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Environ Sci Technol. 2017 Aug 1; 51(fifteen): 8725–8734.

Animal Carrion Contribute to Domestic Fecal Contamination: Evidence from East. coli Measured in Water, Easily, Food, Flies, and Soil in People's republic of bangladesh

Ayse Ercumen,*^† Amy J. Pickering,^‡○ Laura H. Kwong,^§ Benjamin F. Arnold,^† Sarker Masud Parvez,^∥ Mahfuja Alam,^∥ Debashis Sen,^∥ Sharmin Islam,^∥ Craig Kullmann,^⊥ Claire Chase,^⊥ Rokeya Ahmed,^# Leanne Unicomb,^∥ Stephen P. Luby,^∇ and John Yard. Colford, Jr.^†

Ayse Ercumen

^†School of Public Health, Academy of California, Berkeley, California 94720, United States

Amy J. Pickering

^‡Civil and Environmental Engineering, Tufts University, Medford, Massachusetts 02153, United States

Laura H. Kwong

^§Civil and Environmental Technology, Stanford Academy, Stanford, California 94305, U.s.

Benjamin F. Arnold

^†Schoolhouse of Public Health, University of California, Berkeley, California 94720, Usa

Sarker Masud Parvez

^∥Infectious disease Division, International Center for Diarrhoeal Disease Research, Bangladesh, Dhaka, 1212, Bangladesh

Mahfuja Alam

^∥Communicable diseases Partition, International Center for Diarrhoeal Disease Research, Bangladesh, Dhaka, 1212, Bangladesh

Debashis Sen

^∥Infectious Disease Division, International Centre for Diarrhoeal Affliction Research, People's republic of bangladesh, Dhaka, 1212, Bangladesh

Sharmin Islam

^∥Infectious Disease Division, International Centre for Diarrhoeal Disease Inquiry, Bangladesh, Dhaka, 1212, Bangladesh

Craig Kullmann

^⊥Water Global Practice, World Bank, Washington, D.C. 20433, U.s.a.

Claire Hunt

^⊥Water Global Exercise, World Bank, Washington, D.C. 20433, United States

Rokeya Ahmed

^#H2o Global Exercise, World Bank, Dhaka, 1207, Bangladesh

Leanne Unicomb

^∥Infectious Disease Sectionalization, International Heart for Diarrhoeal Disease Research, Bangladesh, Dhaka, 1212, People's republic of bangladesh

Stephen P. Luby

^∇Infectious Diseases & Geographic Medicine, Stanford University, Stanford, California 94305, U.s.

John Grand. Colford, Jr.

^†School of Public Health, University of California, Berkeley, California 94720, United States

Received 2017 Apr 3; Revised 2017 Jun 23; Accepted 2017 Jul 7.

Abstract

Fecal-oral pathogens are transmitted through complex, environmentally mediated pathways. Sanitation interventions that isolate human being feces from the environment may reduce transmission but take shown limited affect on ecology contagion. Nosotros conducted a study in rural Bangladesh to (i) quantify domestic fecal contamination in settings with loftier on-site sanitation coverage; (two) determine how domestic animals affect fecal contamination; and (iii) assess how each ecology pathway affects others. We collected water, manus rinse, nutrient, soil, and fly samples from 608 households. We analyzed samples with IDEXX Quantitray for the nigh likely number (MPN) of E. coli. Nosotros detected East. coli in source water (25%), stored water (77%), child hands (43%), food (58%), flies (50%), ponds (97%), and soil (95%). Soil had >120 000 hateful MPN Due east. coli per gram. In compounds with vs without animals, E. coli was higher by 0.54 log_ten in soil, 0.40 log_x in stored water and 0.61 log₁₀ in nutrient (p < 0.05). E. coli in stored water and food increased with increasing Due east. coli in soil, ponds, source h2o and hands. We provide empirical prove of fecal transmission in the domestic environs despite on-site sanitation. Animate being feces contribute to fecal contamination, and fecal indicator bacteria practise non strictly indicate human fecal contamination when animals are present.

Introduction

Fecal-oral pathogens are transmitted from feces to new hosts through circuitous, environmentally mediated pathways. The complexity arises from a multitude of manual pathways, a wide variety of pathogens, the influence of environmental weather condition and interactions between the environment and human behavior. In the absence of effective sanitation and sewerage facilities that isolate homo carrion from the environment, human fecal organisms can spread into fields and ambient waters. These are subsequently transported past fomites and vectors (due east.g., hands, flies) into drinking h2o and food as well as ingested through mouth contact with contaminated hands and objects or geophagia (deliberate ingestion of soil) by immature children.^1,2

Contamination of drinking water, a directly ingestion pathway, has been studied extensively, and water treatment has been shown to improve microbiological h2o quality as measured by fecal indicator bacteria (FIB) and reduce self-reported diarrhea.^3,4 Other transmission pathways remain understudied fifty-fifty though these could present major sources of fecal exposure. For instance, complementary foods for young children contain FIB in low-income country settings^five and child diarrhea has been linked to food contamination.^vi Loftier FIB levels are plant on hands in low-income countries⁷ and handwashing interventions reduce self-reported diarrhea.⁸ Flies are known to carry man pathogens^ix,10 and fly control programs have successfully reduced diarrheal disease.^eleven FIB and pathogens have been detected in soil¹² and geophagia has been associated with diarrhea, markers of environmental enteric dysfunction, and stunting in young children.^13,fourteen However, it has not been documented how soil contamination affects subsequent contamination of ambience and drinking waters, hands and nutrient.

Sanitation interventions are a chief barrier to disease manual and should block enteric pathogens both by stopping feces from spreading into the environment likewise as eliminating fly breeding sites. Yet, contempo sanitation trials take shown express wellness impact. Two trials in India found no event of sanitation improvements on kid diarrhea, parasite infections, and growth,^15,16 while a trial in Republic of mali demonstrated improved child growth but no diarrhea reduction.¹⁷ These trials also found no reduction in FIB measured in source and stored h2o, and on hands and fomites.^xv−17 A systematic review identified no overall reductions in environmental contamination in response to sanitation improvements.^eighteen Possible explanations include low latrine uptake and continuing open defecation; Clasen et al. (2014) and Patil et al. (2014) reported that <50% of households in intervention villages had a functional or improved latrine, respectively, and Patil et al. plant that >70% of adults in intervention villages reported daily open defecation.^15,xvi

Another potential explanation for the failure of sanitation improvements to reduce domestic fecal contagion and diarrhea is balance contamination from creature carrion. Sanitation programs focus on isolating human feces from the surroundings, typically with no measures to reduce exposure to beast carrion. Many households in low-income countries keep livestock in close proximity to living quarters.^xix Microbial source tracking studies in rural India and Bangladesh advise that fecal contamination from animals is more than prevalent than human contamination in the domestic environment, including source and stored drinking water, easily, and soil.²⁰⁻²² Courtyard soil, household floors, and child hands take been shown to contain animal fecal molecular markers.^xx,23 Presence of animal feces in the compound has been associated with visible dirtiness of caregivers' and children's hands and faces.²⁴ In that location is also increasing evidence that exposure to domestic animals is associated with increased diarrhea.¹⁹ However, the contribution of fauna feces to fecal contamination forth unlike transmission pathways in settings with on-site sanitation has not been assessed.

The objectives of our study were to (1) characterize levels of fecal contamination along multiple environmental manual pathways (source, stored and ambient waters, kid hands, complementary food, courtyard soil, and flies defenseless in the compound) in rural Bangladeshi households, (2) determine how the presence of domestic animals, household sanitary infrastructure and ambient climate conditions affect contagion levels, and (3) assess how dissimilar environmental pathways bear upon each other.

Materials and Methods

Information Collection

Our study was nested inside a randomized controlled trial in rural central Bangladesh (Launder Benefits).²⁵ We randomly enrolled households from the trial'south control arm between July 2013 and March 2014. During household visits, field workers conducted spot check observations on the presence of human and creature feces in the courtyard; human vs specific fauna (cow, caprine animal/sheep, chicken) feces were distinguished based on their visual characteristics. Field workers as well administered a structured questionnaire on animal husbandry. Additionally, they observed h2o, sanitation, and hygiene indicators, including the cover condition of the storage containers from which the drinking water and nutrient samples were collected, presence of a handwashing station with lather and water (tubewell, pond, or container with h2o) inside 10 m of the latrine, and presence and number of latrines in the compound and within 10 m of tubewells and ponds. They differentiated improved latrines based on Joint Monitoring Programme (JMP) categories²⁶ and observed whether the latrine drained into a septic tank, pit, or the environment (pond, ditch, etc.). When collecting soil samples, field staff observed whether the sampled expanse was visibly wet and in the sun or shade.

Sample Drove

Field workers collected samples from the compound, including tubewell h2o, drinking h2o stored in the home, pond h2o, child hand rinses, complementary foods given to young children, flies caught in the food training area, and courtyard soil from young children'due south outdoor play expanse. Samples were collected in sterile Whirlpak bags (Nasco Modesto, Salida, CA). To collect source water (tubewell) samples, field staff removed fabric or other materials attached to the tubewell mouth and flushed the tubewell by pumping five times earlier collecting 250 mL of water. To collect stored h2o, field workers asked the respondent to provide a drinking glass of h2o from their master drinking water storage container as if giving information technology to their children <5 years and pour 250 mL from the glass into a Whirlpak. Swimming samples were collected by dipping a Whirlpak into the pond and collecting 250 mL of h2o from the area where the household reported most commonly accessing the pond. To sample child easily, field workers asked the respondent to place both hands of the youngest kid <5 years, ane at a time, into a Whirlpak prefilled with 250 mL of distilled water. Each hand was massaged from outside the bag for fifteen s, followed past 15 due south of shaking, and the rinsewater was preserved in the Whirlpak.²⁷ To collect soil samples, the respondent was asked to identify the outdoor surface area where the youngest child <5 years had most recently spent time. Field workers marked a 30 × 30 cm^two area with a sterile stencil, and scraped the top layer of soil within the stencil into a Whirlpak using a sterile scoop to collect approximately 50 chiliad of soil. To sample complementary nutrient, field workers identified stored food to exist served to children <v years and asked the respondent to provide a small amount of food in the same style they feed their children. Food was scooped to fill a 50 mL sterile plastic tube using a sterile spoon. Finally, field workers identified a suitable location in the food preparation area (away from the stove and smoke, nether a roof or protected from rain if possible) and hung three horizontal one.5-foot strips of nonbaited glutinous fly tape. The record was left in identify for three–6 h to capture flies. Field workers removed one wing from the middle of the strip with the most flies using sterile tweezers and placed it into a Whirlpak. Clean gloves were worn to collect pond, paw rinse, soil, and food samples.

Sample Processing

Samples were preserved on ice and processed on the aforementioned solar day, typically within 12 h of collection. Tubewell and stored water samples were analyzed without dilution. Pond samples were diluted ane:100 and hand rinses ane:two with distilled water. Nutrient and soil were homogenized with distilled water using a sterile blending pocketbook (BagFilter P, 400 mL, Interscience, Saint Nom, France) and a laboratory-scale food processor (BagMixer C, Interscience, Saint Nom, French republic) for 1 min at a specified mixing speed. A ten g aliquot of food was homogenized with 100 mL of distilled water and then diluted 1:10. A 20 g aliquot of soil was homogenized with 200 mL of distilled water and then diluted 1:10^four. An additional 5 g food and soil aliquot was oven-stale overnight to make up one's mind the wet content and dry weight. Flies were homogenized with a pestle from outside the Whirlpak and mixed with 100 mL of distilled water; this slurry was diluted 1:100.

I field bare per sample collector per week, 1 laboratory bare per laboratory assistant per day, 10% field duplicates (ii samples from one household), and 5% laboratory replicates (two aliquots from the same sample) were processed for quality command. Field workers collected two types of field blanks (1) past asking the respondent to pour distilled water from a sterile bottle into a Whirlpak and (2) by opening and shaking a prefilled Whirlpak in the field as if collecting a hand rinse. Samples were analyzed using IDEXX Quantitray with Colilert-18 media (IDEXX Laboratories, Maine, U.S.A.) and incubated at 44.5 °C for 18 h to enumerate E. coli with the most probable number (MPN) method. The Quantitray-2000 system with a wide detection range of 1–2419 MPN per tray was selected to accommodate variability within sample types.

Statistical Methods

We tabulated the presence/absenteeism, log₁₀-transformed counts, and geometric ways of E. coli; we substituted the value of 0.v MPN for samples below and 2420 MPN for samples above the detection limit to summate the logarithm. Nosotros assessed the association between log₁₀-transformed Eastward. coli counts and ambient climate factors (e.g., season, sunlight and visible moisture in soil sampling area, measured soil moisture content), presence of animals, observed human/animal feces, and household sanitary infrastructure. Season was defined as wet vs dry as Bangladesh receives >80% of its pelting during the monsoon season from June through October and is typically dry otherwise.²⁸ We as well assessed the relationships between different manual pathways by separately estimating the association of E. coli levels in dissimilar sample types (e.k., log₁₀ increment in Due east. coli on hands for every log₁₀ increment in E. coli in soil). We used generalized linear models with robust standard errors to business relationship for the clustered design of the Wash Benefits trial. We assessed whether housing materials, reported income, land buying, presence of electricity, and female person education (≥1 year of formal schooling) equally socioeconomic proxies were associated with the presence of animals and animate being feces using chi-square tests; all models controlled for these potential confounders.

Results and Word

Household Characteristics

Of the 699 households randomly selected from the command arm of the parent trial, we successfully enrolled 608 (87%) households with 13% lost to follow-upward (7% stillbirth, miscarriage, abortion, or death of children in the target age range, v% relocation, and one% refusal). Among 608 enrolled households, 97% had a latrine and 68% had an improved latrine equally per the JMP definition;²⁶ 29% of latrines tuckered into the surround (Table one). The presence and number of latrines were positively associated with all proxies of college socioeconomic condition (finished walls, electricity access, higher up-median reported income, land buying, ≥1 years of female education, all p-values <0.05) while the presence of an improved latrine was non associated with any of these proxies. Human feces were observed in four% of compounds. One-half (47%) of households had water in the latrine area while 7% had lather. Fewer than 20% of drinking water storage containers were covered in contrast to 85% of food storage containers. At least one fly was caught in the food preparation expanse in 32% of households.

Table one

Characteristics of Enrolled Households (Northward = 608)

household characteristics	%
household water, sanitation, hygiene conditions
latrine in chemical compound	97
improved latrine in compound (JMP definitiona)	68
latrine flushes to environment	29
household owns kid potty	17
human feces observed in courtyard	four
stored water covered	17
h2o nowadays in latrine	47
soap nowadays in latrine	seven
food container covered	85
flies captured in food preparation expanse	32
presence of domestic animals and brute feces
compound has animals	94
chickens	91
cows	69
goats/sheep	39
animals roam costless in compound	56
animal carrion observed in courtyard	89
craven feces	87
cow carrion	thirty
goat/sheep feces	xix

Animals and Brute Feces

Almost all compounds (94%) had domestic animals and the most common animal was chickens, while 89% of compounds had observed animal feces in the courtyard and chicken feces were the most common type of feces observed. Whether or non a household had animals was not associated with socioeconomic proxies; notwithstanding, households that owned state were more likely to accept >1 cow or >10 chickens (p < 0.05). Compounds were more than likely to have animal feces in the courtyard if they had unfinished (due east.g., bamboo, mud) walls or no electricity (p < 0.05).

Fecal Contamination

We tested 3254 samples and detected Eastward. coli in every sample type, including 25% of source water, 77% of stored water, 43% of kid hands, 58% of complementary foods, 50% of flies, 97% of ponds, and 95% of soil (Tabular array 2). Geometric mean E. coli was <10 MPN per reporting unit in drinking water, food and on easily. The geometric mean E. coli for flies was 663 MPN per fly. Ponds and soil had extremely high contamination; geometric mean East. coli was >5000 MPN per 100 mL for ponds and >120 000 MPN per dry gram for soil. Across all samples types, v% of samples exceeded the detection limit.

Table 2

E. coli Detection among Ecology Pathways

type of sample	North	unit	lower detection limit (MPNa)	upper detection limit (MPNa)	geometric mean (MPNa)	% positive
soil	591	one dry gram	1000–1515b	ii.four × 10half-dozen to iii.7 × ten6 b	125 530	95
ponds	277c	100 mL	100	241 900	5918	97
tubewells	563	100 mL	1	2419	i	25
flies	193d	i fly	100	241 900	663	50
child hands	584	2 hands	5	12 095	7	43
stored water	497	100 mL	one	2419	nine	77
food	549	ane dry gram	one–8e	2426–xx 158due east	2	58

Ambience Climate Conditions Vs Fecal Contagion

During the rainy season, E. coli was detected significantly more than oft and at higher concentrations forth all pathways compared to the dry season (all p < 0.05 except for log_x E. coli in soil) (Figure ​ 1). Soil E. coli counts were not afflicted by whether the soil was visibly wet at the time of sampling. However, soil samples with in a higher place-median moisture content (median = 7%, range = 0–34%) had 0.70 log_ten MPN college E. coli per dry gram (p < 0.005). Soil from areas sunlit at the fourth dimension of collection had 0.48 log_ten MPN fewer E. coli per dry gram than soil from shaded areas (p < 0.005).

East. coli detection during moisture season (Jun–Oct) vs dry season (Nov–May). The y-axis shows the percentage of E. coli positive samples. Geometric mean Eastward. coli counts are displayed beneath the bars.

Presence of Animals and Beast Feces Vs Fecal Contamination

Animal presence was associated with higher levels of fecal contamination along multiple pathways; soil contamination in detail was independently associated with the presence of individual animal species (chickens, goats/sheep, cows) likewise as the presence of whatever animal in the compound (Figure ​ 2). Compounds with animals had 0.54 log₁₀ MPN higher Eastward. coli in soil, 0.40 log_x MPN college Eastward. coli in stored water, and 0.61 log₁₀ MPN higher E. coli in food (all p < 0.05). This was primarily driven by the presence of chickens; compounds with chickens had 0.70 log₁₀ MPN higher Due east. coli in soil, 0.49 log_x MPN college Due east. coli in stored h2o, and 0.40 log₁₀ MPN higher Eastward. coli in food (all p < 0.05). Compounds where animals roamed freely had 0.22 log₁₀ MPN higher E. coli in soil and 0.27 log₁₀ MPN higher Due east. coli in ponds (all p < 0.05) than compounds with no animals at all or no free-roaming animals. Food had 0.32 log₁₀ MPN higher Due east. coli in compounds where ≥ane fly was captured in the food preparation expanse (p = 0.02).

Increment in log₁₀ Due east. coli associated with the presence of animals, animate being and human feces, and sanitary infrastructure in compound.

Similarly, the presence of animal carrion in the courtyard was significantly associated with increased contamination in the domestic environment; especially soil E. coli was independently associated with the presence of carrion from individual animal species as well equally the presence of any animate being feces in the compound (Figure ​ 2). Compounds with animal carrion had 0.55 log₁₀ MPN college soil E. coli; the increase was 0.51 log_ten for chicken feces, 0.33 log₁₀ for goat/sheep feces and 0.25 log₁₀ for cow carrion (all p < 0.05). Fauna feces were associated with higher levels of E. coli in ponds and food besides. Surprisingly, the presence of animal carrion was associated with lower East. coli levels in tubewells and non associated with E. coli levels on flies. Because human feces were observed very infrequently (4% of households), we did not accept sufficient statistical power to assess associations with this variable.

Sanitary Infrastructure vs Fecal Contamination

The presence of a latrine was associated with significantly lower E. coli in soil and ponds, while the presence of an improved latrine was associated with reduced contamination of ponds, and a higher number of latrines in the compound was associated with reduced contagion of soil, kid hands and stored drinking water (Figure ​ 2). In dissimilarity, ponds had increased East. coli if there was a latrine within ten g (Δlog₁₀₌0.21, 0.02–0.41) or if the latrine was observed to drain into the environment (Δlog_ten = 0.22, 0.00–0.45) or directly into the pond (Δlog₁₀ = 0.30, 0.xiii–0.47). The presence, number, improved vs unimproved status, proximity or drainage location of latrines in the compound was not associated with tubewell water quality or Eastward. coli on flies.

Associations betwixt Pathways

Contamination levels along different ecology pathways were associated with each other (Figure ​ iii). Pond E. coli increased for each log_ten Eastward. coli increase in soil (Δlog_x = 0.13, 0.03–0.23). E. coli on kid hands increased for each log₁₀ E. coli in soil (Δlog_ten = 0.07, 0.01–0.12) and ponds (Δlog₁₀ = 0.15, 0.05–0.25). E. coli in stored water increased for each log_ten Eastward. coli in soil (Δlog₁₀ = 0.fifteen, 0.06–0.24), ponds (Δlog₁₀ = 0.27, 0.09–0.44), hands (Δlog₁₀ = 0.21, 0.08–0.33), and source water (Δlog₁₀ = 0.39, 0.23–0.55). Finally, E. coli in food increased with each log₁₀ E. coli in all other pathways, including soil (Δlog_x = 0.12, 0.02–0.22), ponds (Δlog_x = 0.28, 0.08–0.48), hands (Δlog₁₀ = 0.18, 0.04–0.32), source water (Δlog_ten = 0.21, 0.05–0.37), stored water (Δlog₁₀ = 0.28, 0.17–0.39), and flies caught in the food preparation area (Δlog_x = 0.21, 0.08–0.34).

Associations between environmental transmission pathways, measured as increment in log₁₀ E. coli on a pathway associated with each log₁₀ increment in E. coli forth another pathway. Arrows signal associations that are pregnant at the p < 0.05 level; the lack of an arrow between ii sample types indicates that nosotros did not observe a pregnant clan.

Word

We found ubiquitous fecal contamination along multiple environmentally mediated pathways in rural Bangladeshi households with on-site sanitation access. Nosotros detected East. coli in 25% of tubewells, compared to 77% of stored drinking water, supporting prior evidence on tubewell water quality in Bangladesh²⁹⁻³¹ and subsequent contagion at the bespeak-of-use.^32,33 We found Due east. coli on 43% of child easily. Paw contamination levels were similar to findings from Tanzania³⁴ and urban Bangladesh²³ merely much higher than in high-income countries.³⁵ E. coli was detected in 58% of complementary food, consistent with previous studies in Bangladesh.^{half-dozen,36,37} Among flies captured at the nutrient preparation area, 50% had E. coli, which could accept been present on the outside or in the gut of the wing. Soil and ponds had high levels of E. coli, suggesting these are major reservoirs for fecal organisms. Soil E. coli levels in our written report were substantially higher than previously documented in Tanzania and Zimbabwe.^12,38 Our method may have had higher recovery efficiency since it did not require a settling step similar the protocol used in the Tanzania report. Our results could also indicate heavier fecal input into the environment due to the high population density of People's republic of bangladesh and/or enhanced bacterial growth in soil due to the wet climate and high groundwater table in People's republic of bangladesh; saturated subsurface conditions favor the transport, survival and growth of microorganisms.³⁹ This is consistent with our finding that soil with higher moisture content had higher Eastward. coli counts. However, soil in our written report was also more contaminated than measured in a like rural Bangladeshi setting by enumerating soil homogenates on Petrifilm without a settling step;¹³ one reason for this could be our method'due south high upper detection limit (two 419 000 MPN per wet gram of soil). Nosotros as well establish associations between E. coli levels measured in soil, ponds, groundwater, hands, flies, stored water, and food. Previous evidence supports these findings; however, few studies take explored associations between several dissimilar pathways. Ambient (pond) h2o quality has been shown to affect groundwater quality.^twoscore Source water quality, in turn, is a known determinant of stored water quality.⁴¹ A link betwixt contamination of stored h2o and easily has besides been demonstrated.^22,34,42

Our findings suggest that animal feces contribute more essentially to domestic fecal contamination in rural Bangladeshi households than human carrion; four% of compounds had observed human being feces in the courtyard vs almost 90% having animal feces. This is not surprising considering that 97% of enrolled households had a latrine. Open up defecation is commonly skillful by young children in this setting;⁴³ still, our infrequent observation of human feces indicates that child feces are removed from the chemical compound'southward living area. Indeed, other work in our written report area indicated that, among households where child feces are not disposed of in a latrine, 64% reported disposing of them in the bushes surrounding the compound, 18% in open waste product heaps and 13% in drains while only eleven% left the carrion on the footing.⁴⁴ However, homo feces likely contribute to domestic fecal contamination through other routes, such as latrines draining into ponds/canals or pits leaking into the environment. Indeed, ponds with a latrine within ten m and ponds receiving latrine effluent had higher E. coli levels in our study, consistent with previous evidence from rural Bangladesh.^xl,45

Chickens presented the most prevalent domestic beast exposure in our written report. Roughly 90% of compounds had chickens, followed by cows (69%) and goats/sheep (39%). Similarly, 87% of courtyards had craven feces, followed past cow feces (xxx%) and caprine animal/sheep feces (19%). Chickens typically roam and deposit feces throughout the chemical compound while scavenging for food,⁴⁶ and considering their feces are modest and relatively odorless, they are likely to exist left in identify, fifty-fifty though some households collect craven feces to utilise as fertilizer.⁴⁷ Cow dung is oft collected and used equally cooking fuel and housing material in rural Bangladesh.⁴⁸ This could explain the relatively low prevalence of cow feces; while 69% of compounds had cows, only 30% had observed cow feces.

Due to the infrequency of observed human feces, we had limited power to detect associations between this exposure and Eastward. coli. Fauna feces were associated with increased contamination of soil, ponds and complementary foods. The association with food contamination might point that, when preparing food, caregivers practice non wash hands after handling animal feces. Previous piece of work in Bangladesh constitute that, during nutrient preparation, caregivers feed dung cakes to the burn down with bare easily and resume food treatment or feed children without washing hands.⁴⁹ However, while dung cakes are moist when handled to course them for subsequent utilize, they are sun-stale before beingness used equally fuel, and desiccation should substantially reduce pathogen concentrations.^l Surprisingly, the presence of animal (as well as human being) carrion was associated with lower tubewell contamination. Tubewells in rural Bangladesh are typically located on the periphery of the compound rather than in the fundamental courtyard surface area. Animate being and child feces are oft disposed of in bushes or open waste material heaps on the compound periphery also. Observed feces in the courtyard area could signal that carrion accept not been tending of near the tubewell, where they could more easily infiltrate into the well. E. coli on flies was not associated with animate being feces in the courtyard, potentially indicating that flies can learn fecal contamination from distal sources beyond a given chemical compound.

Testify from microbial source tracking supports the contribution of animal carrion to domestic fecal contagion in our study setting. A subset of 500 stored drinking water, kid hand and soil samples from our study were analyzed by quantitative polymerase chain reaction (qPCR) for human, ruminant and avian molecular fecal markers.²⁰ Over 50% of soil and hands and 22% of stored water contained ruminant markers while the avian marker was detected in 33% of soil, 16% of hand rinses and 9% of water samples.^xx Ruminant and avian markers were more than commonly detected in compounds that had ruminants and birds, respectively,^twenty consistent with our finding of higher East. coli levels in compounds with animals. In dissimilarity, human fecal markers were detected in ix% of soil, 2% of hand rinse and none of the water samples.²⁰ Others have reported similar findings. A recent study in India detected creature fecal markers in 75% of ponds, fifteen% of tubewells, 52% of stored h2o, and 96% of hands in dissimilarity to human markers detected in viii% of ponds, 2% of tubewells, xx% of stored water and 37% of hands.²² A similar written report found evidence of fauna contamination in 70% of households in rural India compared to homo contamination in 35%, based on testing stored drinking water and easily.²¹ Ruminant fecal markers take also been detected on child hands and household floors in urban People's republic of bangladesh.²³

The high prevalence of animals and animal carrion in our study and their associations with fecal contagion in the domestic environs suggest that animals can be a source of fecal pathogen exposure. A previous written report in Bangladesh constitute 8.5 log₁₀ MPN Due east. coli and vii.viii log₁₀ MPN Enterococcus per gram of craven feces²³ and 6.8 log_ten MPN E. coli and 3.8 log₁₀ MPN Enterococcus per gram of cow feces.²³ Animal carrion also carry pathogens that infect humans, such every bit pathogenic E. coli, Salmonella and Campylobacter.⁵⁰ A written report in Republic of ecuador establish that 76% of chickens were positive for Campylobacter;⁵¹ Campylobacter tin can persist in chicken feces for days after degradation.^38,52 Animal feces pose variable levels of man health adventure, depending on the prevalence of homo-infective pathogen strains in the host species.⁵³⁻⁵⁵ A study in rural India found similar odds of diarrhea associated with animal and human fecal markers in the domestic environment.²¹ Identical strains of Campylobacter were isolated from the carrion of children and chickens in Republic of ecuador, suggesting zoonotic transmission.⁵¹ Pathogens tin can be transmitted from animal feces to human hosts through direct and indirect routes. Previous studies have observed children ingesting craven feces.^38,52 Structured observations of 148 children in our study demonstrated that roughly 20% of young children touched animal feces but straight ingestion was rare (<iii%).⁵⁶ Nonetheless, upward to 35% of children placed soil in their oral fissure or put their hands in their mouth without handwashing after touching soil.⁵⁶ Compounds with animals had higher levels of soil contamination in our study, as well equally higher contamination of stored water and food. Taken together, these findings suggest that animal feces are a source of fecal exposure for children in this setting. Environmental pathways, including highly contaminated soil, potentially mediate manual past straight and indirect ingestion.

Our findings are consistent with an emerging body of literature that exposure to domestic animals, especially chickens, is associated with increased run a risk of enteric infection and agin kid growth. A meta-analysis institute associations between diarrheal infections and domestic animal exposure, with an well-nigh 3-fold increase in Campylobacter infections associated with poultry exposure.¹⁹ The presence of creature fecal markers in the household environment was associated with an over 4-fold increase in the odds of child diarrhea in rural India; the magnitude of the consequence was similar to that observed for the presence of human markers.²¹ The presence of animal feces was associated with lower summit-for-age in children in Federal democratic republic of ethiopia and People's republic of bangladesh.²⁴ In rural Federal democratic republic of ethiopia, while poultry ownership was associated with improved child growth (presumably past providing diet-rich foods such as eggs), corralling poultry within the domicile overnight was associated with growth faltering; indoor corralling of other domestic animals was not associated with adverse growth outcomes.⁴⁶ Similarly, keeping animals in the room where children sleep was associated with ecology enteric dysfunction scores and stunting among rural Bangladeshi children; chickens were the most mutual animal corralled in the sleeping area (61%) followed past cows (39%).⁵⁷ In Peruvian shantytowns, children living in households with chickens were at increased risk of Campylobacter infections;⁵⁸ an intervention to corral chickens in an attempt to reduce children's exposure to carrion deposited by free-ranging chickens essentially increased rather than decreased the risk of Campylobacter-related diarrhea compared to letting the chickens free-range.⁵⁹ This could have been due to exposure to full-bodied rather than dispersed fecal matter from chickens. In contrast, cow exposure was not associated with child diarrhea or growth in rural Bharat.⁶⁰

Limitations

One limitation of our study is that E. coli is an imperfect proxy for fecal contamination. It has been suggested that tropical soils and waters can harbor naturally nowadays E. coli;^61,62 these are phenotypically identical to East. coli from fecal sources and can merely be distinguished past genotypic comparison.^63,64 While soil collected from compounds with animals and observed fauna carrion consistently had higher levels of East. coli in our written report, the level of contagion in compounds without animal feces was even so high (four.7 log₁₀ MPN). This could indicate that soil accumulates fecal indicator contamination beyond the immediate contribution of feces observed at the fourth dimension of sampling; still, it could likewise point to the presence of naturally nowadays E. coli. Soilborne E. coli can persist and multiply exterior animal hosts, especially in warm and moist tropical conditions; when incubated at xxx–37 °C in the laboratory, naturally present E. coli can abound in soil to concentrations of ∼five log₁₀ per gram (similar to the soil E. coli levels in our written report).⁶⁵ However, testing of a subset of our soil samples with biochemical assays, phylogrouping and PCR detection of genes associated with enteric vs environmental origin showed no differences betwixt E. coli isolates in soil vs those from fecal samples collected from cattle, chickens, and humans in the study area.⁶⁶ Additionally, qPCR testing of our soil samples for microbial source tracking markers revealed high prevalence of ruminant and avian fecal molecular markers, providing prove for contamination of fecal origin from animal sources, while human fecal markers were rare.^xx This bear witness suggests that, while E. coli tin bespeak fecal contamination, its presence should not be interpreted as evidence of strictly human fecal contagion when animals are nowadays.

Due east. coli is besides imperfectly correlated with the presence of fecal pathogens.⁵⁰ The associations we observed between animal feces and E. coli therefore do not provide standalone evidence for pathogen transmission from animal feces to the domestic environment.⁶⁷ Multiplex PCR testing of a subset of E. coli-positive food and fly samples from our study found pathogenic E. coli genes in 14% of E. coli-positive nutrient and 2% of E. coli-positive flies.⁶⁸ A previous study in rural Bangladesh found that among tubewells with one–x MPN/100 mL Eastward. coli (like to our tubewell E. coli levels), pathogenic E. coli was detected past qPCR in 21%, rotavirus in 57%, Shigella in 7% and Vibrio cholerae in vii% of wells.⁶⁹ Some other report in a similar Bangladeshi setting found that, while 97% of soil samples were positive for E. coli, only 14% contained pathogenic E. coli detected by multiplex PCR.^thirteen Nevertheless, despite its limitations every bit an indicator organism, Due east. coli is used globally to monitor microbiological contamination.^seventy−72 A systematic review has demonstrated that Due east. coli in drinking water is associated with diarrhea, supporting its utilise as an indicator for diarrhea-causing pathogens.⁷³

Some other limitation is that we collected all ecology samples simultaneously; we therefore cannot ascertain the causal direction of observed associations. For example, nosotros tin can only hypothesize that soil contamination preceded the associated contamination of hands, stored water and nutrient, and not vice versa. However, while nosotros cannot directly compare levels of contamination forth the different pathways due to unlike reporting units and detection limits, the ecology media we would expect to exist more proximal to fecal sources (due east.g., soil, ponds, flies) were more than heavily contaminated than those farther down the transmission pathway (e.g., easily, stored water, food). Similarly, all molecular fecal markers had higher prevalence in soil than on hands or in stored h2o,²⁰ although information technology is difficult to compare PCR results across sample types because of differential recovery efficiency. This pattern is consistent with the assumption that contamination would progressively subtract as we move further from fecal sources due to limited transfer efficiencies of transmitting vectors/fomites. I could therefore assume that heavily contaminated soils and ponds led to the lower levels of contamination observed on hands, stored h2o, and nutrient, and not vice versa.

A related limitation is that we sampled each household once. Domestic contamination levels vary temporally, fifty-fifty within 1 solar day;⁷⁴ this variation is not captured by our one-time sampling. Due east. coli counts in duplicate samples collected simultaneously from the aforementioned household in x% of households were correlated 69–79% depending on sample type; repeat samples nerveless at different times would likely exhibit greater variability.

Finally, our analysis was observational and therefore susceptible to confounding. A recent report in Bharat found that animal ownership was associated with college socioeconomic status.⁶⁰ Most all compounds in our study owned domestic animals. Socioeconomic proxies were non associated with animal ownership but significantly associated with the presence of animal feces. We controlled for housing materials, reported income, land ownership, presence of electricity, and caregivers' education in all models; all the same, information technology is possible that residual misreckoning remained in our analysis.

Conclusions

We provide a novel assessment of fecal contamination along several different pathogen transmission pathways in the household environment in a setting with loftier on-site sanitation coverage. Our findings demonstrate widespread fecal contagion. The presence of animals and animal feces, peculiarly chickens, was associated with domestic fecal contamination. It is likely that animate being feces are a dominant source of fecal contamination in low-income country settings with high sanitation coverage and low rates of open defecation; under these circumstances, fecal indicator bacteria will be poor proxies for human fecal contamination. Intervention studies on hygienic removal of animal carrion from children's environment can assess whether reducing exposure to fecal contamination from brute sources tin reduce kid enteric illness.

Acknowledgments

This research was financially supported [in function] by Grant OPPGD759 from the Bill & Melinda Gates Foundation to the University of California, Berkeley, and by a grant from the Earth Bank to the International Centre for Diarrhoeal Illness Research, Bangladesh.

Writer Contributions

^○ Co-primary writer with equal contribution.

Notes

The authors declare no competing fiscal interest.

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Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5541329/

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