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Posted Content•DOI•

Impact of an Urban Sanitation Intervention on Enteric Pathogen Detection in Soils

Drew Capone1, David Berendes2, Oliver Cumming3, David A. Holcomb1, Jackie Knee3, Konstantinos T. Konstantinidis4, Karen Levy5, Rassul Nalá, Benjamin B. Risk6, Jill R. Stewart1, Joe Brown1 •
University of North Carolina at Chapel Hill1, Centers for Disease Control and Prevention2, University of London3, Georgia Institute of Technology4, University of Washington5, Emory University6
02 Apr 2021-bioRxiv (Cold Spring Harbor Laboratory)-
TL;DR: In this article, the impact of a shared onsite sanitation intervention in Maputo, Mozambique on enteric pathogens in the domestic environment was evaluated by collecting 179 soil samples at shared latrine entrances from intervention (n = 49) and control (n= 51) compounds during baseline and after 24 months.
Abstract: Environmental fecal contamination is common in many low-income cities, contributing to a high burden of enteric infections and associated negative sequelae. To evaluate the impact of a shared onsite sanitation intervention in Maputo, Mozambique on enteric pathogens in the domestic environment, we collected 179 soil samples at shared latrine entrances from intervention (n= 49) and control (n= 51) compounds during baseline (pre-intervention) and after 24 months (post-intervention) as part of the Maputo Sanitation Trial. We tested soils for the presence of nucleic acids associated with 20 enteric pathogens using a multiplex reverse transcription qPCR platform. We detected at least one pathogen-associated target in 91% (163/179) of soils and a median of 3 (IQR=1.5, 5) pathogens. Using a difference-in-difference analysis and adjusting for compound population, visibly wet soil, sun exposure, wealth, temperature, animal presence, and visible feces, we estimate the intervention reduced the probability of ≥1 pathogen detected by 15% (adjusted prevalence ratio, aPR=0.85; 95% CI: 0.70, 1.0) and the total number of pathogens detected by 35% (aPR =0.65; 0.44, 0.95) in soil 24 months following the intervention. These results suggest that the intervention reduced the presence of some fecal contamination in the domestic environment, but pathogen detection remained prevalent 24-months following the introduction of new latrines.

Summary (2 min read)

Jump to: [Introduction] – [Sample Collection] – [Sample Processing] – [Data analysis] and [Matched samples]

Introduction

  • Environmental fecal contamination is common in many low-income cities, contributing to a high burden of enteric infections and associated negative sequelae.
  • Enteric pathogens may still move into soils through open defecation19, unhygienic pit emptying20,21, fecally contaminated greywater22,23, improper disposal of children’s feces or anal cleansing materials24,25, latrine flooding20,26,27, animal feces28–30, or subsurface transport from unlined pits31–33.
  • Control compounds were concurrently enrolled from the same or adjacent neighborhoods as intervention compounds and continued using existing shared sanitation infrastructure.
  • This high risk of fecal contamination suggests the authors could plausibly observe a reduction in enteric pathogens in soil at latrine entrances if the intervention infrastructure performed better than controls at safely containing fecal wastes.

Sample Collection

  • The authors prospectively collected latrine entrance soil samples – defined as a location one-meter away from the latrine entrance in the direction of entry or the nearest point not covered by cement – from 49 intervention and 51 control compounds at baseline (pre-intervention) and from the same compounds 24-months following the intervention, for a total of 200 samples (Text S2).
  • The spade and ruler were sterilized between uses with 10% bleach and 70% ethanol.
  • At the time of sampling, enumerators recorded whether the soil was visibly wet and estimated the daily sun exposure (full sun, partially shaded, full shade).
  • 44 Samples were stored on ice for transport to the Ministry of Health in Maputo, Mozambique, frozen at -20oC for approximately six months, aliquoted into 2 ml cryovials while working on dry ice, and then stored at -80oC.
  • CC-BY-NC-ND 4.0 International licenseavailable under a was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.

Sample Processing

  • At Georgia Institute of Technology in Atlanta, GA, USA, the authors incubated 250 mg of each soil sample at 105oC for 1 hour to determine moisture content13,59, then discarded the dry soil.
  • The authors then extracted total nucleic acids from a separate 1-gram (calculated for dry weight) portion of each sample, and spiked samples with MS2 (Luminex Corporation, Austin, TX) as an extraction control.
  • The copyright holder for this preprint (whichthis version posted April 2, 2021.
  • The positive control was a plasmid that included all assay gene sequences and the negative control was either extract from a negative extraction control or sterile water.

Data analysis

  • The authors analyzed data in R version 4.0.0 (R Foundation for Statistical Computing, Vienna, Austria).
  • The copyright holder for this preprint (whichthis version posted April 2, 2021.
  • Likewise, the authors fit DID models to estimate the intervention’s impact for each individual pathogen assessed, but they excluded any pathogen not detected in at least 5% of control and intervention samples during both phases.
  • Ethics .CC-BY-NC-ND 4.0 International licenseavailable under a was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
  • The overall trial was pre-registered at ClinicalTrials.gov (NCT02362932), but the authors did not pre-register this environmental analysis.

Matched samples

  • The authors analyzed latrine entrance soils collected at baseline from 48 control compounds and 43 intervention compounds, and soils collected at the 24-month phase from 45 control and 43 intervention compounds (Table S4).
  • The copyright holder for this preprint (whichthis version posted April 2, 2021.

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1
IMPACT OF AN URBAN SANITATION INTERVENTION ON ENTERIC
PATHOGEN DETECTION IN SOILS
Authors: Drew Capone
1
, David Berendes
2
, Oliver Cumming
3
, David Holcomb
4
, Jackie Knee
3
,
Konstantinos T. Konstantinidis
5
, Karen Levy
6
, Rassul Nalá
7
, Benjamin B. Risk
8
, Jill Stewart
1
,
Joe Brown
1
*
1. Department of Environmental Sciences and Engineering, Gillings School of Public
Health, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United
States of America
2. Waterborne Disease Prevention Branch, Division of Foodborne, Waterborne, and
Environmental Diseases, National Center for Emerging Zoonotic and Infectious Diseases,
Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America
3. Department of Disease Control, London School of Hygiene and Tropical Medicine,
London, United Kingdom
4. Department of Epidemiology, Gillings School of Global Public Health, University of
North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America
5. Civil and Environmental Engineering, Georgia Institute of Technology, 311 Ferst Drive,
Atlanta, Georgia, United States of America
6. Environmental and Occupational Health Sciences, University of Washington, 2980 15th
Ave NE, Seattle, Washington, United States of America
7. Ministério da Saúde, Instituto Nacional de Saúde Maputo, Maputo, Mozambique
8. Department of Biostatistics and Bioinformatics, Emory University, Atlanta, Georgia,
United States of America
*Corresponding author: Joe Brown
Phone: +1 919-360-8752
Email: joebrown@unc.edu
Address: 135 Dauer Dr, Chapel Hill, NC 27599, USA
.CC-BY-NC-ND 4.0 International licenseavailable under a
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprint (whichthis version posted April 2, 2021. ; https://doi.org/10.1101/2021.04.02.438233doi: bioRxiv preprint
2
ABSTRACT
Environmental fecal contamination is common in many low-income cities, contributing to a high
burden of enteric infections and associated negative sequelae. To evaluate the impact of a shared
onsite sanitation intervention in Maputo, Mozambique on enteric pathogens in the domestic
environment, we collected 179 soil samples at shared latrine entrances from intervention (n= 49)
and control (n= 51) compounds during baseline (pre-intervention) and after 24 months (post-
intervention) as part of the Maputo Sanitation Trial. We tested soils for the presence of nucleic
acids associated with 20 enteric pathogens using a multiplex reverse transcription qPCR
platform. We detected at least one pathogen-associated target in 91% (163/179) of soils and a
median of 3 (IQR=1.5, 5) pathogens. Using a difference-in-difference analysis and adjusting for
compound population, visibly wet soil, sun exposure, wealth, temperature, animal presence, and
visible feces, we estimate the intervention reduced the probability of ≥1 pathogen detected by
15% (adjusted prevalence ratio, aPR=0.85; 95% CI: 0.70, 1.0) and the total number of pathogens
detected by 35% (aPR =0.65; 0.44, 0.95) in soil 24 months following the intervention. These
results suggest that the intervention reduced the presence of some fecal contamination in the
domestic environment, but pathogen detection remained prevalent 24-months following the
introduction of new latrines.
.CC-BY-NC-ND 4.0 International licenseavailable under a
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprint (whichthis version posted April 2, 2021. ; https://doi.org/10.1101/2021.04.02.438233doi: bioRxiv preprint
3
INTRODUCTION
Onsite sanitation systems are designed to sequester human feces away from human contact and
prevent the transport of fecal-oral pathogens through well-understood transmission pathways.
1
Large-scale, rigorous randomized controlled trials (RCTs) of onsite sanitation systems –
including sanitation alone and combinations of water, sanitation, and hygiene (WASH)
interventions – have found mixed effects on health outcomes, such as diarrhea and child
growth.
2–7
Assessing the impact of WASH interventions on enteric pathogens in the environment
can improve our understanding of pathogen transmission from an infected individual to a new
host via the environment, a core intermediate outcome of these trials. Such data may help explain
why some WASH interventions observed improved health outcomes and others did not.
8
There is a growing body of literature that soils contaminated by feces in public and domestic
environments pose infection risks.
9–13
In health impact trials that assess improved onsite
sanitation systems, soils are assessed to measure how effectively the intervention sequestered
human feces.
14–18
Latrines and septic tanks are useful barriers against the transport of human
feces into the environment. However, enteric pathogens may still move into soils through open
defecation
19
, unhygienic pit emptying
20,21
, fecally contaminated greywater
22,23
, improper disposal
of children’s feces or anal cleansing materials
24,25
, latrine flooding
20,26,27
, animal feces
28–30
, or
subsurface transport from unlined pits
31–33
. Domestic soils contaminated by enteric pathogens
can pose infection risks beyond incidental
34
and direct
35
soil ingestion: contaminated soil may be
transported to hands, food, fomites, or household stored water.
36
For these reasons, soils may be
a useful matrix to assess the impact of onsite sanitation interventions.
.CC-BY-NC-ND 4.0 International licenseavailable under a
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprint (whichthis version posted April 2, 2021. ; https://doi.org/10.1101/2021.04.02.438233doi: bioRxiv preprint
4
Detecting enteric pathogens via molecular methods is increasingly used to assess the impact of
WASH interventions on the transport of these pathogens through the environment.
37–39
Molecular detection of pathogens offers additional insights, as health impact studies have
historically relied on fecal indicator bacteria (FIB), as a proxy for enteric pathogens for reasons
of cost, capacity and feasibility.
17,36,40–42
However, a 2016 meta-analysis
43
found that improved
sanitation had no effect on the presence of FIB in the environment, possibly because these
indicators are often pervasive in low-income settings
15,16,36,44–46
and common FIB, like E. coli,
may be naturalized in the environment
47–49
.
The Maputo Sanitation (MapSan) Trial was the first rigorous controlled before-and-after trial to
evaluate the effect of an urban onsite sanitation intervention on child health.
24,50,51
We conducted
the trial in low-income, informal neighborhoods in Maputo, Mozambique, where WASH
conditions are poor, and the burden of enteric disease is high.
20,24,44,52
Water and Sanitation for
the Urban Poor (WSUP, a non-governmental organization) delivered the intervention to
compounds composed of household clusters that shared sanitation and courtyard space. The
intervention was built inside the compound boundary and was part of the households’ living
environment. WSUP replaced shared onsite sanitation systems in poor condition with pour-flush
toilets that included septic tanks and soak-away pits (Text S1). Control compounds were
concurrently enrolled from the same or adjacent neighborhoods as intervention compounds and
continued using existing shared sanitation infrastructure. Detailed descriptions of the inclusion
criteria for intervention and control compounds are described elsewhere.
20,24
A latrine entrance is an ideal soil sampling location to determine the effectiveness of onsite
sanitation interventions because it is a standardized location near the fecal waste in the
containment chamber.
15,16,53
Soils in low-income Maputo are characterized as coarse to fine sand
.CC-BY-NC-ND 4.0 International licenseavailable under a
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprint (whichthis version posted April 2, 2021. ; https://doi.org/10.1101/2021.04.02.438233doi: bioRxiv preprint
5
or silty sand.
54
While the fate and transport of pathogens through soils is dependent on the
individual pathogen and environmental conditions
55
, the high porosity of Maputo’s sandy soils
combined with a high water table in the study area
44
offers potential for pathogen movement.
56
This high risk of fecal contamination suggests we could plausibly observe a reduction in enteric
pathogens in soil at latrine entrances if the intervention infrastructure performed better than
controls at safely containing fecal wastes.
57
Our study aim was to assess if the intervention
reduced the detection of ≥1 pathogen, the total number of pathogens, or any individual pathogen
in latrine entrance soils from MapSan intervention compounds compared to controls.
MATERIALS AND METHODS
Sample Collection
We prospectively collected latrine entrance soil samples – defined as a location one-meter away
from the latrine entrance in the direction of entry or the nearest point not covered by cement –
from 49 intervention and 51 control compounds at baseline (pre-intervention) and from the same
compounds 24-months following the intervention, for a total of 200 samples (Text S2). We
defined this sample location a priori as one that could be standardized across all compounds in
the study. Using a spade and ruler, we scooped a 10 cm x 10 cm x 1 cm volume of soil into a
Whirl-Pak
®
bag (Nasco, Fort Atkinson, WI). The spade and ruler were sterilized between uses
with 10% bleach and 70% ethanol. At the time of sampling, enumerators recorded whether the
soil was visibly wet and estimated the daily sun exposure (full sun, partially shaded, full
shade).
44
Samples were stored on ice for transport to the Ministry of Health in Maputo,
Mozambique, frozen at -20
o
C for approximately six months, aliquoted into 2 ml cryovials while
working on dry ice, and then stored at -80
o
C. During storage at -20
o
C, some samples (n = 21)
.CC-BY-NC-ND 4.0 International licenseavailable under a
was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprint (whichthis version posted April 2, 2021. ; https://doi.org/10.1101/2021.04.02.438233doi: bioRxiv preprint
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[...]

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TL;DR: Working in informal communities of urban Maputo, Mozambique, a quantitative, stochastic, mass-balance approach is developed to evaluate plausible scenarios of localized contamination that could explain why the soil-transmitted helminth Ascaris remains endemic despite nearly universal coverage of latrines that sequester most fecal wastes.
Abstract: In low-income, urban, informal communities lacking sewerage and solid waste services, onsite sanitation (sludges, aqueous effluent) and child feces are potential sources of human fecal contamination in living environments. Working in informal communities of urban Maputo, Mozambique, we developed a quantitative, stochastic, mass-balance approach to evaluate plausible scenarios of localized contamination that could explain why the soil-transmitted helminth Ascaris remains endemic despite nearly universal coverage of latrines that sequester most fecal wastes. We used microscopy to enumerate presumptively viable Ascaris ova in feces, fecal sludges, and soils from compounds (i.e., household clusters) and then constructed a steady-state mass-balance model to evaluate possible contamination scenarios capable of explaining observed ova counts in soils. Observed Ascaris counts (mean = −0.01 log10 ova per wet gram of soil, sd = 0.71 log10) could be explained by deposits of 1.9 grams per day (10th percentile 0.04 grams, 90th percentile 84 grams) of child feces on average, rare fecal sludge contamination events that transport 17 kg every three years (10th percentile 1.0 kg, 90th percentile 260 kg), or a daily discharge of 2.7 kg aqueous effluent from an onsite system (10th percentile 0.09 kg, 90th percentile 82 kg). Results suggest that even limited intermittent flows of fecal wastes in this setting can result in a steady-state density of Ascaris ova in soils capable of sustaining transmission, given the high prevalence of Ascaris shedding by children (prevalence = 25%; mean = 3.7 log10 per wet gram, sd = 1.1 log10), the high Ascaris ova counts in fecal sludges (prevalence = 88%; mean = 1.8 log10 per wet gram, sd = 0.95 log10), and the extended persistence and viability of Ascaris ova in soils. Even near-universal coverage of onsite sanitation may allow for sustained transmission of Ascaris under these conditions.

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Abstract: Estimating the risk of infections or other outcomes incident to pathogen exposure is a primary goal of quantitative microbial risk assessment (QMRA). Such estimates are useful to predict population‐level risks, to evaluate exposures based on normative or tolerable risk guidelines, and to interpret the likely public health relevance of microbial measurements in environmental media. To evaluate alternative control measures (interventions), ratio estimates of effect (e.g., odds and risk ratios) are needed that are more broadly interpretable in the health sciences and consistent with convention in epidemiology. In this paper, we propose a general method for estimating widely used ratio measures of effect derived from stochastic QMRA approaches, including the generation of appropriate confidence intervals. Such QMRA‐derived ratios can be used as a basis for evaluating interventions via hypothesis testing and for inclusion in systematic reviews and meta‐analyses in a form consistent with risk estimation approaches commonly used in epidemiology.

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Abstract: Mass drug administration (MDA) of antimicrobials has shown promise in the reduction and potential elimination of a variety of neglected tropical diseases (NTDs). However, with antimicrobial resistance (AMR) becoming a global crisis, the risks posed by widespread antimicrobial use need to be evaluated. As the role of the environment in AMR emergence and dissemination has become increasingly recognized, it is likewise crucial to establish the role of MDA in environmental AMR pollution, along with the potential impacts of such pollution. This review presents the current state of knowledge on the antimicrobial compounds, resistant organisms, and antimicrobial resistance genes in MDA trials, routes of these determinants into the environment, and their persistence and ecological impacts, particularly in low and middle-income countries where these trials are most common. From the few studies directly evaluating AMR outcomes in azithromycin MDA trials, it is becoming apparent that MDA efforts can increase carriage and excretion of resistant pathogens in a lasting way. However, research on these outcomes for other antimicrobials used in MDA trials is sorely needed. Furthermore, while paths of AMR determinants from human waste to the environment and their persistence thereafter are supported by the literature, quantitative information on the scope and likelihood of this is largely absent. We recommend some mitigative approaches that would be valuable to consider in future MDA efforts. This review stands to be a valuable resource for researchers and policymakers seeking to evaluate the impacts of MDA.

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Long-term impacts of an urban sanitation intervention on enteric pathogens in children in Maputo city, Mozambique: study protocol for a cross-sectional follow-up to the Maputo Sanitation (MapSan) trial five years post-intervention

[...]

David A. Holcomb, Vanessa Monteiro, Drew Capone, Virgilio Santo Antonio, M. Chiluvane, Victória Cumbane, Nália Ismael, Jackie Knee, E. Kowalsky, A Lai, Yarrow S. Linden, E. Mataveia, R. Nalá, Gabriella A Rao, Joana Ribeiro, Oliver Cumming, E Viegas, J. Brown 
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01 Jan 2006-Applied and Environmental Microbiology
TL;DR: The first report of the growth of naturalized E. coli in nonsterile, nonamended soils in northern temperate soils is reported, which may confound the use of this bacterium as an indicator of fecal contamination.
Abstract: The presence of Escherichia coli in water is used as an indicator of fecal contamination, but recent reports indicate that soil populations can also be detected in tropical, subtropical, and some temperate environments. In this study, we report that viable E. coli populations were repeatedly isolated from northern temperate soils in three Lake Superior watersheds from October 2003 to October 2004. Seasonal variation in the population density of soilborne E. coli was observed; the greatest cell densities, up to 3 × 103 CFU/g soil, were found in the summer to fall (June to October), and the lowest numbers, ≤1 CFU/g soil, occurred during the winter to spring months (February to May). Horizontal, fluorophore-enhanced repetitive extragenic palindromic PCR (HFERP) DNA fingerprint analyses indicated that identical soilborne E. coli genotypes, those with ≥92% similarity values, overwintered in frozen soil and were present over time. Soilborne E. coli strains had HFERP DNA fingerprints that were unique to specific soils and locations, suggesting that these E. coli strains became naturalized, autochthonous members of the soil microbial community. In laboratory studies, naturalized E. coli strains had the ability to grow and replicate to high cell densities, up to 4.2 × 105 CFU/g soil, in nonsterile soils when incubated at 30 or 37°C and survived longer than 1 month when soil temperatures were ≤25°C. To our knowledge, this is the first report of the growth of naturalized E. coli in nonsterile, nonamended soils. The presence of significant populations of naturalized populations of E. coli in temperate soils may confound the use of this bacterium as an indicator of fecal contamination.

514 citations

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