Is living with cats unhealthy

Is It Unhealthy To Have A Lot Of Cats?

No, it is not unhealthy to have a lot of cats. In fact, many people find companionship and joy in owning multiple cats.

Cats are relatively low-maintenance pets, and as long as they are well-cared for, they can live healthy lives. Of course, like any pet, there are some health risks associated with owning cats, but these can be easily mitigated with proper care and attention.

Is it unhealthy to have too many cats?

There is no definitive answer as to whether or not it is unhealthy to have too many cats, as the answer largely depends on the individual cats and their individual lifestyles. Some cats may have a healthy appetite and be able to thrive with a large number of cats, while others may have difficulty digesting a high number of food sources and may experience health problems as a result.

Additionally, some people may find that having too many cats can be disruptive to their home environment, as cats tend to mark their territory and create a lot of noise.

Can too many cats in a house make you sick?

There is no scientific evidence to support the claim that having too many cats in a home can make people sick. However, there is some evidence to suggest that cats can carry parasites and bacteria that can be harmful to humans, and that a large number of cats in a home can cause a greater concentration of these substances.

Additionally, cats can be destructive and may spread harmful bacteria and parasites through their urine and feces. If you are concerned that your home may be too cats, it may be best to consider getting rid of some of your cats or adopting a smaller number.

Is living with cats unhealthy?

It is generally accepted that living with cats is healthy for both humans and cats. Cats are obligate carnivores, meaning that their body is designed to digest and use meat as the primary source of energy.

This means that cats are unable to digest grains, vegetables, or other plant-based sources of nutrition, which is why they are such good companions for people who have allergies or sensitivities to other types of animals. Cats also require minimal grooming, which is one of the main reasons they make great house pets.

Is having 10 cats too many?

It depends on individual circumstances. Some people may find 10 cats to be a manageable and happy family size, while others may find it to be too many.

Ultimately, it is up to the individual to decide what is best for them and their cats.

There are a few factors to consider when determining how many cats a family should have. The first is the size of the home.

If the home is small, having only one or two cats may be enough. If the home is larger, having more than one cat may be necessary.

The second factor to consider is the personality of the cats. Some cats are more social than others and may not be able to handle being alone.

Others are more independent and may be able to live without human companionship. The final factor to consider is the age of the cats.

Younger cats may be more active and need more space than older cats.

How many cats can you have before its considered hoarding?

The American Animal Hospital Association (AAHA) defines hoarding as an abnormal and persistent accumulation of animals or objects that results in significant distress or impairment to the individual or to those who must live in the same environment. In order to be diagnosed with hoarding, individuals must have five or more animals in their possession, as well as evidence that the animals are not being properly cared for or are in danger of being harmed.

While there is no set number of animals that can be hoarded without becoming a problem, research suggests that as few as two animals can be signs of an issue, and that hoarding can occur with as many as 150 animals. It is important to note that not all animals in a hoarding situation are affected in the same way; some animals may be neglected or have health issues, while others may be housed in excessively cramped or dirty conditions.

Because hoarding is an umbrella term that can encompass a wide range of behaviors, it is important for anyone who suspects they may be living with a hoarder to seek help from a professional. Hoarding can cause serious psychological and physical harm to those affected, and intervention is the best way to ensure that affected individuals are able to live healthy, fulfilling lives.

Is owning 3 cats too much?

It largely depends on the individuals lifestyle and preferences. Some people may feel that owning three cats is too much, while others may find it to be a fun and entertaining addition to their lives.

Ultimately, it is up to the individual to decide how many cats they feel comfortable owning.

How many cats is too many by law?

The number of cats that a person may own is regulated by law in some jurisdictions. In most cases, a person may only own three cats.

Some jurisdictions, such as California, have laws that limit the number of cats a person may own to six. Some people choose to have more than three cats, but they are still in violation of the law if they have more than six cats.

What can I do if my neighbor has too many cats?

There are a few things that you can do if your neighbor has too many cats. The first thing is to talk to them and see if they are aware of the issue and if they are willing to work together to resolve it.

If they are not willing to work together, you can try to get them to spay or neuter their cats. You can also try to talk to the city about regulating the number of cats that a household can have.

Is cat saliva harmful to humans?

There is some debate about whether or not cat saliva is harmful to humans. Some believe that the saliva contains bacteria that can cause oral infections in humans, while others believe that the saliva doesnt contain any harmful bacteria.

Some people also believe that the saliva can contain elements that can irritate the skin. Ultimately, the jury is still out on whether or not cat saliva is harmful to humans.

Why you shouldnt have a cat?

A cat can be a wonderful pet, but there are some reasons why you might not want one.

Cats are independent and often require a lot of attention. This can be a hassle if you work full-time or have other responsibilities.

Cats require a lot of space. If you dont have enough room, a cat can be a nuisance.

Cats can be messy. Theyll often want to be close to you, which means theyll leave trails of hair and dirt behind.

Cats can be unpredictable. They might not like being handled or left alone, and they may be difficult to housetrain.

Why cats are not good pets?

There are a few reasons why cats are not typically considered good pets. First, cats are solitary animals and do not typically enjoy being around other people or other animals.

They also require a lot of attention and care, which may not be feasible for everyone. Additionally, cats can be very finicky about their food and water, and may not be easy to housetrain.

Can cat hair make you sick?

There is no scientific evidence to suggest that cat hair can make people sick, but some people may be concerned about this because of the rumors and myths that circulate online. In general, it is not advisable to clean your cats hair with harsh chemicals or brush it too vigorously, as this may irritate their skin and cause them to shed more hair.

Conclusion

It depends on a variety of factors, including the health of the individual cats and the overall environment in which they are kept. However, it is generally agreed that having a large number of cats can pose some health risks, both for the animals and for the people who live with them.

For example, large numbers of cats can lead to increased stress levels and decreased immunity, which can in turn lead to more sickness and disease. Additionally, living in close quarters with many cats can also increase the chances of exposure to toxoplasmosis, a potentially dangerous parasitic infection.

Exposureto Animal Feces and Human Health: A SystematicReview and Proposed Research Priorities

Environ Sci Technol. 2017 Oct 17; 51(20): 1153711552.

Exposureto Animal Feces and Human Health: A SystematicReview and Proposed Research Priorities

Department of EnvironmentalHealth, Emory University, Atlanta, Georgia 30322 United States

Received 2017 Jun 5; Revised 2017 Sep 7; Accepted 2017 Sep 19.

This is an open access article published under a Creative Commons Attribution (CC-BY)

, which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited.

Abstract

Humans can be exposed to pathogensfrom poorly managed animal feces,particularly in communities where animals live in close proximityto humans. This systematic review of peer-reviewed and gray literatureexamines the human health impacts of exposure to poorly managed animalfeces transmitted via water, sanitation, and hygiene (WASH)-relatedpathways in low- and middle-income countries, where household livestock,small-scale animal operations, and free-roaming animals are common.We identify routes of contamination by animal feces, control measuresto reduce human exposure, and propose research priorities for furtherinquiry. Exposure to animal feces has been associated with diarrhea,soil-transmitted helminth infection, trachoma, environmental entericdysfunction, and growth faltering. Few studies have evaluated controlmeasures, but interventions include reducing cohabitation with animals,provision of animal feces scoops, controlling animal movement, creatingsafe child spaces, improving veterinary care, and hygiene promotion.Future research should evaluate: behaviors related to points of contactwith animal feces; animal fecal contamination of food; cultural behaviorsof animal fecal management; acute and chronic health risks associatedwith exposure to animal feces; and factors influencing concentrationsand shedding rates of pathogens originating from animal feces.

Introduction

Nearly two-thirds ofhuman pathogens and three-quarters of emergingpathogens are zoonotic in origin.^1,2 While researchhas focused on zoonotic transmission of respiratory and vector-bornepathogens, such as Ebola and West Nile Virus, less attention has beengiven to pathogens found in animal feces that are transmitted viawater, sanitation, and/or hygiene (WASH)-related pathways, as illustratedby the classic F-diagram ().³ Accordingto the Food and Agricultural Organization (FAO), domesticanimals such as poultry, cattle, sheep, and pigs generate 85% of theworlds animal faecal waste, proportionally a far greater amountthan the contribution by the human population; the fecal productionrate can total to 2.62 10¹³ kg/year.⁴ Insufficient separation of animal feces from human domesticenvironments, common in low-income countries, can lead to fecal-oraltransmission of zoonotic pathogens through direct contact with humansand/or fecal contamination of fingers, food, and water sources.

TraditionalF-Diagram showing potential fecal-oral transmissionpathways. Adapted from Wagner, E.; Lanoix, J., Excreta disposal forrural areas and small communities. Monograph Series WorldHealth Organization.1958, 39, 182. Copyright 1958, World Health Organization.

Several pathogens of zoonotic origin are associatedwith acutegastrointestinal symptoms that can arise from contact with animalfeces.⁵ Children may experience long-termgrowth shortfalls after exposure to these pathogens, and pregnantwomen and the immunocompromised may also experience severe and/orlong-term adverse health effects after infection with pathogens carriedin animal feces.⁶⁹ Approximately one-third of deaths among children under five yearsdue to diarrhea in the Global Burden of Disease 2015 report are attributedto pathogens that can be found in animal feces.¹⁰ While some studies seek to identify a relationship betweenanimal contact and diarrhea, not all etiologies of diarrhea are transmittedthrough animal feces. While many important viral enteropathogens (e.g.,rotavirus) have limited zoonotic transmission, animal feces may playan important role in the transmission of some important etiologiesof childhood diarrhea, such as Cryptosporidium, whichsubstantially contributes to the childhood burden of diarrheal diseaseand has been associated with severe acute and long-term clinical manifestations,including child growth faltering.¹¹ Unlikerotavirus, there is currently no vaccine for Cryptosporidium and treatment options are limited and often unavailable in developingcountries. Thus, preventive measures for such zoonotic pathogens areimportant for reducing disease burden. Though the total contributionof zoonotic transmission is unknown, it may be substantial, and itmay vary by the virulence and animal host(s) of the specific etiologicagent, geographic and cultural context, and environmental conditions.¹²

Recent reviews, predominantly using observationaldata, suggestthat improved WASH conditions are associated with better childrenshealth outcomes.¹³¹⁵ Yet randomized controlled trials in low-income ruralsettings have demonstrated mixed effects of such interventions ondiarrhea, soil-transmitted helminth (STH) infection, trachoma, andstunting.¹⁶²³ Even comprehensive WASH interventions may be insufficient to preventgrowth faltering in rural settings.²⁴ Onepossible reason for the lack of health effects is suboptimal programfidelity and adherence, yielding less than universal coverage anduse.²⁵ An alternative explanation is thatbecause sanitation interventions have focused primarily on containmentof human excrement, the lack of evidence for healtheffects in large intervention trials could be due to persistent exposureto fecal pathogens of animal origin among the studypopulations.^5,26,27 A recent systematic review and meta-analysis noted that domesticpoultry and livestock exposure are associated with diarrheal illnessin humans;⁵ we expand on this review byexploring the risk of animal exposure on diarrhea, child growth outcomes,environmental enteric dysfunction (EED), pathogenic infection, trachoma,and STH infection.

Human exposure to animal feces is more commonin developing countrieswhere domestic animals and their animal feces may not be properlycontained or separated from domestic environments. Though childrenand adults in high-income countries (HIC) can also be exposed to animalsand/or their feces, potentially causing bacterial, helminth, and/orprotozoan infections,²⁸³⁴ the risk may be greater in low- and middle-income countries (LMIC),where domestic animal ownership and middle- and small-scale animalproduction is more common in both rural and urban households³⁵ compared to households in HIC.

The primaryobjective of this systematic review was to examinewhat is known about human health impacts of exposure to poorly managedanimal feces transmitted via WASH-related pathways in LMIC. We identifiedand synthesized existing literature to assess the extent to whichexposure to poorly managed animal feces could affect health outcomesin humans. We modified the traditional F-diagram tofocus on animal feces exposure in households and small-scale animaloperations, in households with pets, and in communities with synanthropicrodents; through this lens we propose research priorities to betterunderstand human exposure to poorly managed animal feces. We identifiedinterventions that have been used to control human exposure to animalfeces and summarized what is known about their effectiveness in reducingthe presence of animal feces in the environment, preventing humanexposure to animal feces, and/or limiting negative human health outcomes.Based on this review, we identified a set of priority research areasto improve our understanding of the human health burden associatedwith exposure to animal feces, with the ultimate goal of identifyingpotential control measures to reduce this burden in LMIC.

Materials andMethods

Search Strategy

To assess the impacts of animal feceson human health, we searched for papers with terms for animals,feces, exposure, and humans (Supporting Information (SI) 1, p. 2). The search was limited to English-and Spanish-language studies and included papers published beforeOctober 3, 2016. We searched in the following databases: PubMed, Webof Science, Cochrane Library, EMBASE, and CAB Direct. We also includeda partial search of the Environmental Sciences and Pollution Management(ESPM) database, but due to host database server challenges at thetime of the search, 26% of full search results from this databasecould not be downloaded. We conducted a search of gray literaturein International Food Policy Research Institute (IFPRI), ConsultativeGroup on International Agricultural Research (CGIAR), InternationalLivestock Research Institute (ILRI), Food and Agriculture Organizationof the United Nations (FAO), U.S. Centers for Disease Control andPrevention (CDC), and the World Health Organization (WHO). We alsoincluded papers from personal libraries and literature collections,including a limited number of highly relevant studies that were publishedbetween October 2016 and September 2017. We included experimentaland observational study designs. All study settings and populationswere eligible for inclusion.

Selection of Studies

Search resultswere catalogedand organized in EndNote X7 (Clarivate Analytics, Boston, MA). Fourresearchers (GP, JS, LM, BW) examined every publications titleand abstract to assess if the publication met one or more of the followinginclusion criteria: (a) human exposure to poorly managed animal feces;(b) negative human health outcomes from exposure to animal feces (e.g.,diarrhea, gastroenteritis, EED, trachoma, STH infections, child growth(anthropometric) outcomes, and infection by zoonotic pathogens); and(c) animal feces contamination of the environment (e.g., water orfields). First, the four researchers all independently reviewed aninitial 150 publications to ensure consistency among the study teamwhen determining if papers met the above inclusion criteria. Afterward,the remaining search results were divided equally among the four researcherswho independently reviewed the title and abstract of their designatedsearch results. We define poorly managed feces as animal feces thatare not contained or separated from human domestic and public environments.We define exposure to animal feces as behaviors related to handlinganimal feces (e.g., spreading manure on fields or removing domesticatedcat feces from litter) and human activity conducted in close proximityto animals and their feces (e.g., children playing on the ground wherechickens also roam). While identifying publications that met the inclusioncriteria, we simultaneously identified papers that discussed animalhusbandry practices and animal feces/manure management, and we identifiedpapers that discussed control measures for reducing human exposureto animal waste. If researchers were unable to make a decision aboutincluding or excluding a publication during the title and abstractreview process, the publications features were discussed amongthe four researchers and a decision was made.

We excluded publicationsthat discussed one or more of the following: no exposure to animalsor animal feces, exposure to animal or animal feces in occupationalor industrial settings (e.g., commercial farms), exposure to animalurine, animal health outcomes, human respiratory health outcomes,and diseases related to exposure to insect feces (e.g., Chagas Disease).We excluded papers from HIC because piped sanitation and piped waterinfrastructure are prevalent, and we wanted to explore how humansare exposed to animal feces in LMIC where sanitation and water infrastructuremay be limited or nonexistent.

Two researchers (GP, JS) reviewedthe full-text of publicationsthat met the inclusion criteria to confirm the publication met theinclusion criteria as well as one of the following: (a) risk factors,such as exposure to or contact with animals or animal feces, associatedwith zoonotic infection; (b) animal husbandry practices/behaviorsand information about animal feces management; or (c) control measuresor interventions aimed at reducing human exposure to animal waste.Other areas of potential interest that were beyond the scope of thisreview include papers that focused on the epidemiology and etiology,antibiotic resistance, or animal shedding of zoonotic fecal pathogens.No publications from the gray literature met our inclusion criteriafor this review.

Data Extraction and Synthesis

Datafrom papers deemedto meet the inclusion criteria were extracted into a prepiloted extractionform, which included research objectives, key findings, descriptionsof study populations, descriptions of health outcomes, and descriptionsof exposures to animals and/or their feces (SI Table S1). During synthesis, data were classified by healthoutcomes, pathogens of concern, exposures to common domestic animals,and regions in which the studies were conducted. Health outcomes,such as diarrhea and trachoma, were assessed by individual studiesin a variety of methods including recall, health professional diagnosis,and/or testing. Publications that discussed control measures to removeor reduce the presence of animal feces were identified and classifiedaccording to control approach. We did not conduct a meta-analysisor a risk of bias assessment because of the heterogeneity of methods,exposures, and outcomes used across the studies included in the review.We conducted the systematic review according the evidence-based minimumrequirements identified by the Preferred Reporting Items for SystematicReviews and Meta-Analyses (PRISMA) checklist (SI Table S2).³⁶

Results &Discussion

Our search yielded 12425 unique results,of which the fulltexts of 329 articles were reviewed. A total of 62 publications metthe inclusion criteria (SI Figure S1).Characteristics of publications included in this review are summarizedin Table 1 (regions,health outcomes, and animals) and Table 2 (pathogens).

Table 1

Summaryof Characteristics of Studies(n = 62)^a Included in Reviewof Potential Health Impacts from Exposure to Animal Feces

Table 2

Summary of PathogenCharacteristicsof Studies (n = 62)^a Includedin Review of Potential Health Impacts from Exposure to Animal Feces

Most of the studies we identified for this reviewwere cross-sectionalstudies (n = 42); other study designs included case-control(n = 3), experimental and quasi-experimental (n = 2), longitudinal (n = 2), cohort (n = 4), and qualitative studies (n = 1).The remaining publications, reported on secondary data analyses (n = 1), a conceptual model (n = 1), orsystematic review/meta-analysis (n = 1). Study populationsincluded children, adults, animals, and environmental samples (e.g.stool, blood, water). Most of the studies were conducted in Asia (n = 30), but this review also includes studies conductedin Africa (n = 20), South America (n = 12), and Oceania (n = 1) as well; one literaturereview included papers from around the globe. Relevant characteristicsof the publications included in this review are presented in SI Table S3.

Impact of Exposure to Animalsand/or Animal Feces on Human Health

Most studies assessedexposure to animal feces based on contactwith or presence of animals in the environment. Few (n = 9) measured direct human contact with animal feces per se. Weillustrate the role of exposure to animal feces and/or contact withor presence of animals and its impact on WASH-related health outcomesin . Belowwe synthesize findings for each of the health outcomes considered,including diarrhea, child growth, EED, pathogen isolation in humanstool (bacterial, protozoan, microsporidian, viral), trachoma, andSTH infections.

Impact of exposure to animal feces and/or contact withanimalsto human health.

Diarrhea

Heterogeneouseffects of exposure to animalsand animal feces on human diarrheal illness were observed among the18 studies examining diarrhea in this review. A systematic reviewand meta-analysis found consistent evidence of a positive associationbetween domestic poultry and livestock exposure and diarrheal illness.⁵ Animals housed in living quarters increased therisk of diarrhea and/or infection by enteric pathogens in severalstudies and increased the risk of longer durations of diarrhea.³⁷⁴² Living with chickens infected by zoonotic enteric pathogens increasedthe risk of diarrhea among children in Lima, Peru.⁴⁰

No associations were found between the presence ofanimals or animal feces and diarrhea or enteric infection in urbanAccra, Ghana and rural Odisha, India.^43,44 An assessmentof Demographic Health Surveys (DHS) from 30 sub-Saharan African countriesfound an inconsistent relationship across contexts between childhooddiarrhea and household livestock ownership; 13 countries indicatedlivestock ownership as a risk factor but 10 countries exhibited aprotective association likely due to confounding with socio-economicstatus and varied access to improved water and sanitation infrastructure.²⁶ Cattle ownership in Madagascar was found tobe protective against severe diarrhea.⁴⁵

Child Growth

Exposure to fecal pathogens of animalorigin may impair child growth, although these effects are not consistentlyfound in the literature (n = 8). For most studies,child growth was measured using anthropometric measurements to calculatestandardized age- and sex-specific height-for-age Z-scores (HAZ),weight-for-age Z-scores (WAZ), and weight-for-height Z-scores (WHZ)to classify levels of stunting, being underweight, and wasting, respectfully.In a study in rural Ethiopia, poultry ownership was positively associatedwith child HAZ, but corralling poultry indoors at night was negativelyassociated with child HAZ; no association was found between corrallinganimals indoors at night and child HAZ for other animal species (cattle,goats, sheep, pack animals).^46,47 Several studies foundno association between livestock ownership and child HAZ and WAZ,though livestock diseases might be related to lower child HAZ andWHZ in some groups in rural Kenya.^44,48 The presenceof animal feces in household compounds was negatively associated withchild HAZ in rural Bangladesh and Ethiopia.⁴¹

A recent analysis of agricultural, nutritional, and interviewdata, along with anthropometric measurements from sub-Saharan Africa,revealed inconsistent evidence for the effects of animal ownershipand consumption of animal-sourced foods on child growth. Childrenin households that consumed animal-sourced foods in Rwanda, Uganda,and Malawi had better anthropometric scores (WHZ and HAZ) than thosethat did not consume animal-sourced foods; however, children who consumedanimal-sourced foods in Ghana and Senegal had lower relative anthropometricscores (WHZ (Ghana only) and HAZ).⁴⁷ Theanalysis of DHS from 30 sub-Saharan African countries similarly foundinconsistent results, but data revealed a slight protective effectof the number of animals owned on child stunting.²⁶

Child growth effects may be mediated by animal containmentandhousing practices. Children in households that kept poultry outsidethe home had significantly better HAZ compared to those in householdsthat kept poultry inside the home in rural Ethiopia.⁴⁶ Similarly, in rural Bangladesh the odds of being stuntedwere higher among children in households with animals corralled insleeping quarters versus households where animals were not corralledin sleeping quarters.⁴⁹

EnvironmentalEnteric Dysfunction (EED)

Two studiesin this review suggest that exposure to animals and animal feces mightincrease the risk of EED, also referred to as environmental enteropathy,an impairment of intestinal function evident in many young childrenin low-resource settings that leads to growth faltering and cognitiveimpairment.⁵⁰⁵⁵ Children sleeping in households with animal corrals in the sleepingquarters had significantly higher EED scores (calculated from fecalbiomarker measurements) than those without animals in the sleepingquarters in rural Bangladesh.⁴⁹ Among ruralMalawian children, animals sleeping in the same room as the children,combined with use of potentially contaminated water sources and theabsence of household pit latrines, was positively associated withEED.⁵⁶

Pathogen Isolation in HumanStool

Several studies examinedassociations between exposure to animals and/or their feces to subsequentisolation of pathogens in human stool.

Among bacteria, Campylobacter spp. infection was common among children livingwith domesticated animals, especially poultry, compared to childrennot living with animals, because children were likely to be in directcontact with chicken feces.^5,42,57,58 A study in peri-urban Peru notedthat chickens, dogs, and cats were commonly infected with C. jejuni.³⁷ Genetic analysisof animal and child stool samples in semirural Ecuador found that C. jejuni sequence types were identical between childrenand chickens, dogs, guinea pigs, and rabbits; atypical enteropathogenic Escherichia coli (aEPEC) sequence types were identical betweenchildren and pigs, dogs, and chickens.⁵⁹

Among protozoal pathogens, Cryptosporidium spp., Giardia spp., and Entamoeba spp. have beenassociated with exposure to animals. Cryptosporidium spp. identification in child stool was associated with the presenceof chickens in the household in Cambodia.⁶⁰ In urban Kenya, a study among HIV/AIDS patients found that cryptosporidiosiswas associated with contact with animals,⁶¹ and in urban Democratic Republic of the Congo, exposure to farmpigs increased the odds of Cryptosporidium infectionamong HIV/AIDS patients.⁶² Individualswith household pets were 2.6 times more likely to be infected with G. duodenalis assemblage A compared to those without petsin Malaysia.⁶³ A study of outpatient stoolsamples from an urban hospital in Yemen found that contact with animalsincreased the risk of any intestinal protozoan infection (G. duodenalis, E. histolytica, E. dispar) and single infection with Entamoeba spp.; single infection of G. duodenalis was not associated with contact with animals.⁶⁴ A study in rural China among individuals with pulmonarytuberculosis found that those raising chickens, ducks, or pigs, andworking farmlands barefoot to be significantly associated with protozoan(Blastocystis hominis, Entamoeba spp., Trichomonas hominis) and helminthic infections(hookworm, Trichuris trichiura, Ascaris lumbricoides, Clonorchis sinensis), respectively.⁶⁵

Immunocompromised populations are particularlysusceptible to infectionby microsporidia, specifically Enterocytozoon bieneusi. A study of microsporidiosis in HIV patients in hospitals in Lima,Peru found that contact with duck or chicken fecal droppings was arisk factor for infection with the E. bieneusi genotype,Peru-1, as were lack of running water, flush toilets, or garbage collection.⁶⁶ Among HIV/AIDS patients in Kinshasa, DemocraticRepublic of the Congo, exposure to farm pigs was associated with higherodds of infection with E. bieneusi or Cryptosporidium spp.⁶² In urban India, a study amongHIV-positive individuals found that contact with pets and other animalsincreased the odds of infection with enteric pathogens, includingbacterial, protozoan, helminthic, and microsporidian species.⁶⁷

Several studies reported no associationbetween presence of orcontact with domestic animals or rodents and their feces and pathogenicinfection with certain species of bacteria,^43,68,69 protozoans,^60,64 and viruses.⁷⁰

Trachoma

Exposure to animals andanimal feces mightincrease the risk of trachoma, an infection by the bacterium Chlamydia trachomatis, by potentially providing breedingsites for flies that propagate the infection. The studies in thisreview do not assess if flies carrying C. trachomatis actually bred on animal feces; the presence of human feces in ornear study sites may be a confounding factor. In rural Nigerian households,the presence of animal feces in household compounds was a risk factorfor trachomatous inflammation-follicular (TF), a precursor conditionto blinding trachoma.⁷¹ In rural Ethiopianhouseholds, active trachoma, measured by TF and trachomatous inflammation(TI), was more common in children in families who specifically housedtheir cattle in their sleeping quarters, though cattle ownership wasnot associated with trachoma risk.⁷² Anotherstudy in rural Ethiopia also noted that the presence of animal fecesnear the house was associated with active trachoma in at least onechild in the study households.⁷³

Soil-TransmittedHelminth (STH) Infection

Evidencesuggests that exposure to animals and animal feces, particularly thoseof cats and dogs, leads to an increased risk of STH infections. Individualsin urban, low-income households in Brazil were more likely to be diagnosedwith hookworm-related cutaneous larva migrans (HrCLM), a parasiticskin disease caused by feline or canine hookworms, if animal feceswere present in the compound.⁷⁴ Dog ownersin Chile and Argentina displayed positive human seropositivity to Echinococcus granulosus and Toxocara canis, respectively.^75,76 Similarly, the presence of dogsand their feces significantly contributed to children being seropositivefor toxocariasis in Sri Lanka.⁷⁷ Pregnantwomen in Bali exposed to oocyst-positive cat feces in their environmentwere more likely to be serologically positive for Toxoplasmagondii than pregnant women who were not exposed to oocyst-positivecat feces.⁷⁸

Pathways of Exposure toAnimal Feces

The means of characterizing exposure to animalsand animal fecesvaried considerably in the literature we reviewed. Researchers assessedpresence of or contact with animals, presence of or contact with animalfeces, animal ownership, environmental contamination of public anddomestic spaces, and risky husbandry practices (e.g., using cow dungas cooking fuel and slaughtering practices) through structured observationsand semistructured interviews. Most publications assessed impactsof raising poultry (chickens, duck, geese, quail) and cattle; studiesalso assessed impacts of exposure to goats, dogs, sheep, cats, pigs,buffalo, synanthropic rodents (mice, rats), and less commonly, horses,guinea pigs, and rabbits.

We reviewed the literature to identifythe extent of human-animalcontact with attention to regional, cultural, and urban-rural contextualdifferences. The evidence of human-animal contact between regionaland cultural contexts revealed anecdotal study site-specific information,but did not provide a sufficiently generalizable set of behaviors.The comparative risk of exposure to animal feces in urban comparedto rural areas is therefore difficult to determine.

illustratesthe pathways for human exposure to zoonotic fecal pathogens usinga modified F-diagram. We distinguished transmission pathways dependenton animal species and behaviors versus pathways dependent on humanbehaviors and practices; the pathways corresponding to human behaviorsare independent of the animal species that is the source of the fecalexposure. Below we present the evidence around each of the exposurepathways highlighted in ; the numbers correspond to the pathways in .

Modified F-diagram showingtransmission routes of animal fecesto humans. Adapted from Wagner, E.; Lanoix, J., Excreta disposal forrural areas and small communities. Monograph Series WorldHealth Organization.1958, 39, 182. Copyright 1958, World Health Organization.

Pathway 1: Contamination of Water Sources

Contaminationof both source and stored drinking waters is an important human exposureto animal feces. Several studies demonstrated that open ponds andsurface waters are more susceptible to contamination by animal feces,though significant contamination has been observed in public and privatetube wells also.^27,79,80 In rural India, higher sheep populations in villages increased theodds of detecting higher concentrations of Cryptosporidium spp. in public ponds.⁸¹ Humans sharingwater sources with livestock represents a particularly risky behaviorin low-income settings.^79,8284

Pathway 2: Contamination of Soil

Many of the pathwaysfor exposure to animal feces occur directly in and around the domesticenvironment. We found consistent evidence of animals contaminatingfields and soil by indiscriminate defecation. Positive associationswere found between seropositivity for helminths and soil contaminatedby dog and cat feces in households and public settings (e.g., parks,playgrounds).^75,77 Stray, free-roaming cats anddogs contaminated domestic and public environments with Toxoplasma spp. and helminth eggs in rural and urban communities in LMIC.^29,31,85,86

Ruminant fecal markers were observed in soil and hand rinsesamples from households that did and did not own ruminant speciesin Bangladesh.^87,88 Widespread chicken feces contaminationhas been observed in household kitchens and backyards;⁸⁹ chickens might therefore be of particular concernin household environments, because children (up to five years old)have been observed to have contact with chicken feces an average of2.9 times in a 12 hour span.⁵⁸

Soilwas contaminated during the use and disposal of manure onagricultural or residential areas as fertilizer.^84,90,91 Manure effluents may also be dischargedfrom cattle storage, potentially contaminating surrounding land.⁸²

Pathway 3: Contamination of Food

In the United Statesand other HIC, where human waste is arguably well-controlled, theburden of enteric disease is largely related to foodborne or animal-associatedoutbreaks. Most of the important bacterial pathogens of foodborneillness in the United States are transmitted by animals.⁹² Even in the case of sophisticated human wastecontainment, pathogens from poorly managed animal feces can directlycontaminate food during the food production process, particularlyrelated to slaughter. As such, foodborne exposure to animal fecesin LMIC is likely an important pathway that warrants further research.

Our search, however, uncovered few studies (n =2) that reported on the contamination of food from animal feces. Campylobacter spp. contamination was found in 34.6% of samplesof various types of goat meat collected in the Democratic Republicof Congo.⁹³ Fresh produce collected froma suburban market in Vietnam was widely contaminated with parasiteova excreted by both humans and animals.⁹¹

Pathway 4: Contamination via Flies

Flies, potentialvectors of fecal contamination, may be associated with negative healthoutcomes. Three studies specifically examined flies as vectors fortrachoma infection^71,73 and diarrheal illness.³⁹ In rural Ethiopia and Nigeria, the presenceof flies in the home (due to presence of cows, waste disposed nearthe home, and defecation near the home)⁷³ and on the face⁷¹ was positively associatedwith trachoma. In rural India, higher fly densities were associatedwith longer durations of diarrhea.³⁹ Also,the absence of animals in or near the home was protective againsthigh fly densities. An additional study in rural Indian householdsassessing the presence of cowsheds and the presence of flies notedthat fly counts were higher in households owning cowsheds versus thosewithout cowsheds.⁴⁴

Pathway 5: Contaminationof Human Hands

Cohabitationof animals and humans is a common practice in LMIC and is one of theprimary risk factors we identified in this review. Though most studiesdid not explicitly observe human-to-animal contact, we used animalownership and the presence of animals in and around households asa proxy for direct contact with animals, a pathway important for exposureto animal feces. In many domestic settings, livestock, including cattleand poultry, were housed in the familys sleeping quarters,^46,49,64,90 increasing the potential for contamination in the household environment.Households kept livestock in sleeping quarters at night to protectthem from thieves or from being hunted by other animals.⁹⁰ Poultry were generally allowed to scavenge forfood inside and outside living quarters in rural villages in Bangladesh.⁹⁰ Household members directly contacted animalfeces when handling manure, sometimes handling cow manure from E. coli-positive and negative herds with bare hands.^82,84,94

Multiple studies in ruraland urban settings found positive associations between high levelsof contact with animals and/or animal feces and negative health outcomes.^{34,63,70,75,95,96} The presenceof animal feces in household compounds has been associated with diarrhea,lower HAZ, and HrCLM.^38,41,74 Contact with manure has also been associated with the presence ofantibodies to C. jejuni and pathogenic E.coli.(28)

Pathway 6: Contaminationof Fomites

Other sources ofdirect or indirect contamination by animal feces include fomites,such as cooking and infant feeding utensils and toys. Two studiesin South Asia evaluated environmental fecal contamination in ruralhouseholds using toys which may be more likely to come into directcontact with animal feces as they are used for play. In rural India,the average fecal contamination of toys increased as the number ofanimal fecal piles observed in the household or within the compoundincreased.⁹⁷ The authors suggest that thefecal contamination detected on the toys is likely from both humanand animal feces. In rural Bangladesh, fewer toys were contaminatedwith E. coli (used as a fecal indicator bacteria)in households in villages with more than 50% latrine coverage, noopen defecation, handwashing facilities with soap, protected sourcewater in dwellings, safe disposal of child feces, and no animals presentin the household but used plaster floors with cow dung.⁹⁸ In this study, the households substantialWASH infrastructure used to limit human fecal contamination likelyplayed a role in minimizing fecal contamination in the household,but the absence of animals is also noteworthy. Interestingly, thestudy noted that households with floors of soil or mud surfaces inthe living and entrance areas had statistically lower amounts of bacteriaon toys compared to households with cement floors, but there was nodifference in contamination levels of the toys between householdsthat plastered with cow dung versus households that did not plasterwith cow dung.⁹⁸

Two studies in thisreview examined fecal contamination on cooking and feeding utensils.In a peri-urban community in Lima, Peru, a study of environmentalcontamination of household objects, including infant bottle nipples,feeding bottles, spoons, and can openers, found that 35% of the objects(n = 80) were positive for E. coli cultures.³⁷ Another household-level studyfound that infants cups and spoons yielded E. coli cultures in 23% of households (n = 5).⁸⁹ In these studies, indirect contamination offomites likely occurred when the fomites dropped onto contaminatedfloors or were handled by contaminated fingers; direct exposures offomites to animal feces were not addressed in these studies.^37,89

Interventions Limiting Exposure to Animal Feces

Weadapted the traditional F-diagram to show pathways of humanexposure to animal feces and assessed potential interventions alongthose pathways (). While secondary barriers to block transmissionof animal feces to humans are capable of controlling both human andanimal feces, primary barriers are specific to controllingexposure to animal feces. These primary barriers have largely notbeen considered in traditional WASH interventions designed to limitexposure to human feces, and few studies have evaluated their potentialin reducing the burden of animal feces on human health. Our reviewuncovered only seven intervention studies specifically aimed at controllingthis primary barrier of exposure to animal feces. The control measuresthat have been evaluated and/or suggested as potential interventionsin the studies included in this review are described below; Table 3 summarizes theseintervention studies.

Modified F-diagram including interventions that can blockhumanexposure to animal feces. Adapted from Wagner, E.; Lanoix, J., Excretadisposal for rural areas and small communities. MonographSeries World Health Organization.1958, 39, 182. Copyright 1958, World Health Organization.

Table 3

Summary of TrialsEvaluating PotentialInterventions Limiting Exposure to Animal Feces

Separating Chickens fromHuman Living Quarters

Cohabitationwith animals has been associated with negative health outcomes. Animalcontainment practices can reduce human exposure to animal feces contaminationin domestic environments. However, according to two studies that evaluatedthe effects of separating chickens from human living quarters in peri-urbanareas of Lima, Peru, corralling chickens did not eliminatechild exposure to poultry; it might actually increase the risk ofcampylobacteriosis potentially due to continued exposure to chickensand/or from increased concentrations of Campylobacter spp. in the corralling area.^42,99 Harvey et al. evaluatedan intervention to contain poultry in wooden corrals with commercialfish netting walls and fiberglass roofs, in addition to separatingpoultry by age, sex, and/or species.⁹⁹ Householdsthat used corrals most of the time before the study consistently usedthe experimental corrals from the start; households who let theirpoultry roam before the study intervention housed their poultry incorrals less consistently. Despite efforts to separate children frompoultry, some children were still exposed because they helped catchpoultry and move them into the corral, climbed on corral walls anddoors, poked fingers through the netting, entered corrals to playwith the poultry, or helped with daily animal care. In another areaof peri-urban Lima, researchers installed chicken corrals in interventionhouseholds.⁴² They found that chicken fecesfrom the control group were colonized with Campylobacter spp. more often than that from the corral group, but both groupswere heavily colonized (63.9% and 58.1% of chicken stool samples,respectively). The rate of diarrhea in children was higher in thecorral group (2.79 episodes per person per year [epy]) than the groupwithout corrals (2.07 epy; p = 0.017), suggestingthat chicken corralling may have increased the risk of Campylobacter-related diarrhea in children from children entering and handlingthe chickens in the corrals and/or encouraged the children to interactwith the chickens due to close proximity of the corrals to the home.In addition, the corrals concentrated chicken feces in a single areathat could have contributed to an increased concentration of Campylobacter spp. in the area.

Providing Animal FecesScoops

Similar to animal containmentpractices, promotion of animal waste removal from the domestic environmentand proper disposal could disrupt the contamination of environmentalreservoirs by animal feces. Though sanitation interventions have primarilyfocused on containing human feces by providing improved latrines,some studies have added components to encourage the safe disposalof animal feces as well. The WASH Benefits trial provided a metalscoop to households for removal of animal feces from the environmentand safe disposal in a dual-pit latrine as part of a sanitation interventionin rural Bangladesh.¹⁰⁰ The authors hypothesizethat the use of the metal scoops might remove animal feces from sanitationcompounds, but might ultimately contaminate the communityswater source downstream of the disposed animal feces. While the interventiongroup had lower ruminant fecal markers, the scoop was coupled withprovision of a household dual-pit latrine as well as potties for youngchildren, so disaggregating the impact of animal feces disposal wasnot feasible.⁸⁷

In rural Bangladesh,households were provided potties and sani-scoops,hoe-like tools for disposal of child and animal feces. Although reporteduse of the hardware was relatively high, minimal differences weredetected between the presence of human and animal feces in compoundsat baseline and follow-up visits.¹⁰¹ Interviewswith study participants revealed that liquid feces was hard to removefrom uneven or hard surfaces with the sani-scoop, and animal feceswas not generally perceived as disgusting. Additionally,household members were unlikely to change their habits of sweepingand cleaning courtyards of feces only at certain times during theday, potentially exposing them to fecal contamination at other timesof day.¹⁰¹ To reduce exposure to animalfeces, education regarding safe animal feces disposal methods mightbe necessary as a complement to provision of sanitary scoops designedto remove animal feces.

Reducing Contamination of Environmental Sourcesby ControllingAnimal Movement

Soil is oftentimes a reservoir for animalfeces contamination in both public and domestic areas, and animalcontainment measures may reduce animal fecal contamination. In urbanBrazil, fencing around public sandboxes was a significant protectivefactor against soil contamination of helminths from dog feces becausethe fences prevented stray dogs from accessing the area.⁸⁵

Creating Safe Child Spaces

Ratherthan corralling animals,protective and hygienic barriers may prevent humans, specificallychildren, from coming into contact with animal feces. Since thereare constant opportunities for young children to put contaminatedfingers in their mouths or ingest feces-contaminated soil, creatingspaces for children separate from livestock could reduce exposureto animal feces. The Sanitation, Hygiene, and Infant Nutrition Efficacy(SHINE) trial in Zimbabwe is testing this approach by providing householdswith safe play areas for children in addition to a package of otherwater and sanitation interventions.¹⁰² Thetrial is ongoing, and results have not yet been published.

ImprovingAnimal Veterinary Care

Veterinary care mayreduce the spread of zoonotic fecal pathogens from livestock and domesticanimals by reducing pathogen carriage in animals. In Bangladesh, exposureto emerging infectious disease hazards were significantly reducedby removing livestock from one in three households, improving manuremanagement in all villages, improving water and latrines in all villages,and increasing access to health serviceshuman and veterinaryinmost villages.¹⁰³ The intervention alsoincreased income from animal agriculture.

Promoting Handwashing andDomestic Environment Hygiene

Handwashing and domestic hygienehave been recommended by severalstudies finding positive associations between animal exposure, rawvegetable consumption, geophagy, or lack of handwashing before mealsand zoonotic pathogenic infection.^{37,57,63,75,104} Unlike the animal feces sanitation interventions,handwashing and domestic hygiene are designed to protect humans fromexposure to both animal and human feces. Lack of handwashing mightbe a generalizable and important behavior to target; another studyfound that handwashing by mothers was infrequent and children placedtheir hands in their mouths 38 times in 130 h on average.⁸⁹ However, we did not find any studies that explicitlyexamined the effects of handwashing after contact with animals.

Limitations

We included all studies that meet the inclusioncriteria regardlessof methodological rigor. A majority of the publications are cross-sectionalstudies, making it difficult to assess the causal attribution of exposureto animal feces on human health. Due to the lack of in-home observations,most studies we reviewed used surveys and interviews assessing animalownership or contact with animals as proxies for exposure to animalfeces. Such exposure measures might be poor indicators of true exposureto animal feces, and in fact, could measure behaviors associated withpotential health benefits to households. For example, a study in ruralEthiopia carefully looked at the benefits of poultry ownership onegg consumption versus the risks posed by corralling poultry insidethe home,⁴⁶ but few studies empiricallyaddress these competing risks and benefits. There is also limitedresearch on specific exposure pathways to animal feces and importantconfounding variables are not well understood or quantified. Due tothe use of household interviews, studies were subject to recall biaswhen participants were asked to self-report past bouts of diarrhea.The use of convenience sampling methods, instead of random samplingmethods, may have led to selection bias. Many of the studies includedin this review had small sample sizes, thus preventing them from achievingsufficient power to detect many of the health outcomes examined inthis review.

Future Research

Our review highlightsthe scarcity of information available onthe human health impacts of exposure to poorly managed animal fecestransmitted via WASH-related pathways. To accurately capture humanexposure to animal feces, future research could prioritize longitudinalstudies with in-home observation methodologies. In addition, datato inform a rigorous assessment of the contribution of poorly managedanimal feces to the global burden of disease is not available. Yetmany associations between some measure of animal or animal feces exposureand health effects have been explored, and interventions designedto control human fecal waste will likely lead to suboptimal healthgains in the absence of efforts to control animal feces in the sameenvironment. Understanding the true burden of disease from poorlymanaged animal feces given the current infrastructure and behavioralcontexts would provide important guidance for policy and programs.

It would be of considerable value to categorize and measure exposureto animal feces and to develop and evaluate interventions to mitigatethat risk. Using direct observations and interviews/discussion withdomestic animal owners, household members including women and children,veterinarians, and community leaders, more data are needed to

• understand the key behaviors andcontexts associatedwith exposure to animal feces;

• identifykey points (hot spots) of humancontact with animals and/or their feces in different contexts (e.g.,domestic, community);

• understand thefactors associated with direct contaminationof food from poorly managed animal feces, particularly in food marketsand noncommercial agricultural/meat production facilities; and

• identify cultural behaviors that influenceanimal husbandryand animal feces management practices.

Understanding the various pathways and behaviors that expose humansto animal feces could allow researchers develop innovative interventionslimiting such exposures in LMIC. Behavioral approaches to WASH shouldbe evaluated further to understand their potential for controllinghuman exposure to animal feces. Our review demonstrates that manypeople did not feel disgust toward animal feces¹⁰¹ and exposure to poorly managed animal feces might occurat the community-level rather than just the household-level. An evaluationof a community-led total sanitation (CLTS) program in rural Mali foundthat households that participated in the CLTS program were less likelyto have observable animal feces in their compound courtyard;²⁰ CLTS programs integrating animal feces managementcould therefore be considered as potential control measures. Interventionsexecuted in HIC, such as building bridges across streams to reducepoint source contamination of waterways by livestock, could be alsoadapted for LMIC.¹⁰⁵

Once the variouspathways of human exposure to animal feces areexplored and understood, it would be possible to calculate specifichealth risks associated with exposure to animal feces, including bothacute infectious diseases and chronic sequelae, such as EED and growthfaltering, by conducting intervention trials. These intervention trialscan measure before-and-after health outcomes among study populationswho are provided interventions to limit or eliminate exposure to animalfeces across multiple pathways compared to health outcomes in similarstudy populations who are not provided interventions to limit or eliminateexposure to animal feces. In addition to understanding the human behaviorsand possible health outcomes associated with exposure to animal feces,future laboratory and field-based research must also consider pathogenbiology by

• quantifying the concentrationand shedding rates ofpathogens in the feces of animal hosts and understanding the factorsthat determine variability in these parameters;

• quantifying die-off rates of pathogens outside of animalhosts and the factors that determine them;

• understanding the factors controlling the fate and transportprocesses of pathogens outside of the animal host, under varying environmentalconditions; and

• understanding how antibioticusage in humans and animalsmay be contributing to antibiotic resistance of zoonotic pathogens.

These types of data will be critical forparametrizing quantitativemicrobial risk assessment models and transmission models that canprovide important insights on zoonotic transmission of pathogens fromanimal feces to humans. Studies could also take advantage of new moleculartechniques that provide insights into transmission processes, suchas microbial source tracking,¹⁰⁶ straintyping, multiplex enteropathogen assays,^107,108 and metagenomics.¹⁰⁹

In addition,work is needed to understand the role of exposureto animal feces on negative human health outcomes in various rural,urban, and peri-urban contexts, from human host and pathogen biologyto overarching public policy. This is illustrated in , a diagram showing priorityresearch gaps in assessing the role of contact with animal feces onhuman health, which we adapted from the socio-ecological model.¹¹⁰ The potential for acute and chronic human healthimpacts to manifest from exposure to animal feces is dependent onbiology within the human host (i.e., intestinal microbiome), includingage- and sex-dependent susceptibilities to different zoonotic fecalpathogens and potential immunities developed from low-level exposuresto animals and their feces. To understand the health risks associatedwith exposure to animal feces, it is crucial to understand the microbiologyof pathogens found in animal feces, including their shedding and die-offrates and their transport processes. Human behaviors and practicesare additional vital elements to assessing human health outcomes fromexposure to animal feces. At the individual level, it is importantto understand knowledge around risks and preventions of exposure toanimal feces. In LMIC, gender and age divisions in responsibilityfor care, decisions, and the control of livestock production are common.^94,111 Gender and age divisions in labor should be explored further tounderstand how these variables influence risk of exposure to animalfeces. Future research could characterize human behaviors in the householdthat result in exposure to animal feces, such as animal housing andcontainment practices or animal feces management. Our review pointsto the probable importance of community-level animal feces contaminationon the human health burden, particularly in regards to food contaminationin markets, soil contamination in the public environment from free-roaminganimals, and contamination of community water sources; as such futureresearch should investigate traditional husbandry practices in differentregions and contexts. At the policy level, it would be valuable tomonitor and evaluate the effect of national policies and regulationsaimed at promoting animal health (e.g., immunization, feed standards),veterinary care (e.g., neutering/spaying policies), and safe managementof animal manure and feces.

Priority research gaps in assessing human healthimpacts from exposureto poorly managed animal feces. This figure, an adaption from thesocio-ecological model, represents how the spheres of influence,from human host and zoonotic pathogen biology to national policies,influence the health of the human host. Example items for future researchwithin each sphere are provided.

One particularly interesting line of inquiry would be toevaluatethe trade-off between the nutritional benefits of livestock ownershipwith the health risks associated with exposure to animals. Many developmentprojects promote animal husbandry as a way to improve nutrition andlivelihoods, yet this review highlights the ways that contact betweenanimal feces and humans may potentially be deleterious to health,especially in children. This trade-off was highlighted by severalof the articles in this review.^26,45 Once more informationis available on the magnitude of the health risk posed by animal fecesexposure, knowledge around animal feces management, and key pointsof contact between humans and animals, culturally appropriate interventionstrategies can be developed and rigorously evaluated.

Conclusions

As envisioned by the Sustainable Development Goals, the world willachieve universal access to safe water, coverage of safely managedsanitation, and handwashing with soap by 2030.¹¹² However, even if these ambitious targets are met, effectivelyeliminating direct and indirect exposure to human feces, risks associatedwith exposure to animal feces will remain. The literature in thisreview suggests that exposure to animals and animal feces has mixedeffects on diarrhea and child growth, potentially increases risksof EED, STH infection, and trachoma, and has mixed effects on isolationof zoonotic pathogens in human stool. There is some evidence for theWASH-related pathways by which humans are exposed to animals and animalfeces, but more research on pathogen transmission parameters, animalhusbandry practices, and cultural/social influences is warranted.Furthermore, few studies have tested interventions that control thetransmission of pathogens in animal feces and limit human exposureto animal feces. As we increasingly understand the contribution ofpoorly managed animal feces to the overall global burden of disease,it is important to gain insights into the routes by which humans areexposed to animal feces to design efforts to interrupt these pathwaysand reduce subsequent human health impacts.

Acknowledgments

This work was supported by the Bill & Melinda Gates Foundation(grant OPP1157522 to Emory University). K.L. is supported by the NationalInstitute for Allergy and Infectious Diseases, NIH (grant 1K01AI103544).The content is solely the responsibility of the authors and does notnecessarily represent the official views of the funders.

Supporting Information Available

The Supporting Informationis available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.7b02811.

• Further detailsabout methods including full searchstring and databases used, global PRISMA chart, data extraction form,PRISMA checklist, and table of study characteristics (

  PDF

  )

Notes

The authorsdeclare no competing financial interest.

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