BACKGROUND: In Ethiopia, domestic animals and their feces are not properly contained. However, the risk of exposure to zoonotic pathogens is not well documented. This study was conducted to assess animal handling practices and the risk of childhood diarrhea among rural households in northwest Ethiopia.
METHOD: This study was done among 403 randomly selected households. Information on animal handling was collected using a questionnaire and spot-check observation. The occurrence of childhood diarrhea in 14 days prior to the survey was assessed based on the reports of female head of households. Multivariable binary logistic regression analysis was performed to identify the association between animal handling practices and childhood diarrhea.
RESULT: All the female head of households had contact with animal feces when preparing fuel disks and plastering the house components with animal dung. Domestic animals shared a corral within the living space of the humans in 20% of the households. Animals entered the human living quarters and accessed foods in 32% of the households. Moreover, 24% of the children aged 24 to 59 months had diarrhea in a 2-week period prior to the survey. Childhood diarrhea was associated with domestic animals sharing the same house as humans (AOR: 3.3, 95% CI: 1.3, 8.6), presence of animal excreta in child playing areas (AOR: 2.4, 95% CI: 1.2, 4.6), contact of domestic animals with stored foods (AOR: 3.5, 95% CI: 2.0, 5.9), trapped dirt under fingernails of female heads (AOR: 3.7, 95% CI: 1.9, 7.5), open defecation (AOR: 3.24, 95% CI: 1.8, 5.9), and unprotected sources (AOR: 4.2, 95% CI: 1.1, 15.3).
CONCLUSION: Domestic animals and their excreta are not hygienically contained in the area. Animal handling practices including their excreta and the hygiene behavior of female head of households (eg, handwashing and food handling practices) should be improved to prevent childhood diarrhea.
Introduction
The livelihoods of rural communities in low-income countries largely rely on livestock.1,2 About 1.3 billion poor people all over the world rely on livestock for their livelihoods and globally, livestock contributes 40% to the agricultural gross domestic product.3 Food supply and family nutrition, income generation, soil fertility, livelihoods, transportation, and agricultural production are among the benefits of livestock contributions to rural communities.3 However, livestock rearing has critical public health problems, for instance, about 60% of all known infectious agents and 75% of emerging human pathogens are zoonotic.4 Moreover, zoonotic diseases are responsible for about one billion cases of illness and millions of deaths every year.5 The burden of zoonotic infections is disproportionately high in Africa. In the continent, there has been a 63% increase in the number of zoonotic outbreaks in the region in the decade from 2012 to 2022 compared to 2001 to 2011.6 The increase in zoonotic cases may be due to several reasons. Africa has the world’s fastest-growing population and there is a growing demand for food derived from animals including meat, poultry, eggs, and milk. The population growth is also leading to rising urbanization and encroachment on the habitats of wildlife.6,7
Moreover, fecal contamination of the living environment from human and animal sources also poses a significant risk of transmission of zoonotic pathogens in human. The living environment is defined here as an assembly of the natural and built environment which is offered to the inhabitants of the place who perform various kinds of social, cultural, religious, and economic activities.8 The predominant risk factor for human diarrhea is environmental contamination from human excreta.9,10 However, zoonotic infections can also cause diarrhea in humans and can be transferred through animal feces.11 Many pathogens, for example, Campylobacter, non-typhoidal Salmonella (NTS), Cryptosporidium, and Toxoplasma gondii substantially contribute to the global burden of diarrheal disease in humans through their spread in animal feces in the domestic environment.12 Combined, these pathogens cause close to one million deaths annually.12 Similarly, zoonotic illnesses are prevalent in northern Ethiopia. For instance, Menghistu et al reported that 53 614 (4.2%) of human cases out of 1 273 145 observed cases in the northern parts of the country were zoonoses.13 This could be due to inadequate hygiene and sanitation conditions and poor living quality due to climate change-driven poverty and civil war in the region.14,15
Rural communities can be exposed to pathogens from poorly managed animal feces.12,16 Poor animal feces disposal leads to fecal-oral transmission of zoonotic pathogens. Fecal–oral transmission is primarily occurred indirect exposure, that is, through contaminated foods and water. However, it can also operate through direct contact with feces or contaminated body parts, such as through contaminated hands16-20 as illustrated in Figure 1 which is adapted from the classic “F-diagram.”21
Figure 1.
Exposure pathways of rural communities to animal excreta (adapted from the classic “F-diagram”21). Mechanical vectors are insects such as flies that carry pathogenic microorganisms and transmit them through physical contact without supporting their development.
Hands play a significant role in the fecal-oral transmission of diseases22 and hand hygiene can reduce the risk of infection transmission.23,24 Evidence indicates that the hands, along with contact with food and other environmental surfaces, cause 60% of the spread of gastrointestinal infections and are associated with up to 50% of respiratory tract infections.25 Moreover, handwashing with soap reduces gastrointestinal and respiratory tract infections by up to 50% to 60%.25 Education about handwashing in the community reduces the number of people suffering from diarrhea by 23% to 40%24,26,27 and respiratory illnesses by 16% to 21%.24,28 However, rural communities in the study area have poor knowledge about the importance of hand hygiene and have poor awareness of effective hand hygiene procedures. For instance, a randomized controlled trial study conducted in a rural setting of northwest Ethiopia reported that 27% and 24% of women in the intervention and control groups, respectively, did not think that they always have to wash hands after visiting the toilet and 37% and 36% women in the intervention and control groups, respectively, believed that they only need to wash hands with soap when their hands are heavily dirty.29 Another study in a rural setting of northwest Ethiopia also reported that only 65 (18%) of women thoroughly rubbed all parts of their hands for at least 20 seconds and 44 (12%) of the women wiped their hands on their cloth to dry.30
It is therefore important to investigate risky behaviors of humans that lead to exposure to zoonotic agents in rural settings. This study was conducted to assess animal handling practice and its association with the risk of childhood diarrhea among rural households in northwest Ethiopia.
Methods
Study design and setting
A community-based cross-sectional study was conducted in rural settings of the east Dembiya district in May 2021. East Dembiya district is one of the 13 districts in the central Gondar zone, the Amhara national regional state, Ethiopia. The district had a total population of 210 761 of whom 192 020 (91%) and 18 741(9%) were rural and urban residents, respectively.31 The district is densely populated with an average of 277 inhabitants per km2 in 2022.32 In the district, large ruminants are the dominant livestock population followed by small ruminants and equines. The overall cattle population in the district is 166 046; sheep (8886); goats (5427); donkeys (10 717); and mules (805).33 The district had 27% and 55% coverage for clean water and traditional pit latrines, respectively.34
Sample size determination and sampling procedures
The sample size was calculated using single population proportion formula with the following assumptions: proportion of rural households who properly contained domestic animals including their excreta (p) =50% since there was no similar study in the area, level of significance (α) =5%, 95% confidence interval (standard normal probability), z: the standard normal tabulated value, and minimum detectable effect (d) =5%. The final sample size was 403 after considering a non-response rate of 5%. All households that have livestock and children under the age of 5 years in the rural kebeles (the lowest administrative unit in Ethiopia) in the district were considered for sampling. First, we chose 6 rural kebeles at random out of 28 kebeles using a simple random sampling technique. We then selected 403 households using a systematic random sampling technique. We began collecting data in households located on the right side of local administrators’ offices. Assuming that the average number of households in each rural kebele is 200,35,36 a sampling interval (K = 3) was calculated by dividing 200 by the kebele’s predetermined sample size (n = 67). Following that, a number between 1 and the sampling interval was chosen at random using the lottery method, which is known as the random start, and was used as the first number included in the sample. Then, after the first random start, every third household was sampled until the desired sample size for each kebele was reached. The sampling interval was corrected accordingly based on the presence of livestock, children under the age of 5 years, and female head of households.
Data collection tools and procedures
We used a structured and pretested questionnaire and spot-check observations to collect data. Questionnaire and observation checklists were prepared based on a review of relevant literature.16,37-39 The questionnaire was first prepared in English language and translated to the local Amharic language and back-translated into English to check consistency. The questionnaire was organized into 5 parts: (i) socio-demographic characteristics of female head of households and children, (ii) livestock ownership, (iii) animal handling and animal waste management practice, (iv) perception of animal excreta, (v) water sources, hand hygiene and defecation practice, and (vi) childhood diarrhea. Field data collectors, who were environmental health professionals interviewed female head of households about their handling practices of animals including animal excreta and observed the presence of animal excreta in the living environment and child playing areas. Female head of households were interviewed because they are responsible for childcare, food preparation, fuel disk preparation, cleaning of animal barns, and plastering of the house components in the area. Field data collectors looked at the hands of female head of households and asked the respondents to identify the area where children usually played.
Measurement of variables
In this study, we analyzed the association between childhood diarrhea and animal handling practices in rural households in northwest Ethiopia. Childhood diarrheal disease was defined as having 3 or more loose or watery stools within a 24-hour period.40 A two-week period of diarrheal disease in children41 was determined based on the response of female head of households. Animal handling practice, including handling of animal excreta, was assessed using the following questions: (i) where are domestic animals kept during day and night times? (ii) is there animal excreta in the courtyard or other open places where children spend most of their time playing? (iii) how do households manage animal excreta? (iv) do domestic animals enter to human living quarters and access prepared and stored foods? (v) do female head of households prepare fuel disks, plaster the house component, and clean animal barns with bare hands? and (vi) do female head of households wash their hands with soap or other rubbing agents after preparing fuel disks, plastering the house component, and cleaning animal barns? A description of the variables used in the study is given in Table 1.
Table 1.
Description of variables used in the study.
Data processing and analysis
We used STATA version 1445 to analyze the data. Descriptive statistics such as frequency and percentages were used to analyze data. Data were presented using frequency tables and a bar chart. We also used pictures or photos to visualize animal handling practices including their excreta. Multivariable binary logistic regression analysis was performed to identify the association between animal handling practices and childhood diarrhea. All the relevant predictors included in the questionnaire were entered to the multivariable binary logistic regression model regardless of their bivariate P-value because selecting candidate variable for the adjusted models based on their univariable P-value could lead to incorrect exclusion of potential confounders and hence led to inadequate adjustment for confounding.46,47 Handling practice of domestic animals, animal excreta in child playing areas, access of animal to the stored food, hand washing practice of female head of households after touching animals and their excreta were the exposure variables of interest entered into the multivariable model. Moreover, covariates like education status of female head of households, drinking water sources, and defecation practices were added to the model to control their confounding effect. In the adjusted model, statistically significant associations were declared based on the adjusted odds ratio (AOR) with the corresponding 95% confidence interval and P-value < .05. Model fitness was checked using the Hosmer–Lemeshow model fitness test.
Results
Demographic characteristics of study participants
Data were collected from 372 out of 403 sampled households with children under the age of 5 years and owned livestock. We did not collect data from 31(12%) of the households because female heads were not available at the time of data collection. The age of female head of households included in the current study ranged from 20 to 45 years, with a mean (± SD) age of 31.7 (± 6.4) years. One hundred twenty-eight (34%) of the female head of households were between the ages of 26 and 30 years. One hundred and sixty-five (44%) of the female head of households did not attend formal education. Moreover, 192 (52%) of the children in this study were male. The age of children ranged from 24 to 59 months, with a mean (± SD) age of 42 (± 12.5) months. One hundred fifty-eight (43%) of the children were aged between 48 and 59 months (Table 2).
Table 2.
Demographic characteristics of study participants (n = 372) in a rural setting of northwest Ethiopia, May 2021.
Livestock ownership and sanitation conditions of households
Two hundred and sixty-two (70%) of the households have cattle, 177 (48%) have ovine, 111 (30%) have equine, 358 (96%) have chickens, and 118 (32%) have pets. One hundred ninety-six (53%) of the households collected drinking water from unprotected sources (rivers, unprotected springs, or unprotected wells). Vast majority, 299 (80%) of the households collected less than 20 l/c/d of water. About two-third, 242 (65%) of the households defecated in the open field. We observed animal excreta in child play areas in 272 (73%) of the households and animals entered the human living quarters through open doors and windows to look for food in 118 (32%) of the households (Table 3 and Figure 2), through which fecal contamination of foods and food utensils occurs in the study area.
Table 3.
Livestock ownership and sanitation conditions of households (n = 372) in a rural setting of northwest Ethiopia, May 2021.
Animal handling practice
In the current study, all the households kept animals openly in the yard and public open spaces in the daytime, as shown in Figure 3. Nearly one-fifth, 74 (20%) of the households kept animals in a corral within the living space of the humans at night, 254 (68%) of the households kept animals in a barn attached to the main building, and 44 (12%) kept animals in a separately constructed barn (Figure 3). The primary reported reason to keep animals in a corral within the living space of the humans at night is fear of robberies. Thieves could steal the animals unless the owners kept them attentively in secure places.
Animal excreta handling practice
In the current study, we interviewed female head of households about their perception on the health effects of animal excreta. One-third (33%) of the female head of households did not perceive that animal excreta contains infectious agents. As illustrated in Figures 4 and 5, all the female head of households prepared fuel disks from animal dung and plastered the housing component, such as floors and walls by animal dungs with bare hands. All the female head of households who prepared fuel disks and plastered the house component with animal dung reported that they usually washed their hands after they cleaned animal barns, plastered floors/walls, and prepared fuel disks. However, one-third, 130 (35%) of them reported that they used soap to wash their hands (Figure 6) and we observed visible dirt under the fingernails among 253 (68%) of the female head of households after washing. In the area, all the households used local receptacles or “tippy tap” to wash hands (Figure 7).
Figure 4.
Fuel disks prepared from animal dung on the wall and courtyards in a rural setting of northwest Ethiopia.
Figure 5.
Cracked wall plastered with animal dungs (A) and a woman plastering floors using animal dungs with bare hands (B) in a rural setting of northwest Ethiopia.
Association between animal handling practices and childhood diarrhea
In the current study, 90 (24%) (95% CI: 20, 29%) of the children aged 24 to 59 months had diarrhea in a 2-week period prior to the survey. Childhood diarrhea in the study area was associated with how the households handle domestic animals and their excreta. Children in households where domestic animals share the same house with humans had 3.3 times more odds of diarrhea compared with children in households where domestic animals are kept outside the main building (AOR: 3.3, 95% CI: 1.3, 8.6, P: .029). The odds of childhood diarrhea was 2.4 times higher in households where animal excreta was observed in child playing areas compared with their counterparts (AOR: 2.4, 95% CI: 1.2, 4.6, P: .007). Moreover, the odds of childhood diarrhea was 3.5 times higher in households where domestic animals entered human living quarters and accessed prepared and stored foods (AOR: 3.5, 95% CI: 2.0, 5.9, P: .000). Hand hygiene of female head of households, for example, trapped dirt under fingernails was significantly associated with childhood diarrhea in the area (AOR: 3.7, 95% CI: 1.9, 7.5, P: .000). Drinking water sources and defecation practices were also significantly associated with childhood diarrheal disease in the study area. The prevalence of childhood diarrhea was higher in households who collected drinking water from unprotected sources (AOR: 4.2, 95% CI: 1.1, 15.3, P: .020) and defecated in open fields (AOR: 3.24, 95% CI: 1.8, 5.9, P: .000) compared with their counterparts (Table 4).
Table 4.
Binary logistic regression analysis to show the association between animal handling practices and childhood diarrhea in a rural setting of northwest Ethiopia, May 2021.
Discussion
This study was conducted to assess animal handling practices including their excreta and its association with the risk of infections in a rural setting of the east Dembiya district and we found that the way rural households handle animals, and their excreta increases the risk of exposure to pathogens from animal sources. In the area, domestic animals and their feces are not properly contained or separated from domestic environments. In the daytime, all the households kept animals in the yard and public open places, and in the nighttime significant proportion of households kept animals in a corral within the living space of the humans and/or in a barn attached to the main buildings. This animal husbandry and keeping practice could result in contact of rural households with animals or animal feces. Contact with animal feces and fecal contaminated living environments could pose a substantial risk to human health.48-50 For instance, children in households where domestic animals shared the same house as humans had higher odds of diarrhea and the odds of childhood diarrhea was higher in households where animal excreta was observed in child playing areas. Enteric pathogens from animal excreta could reach humans via fecal contaminated water,30,51-53 foods,30,54 hands,20,30,55 and mechanical vectors.30,56,57 In areas where open defecation is commonly practiced, animals, particularly chickens, may carry human feces and contaminate floors, food, and food utensils during scavenging, increasing the risk of disease transmission in the area. As this study depicted, children in households with no access to latrine and protected water sources had higher risk of diarrhea. Open defecation causes fecal contamination of soil and fecal contamination of soil results cross-contamination of water and foods with fecal maters, which are the main exposure pathways of diarrhea and other enteric infections.58,59
In the current study, we observed that domestic animals entered the human living quarter and accessed prepared and stored foods in 32% of the households and this was significantly associated with higher odds of childhood diarrhea in the study area. When domestic animals enter the human living quarters and access prepared and stored foods, they can cross-contaminate the floor and foods with fecal matter. Children might acquire diseases through mouthing of soil-contaminated materials (geophagy) and ingestion of fecal contaminated foods.60-63
This study revealed that all the female head of households touch animal excreta with bare hands and do not effectively wash their hands with soap in the studied region. This could be due to the rural community not perceiving that animal excreta contains pathogenic microorganisms. If a person believes that animal excreta contain infectious agents, he or she may wash hands with soap after touching it. On the other hand, a person may not effectively wash hands if he or she believes there is a low risk of infection from animals or their excreta.37,64,65 People’s beliefs and perceptions influence their behaviors as well as their ability to adapt or cope with existing health interventions.66
According to the findings of this study, all the households used animal dung to make fuel disks and to plaster the walls and floors of their homes with their bare hands. These practices may expose the living environment to infectious agents derived from animal waste.12,17,67 Hands are frequently contaminated with pathogenic microorganisms when preparing fuel disks and plastering houses with bare hands.16,68-70 Because rural communities do not effectively and frequently wash their hands with soap, the problem of hand contamination with animal feces is recognized as a public threat.29,71,72 We also observed dirt under the fingernails of more than two-thirds of the female head of households after they washed their hands. Dirt trapped under fingernails was significantly associated with childhood diarrhea in the study area. This association can be justified that the area beneath the fingernails that trapped dirt can harbor disease causing pathogens. These pathogens could contaminate foods during preparation or serving.30,73,74
In the current study, about one-third of the female head of households did not perceive that animal excreta contains infectious agents. The perception might negatively affect their attitudes or beliefs about the potential harms of animal excreta. It is widely accepted that perception is fundamental for triggering behavioral changes.75 Those who downplay the potential harm of animal excreta or a risk event are less likely to take targeted actions to prevent the event, for instance, they may not hygienically manage animal excreta, may not contain animals, and may unnecessarily touch animal excreta with bare hands.76 On the other hand, individuals will manage animal excreta hygienically, will contain animals or will avoid unnecessary touching of animal excreta and surfaces in close proximity to a source of contaminants, and will wash their hands frequently if they believe animal excreta contains infectious agents.77-79
This study provides important information on the animal handling practices of rural households that increase the risk of exposure to zoonotic agents and this information could lead to tailored public health and veterinary public health messages and interventions for the participants. However, the self-reported data may not be reliable since the study subjects may make the more socially acceptable answers rather than being truthful and they may not be able to assess themselves accurately, which might result in reporting bias.
Conclusion
Domestic animals and their excreta are not properly contained in the study area. This could result in contact of rural households with animals and/or animal feces, which may pose a substantial risk to human health. Containment of animals and their excreta is needed in the area to prevent the domestic environment from fecal contamination. Because the rural communities have no alternative clean energy sources, they rely on biomass fuel energy sources, for example, fuel disks. This culturally important practice results in close contact of rural communities with animal excreta. Making animal excreta handling practices safer is very important in the area. For instance, instead of preparing fuel disks with bare hands, it is possible to use animal dung for biogas energy production. Since biogas technology is a good means of treating human and animal wastes, the local health department in collaboration with other energy sectors needs to help the community to construct a small-scale biogas plant at the household level. In addition to good animal husbandry practice (ie, containment of animals and their excreta), the hygiene behavior of female head of households such as handwashing behaviors and food handling practices need to be improved to minimize the risk of food and hand contamination with animal excreta. Moreover, water and sanitation services should be improved in the area.
Acknowledgements
The authors are pleased to acknowledge the University of Gondar, One Health Eastern Africa Research Training (OHEART) program at the Ohio State University, Global One Health Initiative (GOHi) and National Institutes of Health (NIH) Fogarty International Center for their support.
© The Author(s) 2024
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Author Contributions
ZG designed the study, conducted data analysis, and produced the initial draft of the manuscript. BDB supervised data collection. AWY, JL, and MB contributed to conceptualizing the study. All authors approved the final version of the manuscript.
Availability of Data and Material
Data will be made available upon requesting the primary author.
Consent for Publication
Informed consent was obtained from female head of households to publish the information/image(s) in an online open-access publication.
Ethics Approval and Consent to Participate
Ethical clearance was obtained from the Institutional Review Board of the University of Gondar (reference number: V/P/RCS/05/1933/2020). There were no risks due to participation and the collected data were used only for this research purpose with complete confidentiality. Written informed consent was obtained from female head of households. All the methods were carried out in accordance with relevant guidelines and regulations.
