and location of poultry housing used were significantly associated with exposure to environmental contamination in the household environment. Our results showed a strong relationship between the distance of chicken housing from the house and risk of children’s hands being dirty and observing animal feces on the property. While we only used proxy measures of exposure to contamination, previous literature has shown that keeping chickens in the house was negatively associated with environmental enteropathy [
39] and lower height-for-age z-scores in children [
22]. Among households with coops, the strongest predictors of reducing exposure to contamination were having a coop that is separated from the household and having enclosed chicken housing. It is notable that many of these practices reduced the risk of observing animal feces on the property, since the presence of visible animal feces has been associated with an increased risk of diarrheal disease for young children [
7]. These findings suggest having coops that are enclosed and located a safe distance away from the household could potentially reduce the health risks of household members.
Third, a major contribution of this study was to identify the nuance that was not captured by proxy measures of exposure—for example, the variation in what households considered to be a “coop.” These findings can help to inform future data collection. Since simply asking about whether or not a coop exists might not be an adequate measure of animal husbandry or level of exposure to environmental contamination, researchers should consider asking about scavenging practices (is there an enclosed grazing corral, or do chickens scavenge freely?), where chickens sleep at night, location of a chicken coop relative to the main house (is it inside of a kitchen or grain store? Inside the main house or sleeping room?), type of structure, and whether or not the coop is enclosed. Our results clearly show that while having a coop might act as a proxy for an adverse health exposure, more detail regarding the type of coop can indicate protective practices.
Fourth, from the direct observation results, we showed that young children were directly affected by animal mobility and environmental conditions. Animals were frequently found inside the house and/or next to children. In two-thirds of households, index children directly touched an animal, and in 83% of households children put dirt in their mouths. As previous research has shown, in settings where animals are allowed to roam freely it is highly likely that the dirt to which children are exposed contains harmful pathogens [
14,
40]. Although we observed some potential behavioral compensation in the form of handwashing, most handwashing occurred without soap and thus was unlikely to fully eliminate any harmful pathogens. Overall, these behaviors demonstrated that children living in chicken-producing households faced regular exposure to contamination in this context, especially when animals and children were not physically separated.
Lastly, our results highlighted the factors that drive the adoption (or the lack of adoption) of specific chicken husbandry practices. While households participating in the ACGG intervention were more likely to have a chicken coop due to the intervention encouraging this practice, the qualitative data revealed a number of factors that influenced where the coop was located and how it was used in practice. Perceived threats of predation, other animals, theft, loss, and destruction of crops can drive households to keep their poultry either in a coop or inside of the household. While the majority of households recognized the potential health, cleanliness, or physical harm of animals staying in the house or in close proximity to children, there were a number of factors that prevented women from adopting different practices, especially access to feed and resource constraints. Analysis of the interview data by treatment group highlighted how the ATONU group appeared to be more sensitized to the threats of exposure to contamination, although households were not necessarily equipped with the resources to act on these perceptions. While we recognize that decision making is only one dimension of women’s empowerment, previous research from Indonesia, Bolivia, Peru, and Kenya has shown that women’s control over livestock and the productive resources needed to raise them has been associated with increased bargaining power, access to animal source foods that can benefit their children, and their empowerment [
41]. Thus, poultry interventions should be designed specially with women’s empowerment as a goal in order to ensure their control over the benefits gained from production.
Previous research has also found high levels of fecal contamination from poultry in rural Ethiopia, and that contamination has been negatively associated with health and nutrition outcomes. Using spot checks and household survey data, the study by Headey et al. (2017) found that while poultry ownership was positively associated with child height-for-age z-scores [β = 0.291], the practice of corralling poultry inside the house overnight was negatively associated with height-for-age z-scores [β = − 0.250]. The authors also found no negative associations between HAZ and corralling other livestock species indoors [
22]. A follow-up paper also found that the presence of animal feces on a household’s property was negatively associated with diarrhea and fever in Vietnam and Bangladesh, cough/cold in Vietnam, and child height-for-age z-scores in Bangladesh and Ethiopia [
11]. As part of formative research for a household nutrition and WASH trial (the Sanitation, Hygiene, Infant Nutrition Efficacy Project, or SHINE trial), Ngure et al. (2013) observed the WASH behaviors and exploratory ingestion of infants in 23-caregiver-child pairs. All chicken feces sampled later tested positive for
E. coli.
E. coli were found on 30% of the dominant hands of caregivers and on infants’ left and right hands in 11 and 5% of cases, respectively. The paper estimated that a one-year-old child in rural Zimbabwe may typically consume up to one gram of chicken feces, 20 g of soil, and 400 mL of contaminated water per day. As a result, infants would ingest anywhere from 4.7 million to 23.0 million
E. coli bacteria [
14]. Together, these previous findings support the fact that our proxy measurements related to exposure to contamination are predictive of actual exposure levels, and that these levels are associated with adverse child nutrition and health outcomes.
Nonetheless, the ACGG+ATONU evaluation did not observe acute health risks associated with an exogenous increase in chicken production in this same population [
26]. Using household survey data from 9 and 18 months of follow-up, Passarelli et al. explored the effectiveness of the African Chicken Genetic Gains (ACGG) chicken production intervention both with and without the additional ATONU nutrition promotion component. The authors observed a benefit of the ACGG intervention for children’s height-for-age and weight-for-age z-scores, but found no evidence of an increase in child morbidity [
26]. Conversely, other research has shown that exposure to animal feces does lead to acute disease outcomes, and notably, that it can also lead to chronic conditions like environmental enteric dysfunction that were not assessed in the ACGG/ATONU trial.
Recent research from the Democratic Republic of the Congo (DRC) provides a useful mixed-methods perspective that builds upon the framework of Passarelli et al. to inform our findings. Kuhl et al. conducted formative research to understand the primary sources of exposure to fecal contamination in DRC and to develop theory-driven and evidence-based interventions to reduce these exposures. To design their research activities, the authors applied the IBM-WASH framework [
42] to consider how contextual, psychosocial, and technological factors influence health behaviors across multiple levels (structural, community, interpersonal, individual, and habitual) [
24]. They found that while caregivers were often aware that children’s exposure to feces was an issue, a lack of caregiver time, financial resources, and enabling technologies (including safe child play spaces and enclosures for small animals) served as barriers [
24]. Our qualitative findings similarly support the fact that, while the specific barriers to safe environmental conditions may vary across contexts, access to improved husbandry technologies can help to alleviate the resulting health risks.
Our results have several implications for policy and practice. First, there can be negative consequences related to projects that promote increases in animal production, especially if appropriate animal husbandry practices are not implemented. This is especially true in the context of semi-scavenging systems, where an increase in animals may result a higher concentration of roaming animals depositing feces. One solution might be to move away from semi-scavenging systems towards systems with enclosures. However, as the qualitative interviews suggested, one of the disadvantages of corralling animals is the increased requirement for food, water, and veterinary care, which are often not available or accessible in remote settings. Thus, any efforts to move away from semi-scavenging systems should ensure that these inputs are available and affordable.
Previous trials have tested the effectiveness of enclosed child play areas to reduce young children’s exposure to threats such as feces from animals, but these were not shown to be effective in reducing stunting, diarrhea [
43], or enteric infections [
44]. Based on our results, perhaps addressing animal husbandry practices such as the type and location of livestock housing could provide a health benefit. Several projects designed to test different methods of limiting exposure to contamination from poultry are currently already underway [
20,
45]. In addition, training should be provided on the safe management and disposal of manure, given some research suggesting that chicken coops actually increase health risks, due to the potential for exposure to a higher concentration of manure [
46].
Overall, our findings suggest the need for greater collaboration across the nutrition, health, livestock, and agricultural sectors. Integration of social and behavioral change communication for nutrition and health would benefit from including messaging on animals in contexts where livestock rearing is common, and that livestock interventions would benefit from a greater focus on practices that minimize exposure to humans. Moreover, animals should no longer be left out of traditional water, sanitation, and hygiene interventions. As Prendergast et al. (2019) argue, practitioners must put the “A”—for animals—into “WASH” for integrated management of water, animals, sanitation, and hygiene in public health interventions [
47]. Movements such as “One Health” recognize the interconnectedness of human, animal, and environmental health, and the benefits that can be gained for all by working collaboratively across multiple disciplines [
48].
This study has several limitations. These results are not generalizable to all rural populations, but specific to the study population of chicken-rearing farmers included in our analysis. In order to maximize the number of observations in our quantitative analyses, we did not restrict all analyses to households with young children. As a result, the relationships observed in the quantitative analyses may not be directly applicable to the households for which we have qualitative data, and vice versa for the qualitative findings. Moreover, we recognize that our regression results are based on cross-sectional data, and thus could be subject to confounding; we attempted to address this by controlling for a number of potential confounders, but we do not assert that the relationships we observe are causal, merely associative. In addition, this study does not measure contamination directly (for example, as E. coli counts), but rather uses proxy measures of contamination. While direct measurement was beyond the scope of this study, we recognize the limitation of these proxies for estimating specific types and levels of pathogens. Lastly, this study only explores how chicken management practices influence waste and does not account for other animal-related health risks, like other livestock, human excrement, physical harm, fungi, and insects.
Our analysis also has several strengths; namely, the mixed-methods approach supports the research questions from several different perspectives and data sources. Our qualitative sampling by treatment group also allowed us to observe differences in behaviors that might be influenced by the intervention, while also identifying commonalities in constraints across all households. In addition, the qualitative interview data helped shed light on practical considerations for implementers of nutrition-sensitive agriculture interventions by showing the constraints that households face when considering the adoption of alternative methods.
Based on our findings, practitioners promoting animal agriculture must thoroughly provide all of the knowledge and inputs required for a safe and sustainable animal production system. Household environments with limited WASH conditions might not be able to adequately absorb an intensification of animal agriculture. However, approximately 60% of rural households in low and middle-income countries depend on livestock for their livelihoods. Thus, the pertinent question is not whether livestock should continue to be raised on a small scale, but how to do so safely.