Taking care of the backside: Aspects of the sanitation chain beyond the household toilet and their associations with fecal contamination in the public and private domains and enteric infection risk in children Public
Berendes, David (2016)
Abstract
Enteric infections cause over 1.7 billion cases of diarrhea each year and other long-term morbidity, especially in children. Exposure to fecal contamination, and subsequent enteric infection risk, occurs in both public and private domains, especially in urban slums, where interactions between household-level sanitation, neighborhood-level fecal sludge management (FSM), and fecal contamination are poorly understood. This dissertation examined the interactions of household sanitation and FSM, and their spatial heterogeneity, in poor urban neighborhoods in Accra, Ghana and Vellore, India, and evaluated associations with fecal contamination in both domains and risk of enteric infection. Household surveys described household and neighborhood structural and behavioral risk factors, which were tested for local spatial clustering and overlaid on drainage maps. Fecal indicator bacteria and selected enteric pathogens were quantified in environmental samples inside and outside the household. Stool samples collected from children in both cross-sectional and longitudinal studies were tested for a panel of enteropathogens. Associations between microbiological outcomes and household or neighborhood risk factors were examined by generalized linear models. Cross-sectional study results in Accra indicated that sub-neighborhood clustering of household sanitation with good FSM was associated with lower levels of fecal indicator bacteria, but not human enteric viruses, in open drains. Cross-sectional study results from Vellore suggested that poor FSM was associated with higher prevalence of pediatric enteric infection and higher concentrations of norovirus in drains. Further, associations between household sanitation and within-household fecal contamination varied by neighborhood coverage level and household hygiene practices. The longitudinal assessment of enteric infection in 0-2 year olds suggested that aspects of neighborhood-level FSM and urban geography--clustering of flooding during a monsoon--affect enteric infection risk independent of exposure behaviors. Further, enteric viruses were major causes of diarrhea with atypical associations with "traditional" water, sanitation, and hygiene-associated risk factors, requiring new strategies for mitigation. Overall, this dissertation underscores the importance of the public domain and urban geography in fecal contamination exposures and enteric infection risk. The spatial heterogeneity and FSM associated with household sanitation have community-level exposure and health implications, which must be measured and accounted for in future infrastructural and behavioral interventions.
Table of Contents
Introduction 1
Enteric organisms and environmental transmission 1
Sanitation-related approaches to containing enteric organisms and fecal contamination 3
Figure I-1: The F-diagram 4
Spatial Analysis and WASH-associated Infections 6
Measurement of health outcomes 8
Measurement of exposure outcomes 9
Sanitation and Risk of Exposure to Fecal Contamination in the Urban Environment 14
Recent approaches to quantifying health risks from poor urban sanitation 19
Study cities 22
Rationale and Aims of the Dissertation 23
Urban Sanitation Coverage and Environmental Fecal Contamination: Links Between the Household and Public Environments 25
Abstract 26
Introduction 27
Methods 29
Study Site 29
Ethics 30
Environmental Sampling and Processing 30
Household Surveys 31
Public Toilet Surveys 32
Analyses 33
Results 35
Neighborhood demographics and coverage/clustering of household sanitation 35
Variation in environmental fecal contamination between urban neighborhoods and by season 36
Variation in environmental fecal contamination by animal ownership and population density 37
Variation in E. coli contamination in soil by neighborhood sanitation 37
Variation in E. coli contamination in drain water by neighborhood sanitation 38
Variation in enteric virus detection in drain water by neighborhood sanitation 39
Discussion 40
Tables and Figures 47
Table 1: Population density, animal ownership, and neighborhood sanitation, including spatial clustering 47
Table 2: E. coli concentrations and enteric virus detection in public domain samples, by neighborhood 48
Table 3: E. coli contamination in soil in the public domain by sanitation coverage cluster 49
Table 4: E. coli contamination in public drains by sanitation coverage cluster 50
Figure 1: Neighborhood sanitation coverage and sample sites, Shiabu, Accra, Ghana 51
Supporting Information (SI) 52
Table S1: E. coli contamination in soil and drains by season, population density, and local household animal ownership 54
Table S2: E. coli contamination in soil in the public domain by local sanitation coverage 54
Table S3: E. coli contamination in public drains by local sanitation coverage 55
Table S4: Adenovirus, NoV GI, and NoV GII contamination in public drains by local sanitation 56
Table S5: Adenovirus, NoV GI, and NoV GII contamination in public drains by sanitation coverage cluster 57
The Influence of Household- and Community-Level Sanitation and Fecal Sludge Management on Urban Fecal Contamination in Households and Drains and Enteric Infection in Children 59
Abstract 60
Introduction 61
Materials and Methods 63
Data source 63
Study site 64
Ethical approval 65
Environmental and stool sample collection, analysis, and processing 65
Survey data collection 69
Analyses 69
Results 71
Frequency and within-neighborhood spatial clustering of household sanitation 71
Microbiological concentrations in environmental samples and enteric pathogen detection in stool 72
Association between household- and cluster-level sanitation coverage, FSM practices, and within-household fecal contamination 74
Association between demographics, neighborhood, and household- and cluster-level sanitation variables and fecal contamination outside the household 75
Household- and cluster-level sanitation and enteric infection in children 76
Discussion 76
Tables and Figures 84
Table 1: Reported frequency and clustering of household sanitation and fecal sludge management (FSM) in Chinnallapuram and Old Town 84
Table 2: Variation in detection and concentrations of E. coli in environmental samples within households with neighborhood and hygiene status 85
Table 3: Variation in detection of enteric pathogens in stool with neighborhood and hygiene statusa 85
Table 4: Variation in GII norovirus detection and concentration in drain water 86
Table 5: Any enteric pathogen detection in child stoola by household- and cluster-level attributesb 87
Figure 1a: Sanitation coverage and clustering in Chinnallapuram. 88
Figure 1b: Sanitation coverage and clustering in Old Town 89
Supplemental Information 90
Table S1: Analysis of E. coli concentrations in child hand rinses by household- and cluster-level sanitation and FSMa 90
Table S2: Analysis of E. coli concentrations in household swabs by household- and cluster-level sanitation and FSMa 91
Table S3: Analysis of E. coli concentrations in sentinel object rinses by household- and cluster-level sanitation and FSMa 92
Risk Factors for Pediatric Enteric Infection in a Low-Income Urban Neighborhood: Examining the Contributions of the Household Environment, Neighborhood Geography, and Exposure Behaviors 93
Abstract 94
Author Summary 95
Introduction 96
Methods 99
Data sources 99
Study site 99
Ethical approval 100
Stool specimen collection and testing 100
Transect walks and household survey data collection: SaniPath Tool 101
Survey data collection: public toilet surveys 102
Analyses 102
Results 103
Household and neighborhood environments and exposure behaviors in the study neighborhood 103
Public toilet maintenance and conditions 105
Distribution of pathogenic organisms in children's stool 105
Pathogens associated with diarrheal stool 106
Spatial and temporal clustering of enteric infections 106
Effect of household and neighborhood environments on enteric infection risk, by pathogen type 107
Effect of exposure behaviors on enteric infection risk, by pathogen type 109
Multivariate modeling of enteric infection, by pathogen type 110
Discussion 111
Tables and Figures 119
Table 1: Reported household/neighborhood conditions and exposure behaviorsa 119
Table 2: Detection of pathogens in children's stool in SaniPath and all MAL-ED households from 2010-2014 120
Table 3: Bivariate relationships between household and neighborhood conditions and pathogen detection in stool collected from children in SaniPath households, 2010-2014a 121
Table 4: Bivariate relationships between spatial clustering of flooding in neighborhood, seasonality, and pathogen detection in stool collected from children in SaniPath households, 2010-2014a 122
Table 5: Bivariate relationships between household exposure behaviors and pathogen detection in stool collected from children in SaniPath households, 2010-2014a 123
Table 6: Multivariate fecal exposure models by pathogen group for children in SaniPath households, 2010-2014a 124
Figure 1: Reported drain and house flood clustering, Old Town 125
Figure 2: Space-time clustering of infections, Old Town, 2011 126
Figure 3: Space-time clustering of infections, Old Town, 2012 127
Conclusions 128
Strengths and Limitations 131
Future Directions 135
Policy and Involvement of Local Governments and Communities 136
Research and Evaluation 138
Contribution to the field 141
Appendix: Additional analyses and data 142
Aim 1 (Accra, Ghana) 142
Associations between drain size, construction, and detection of enteric viruses 142
Associations between sanitation variables and Ct values of enteric viruses in Accra, Ghana 145
Table A1.2: Adenovirus, NoV GI, and NoV GII Ct values for public drain water by local sanitation prevalence in Accra, Ghana 147
Table A1.3: Adenovirus, NoV GI, and NoV GII Ct values for public drain water by sanitation coverage cluster in Accra, Ghana 148
Aim 2 (Vellore, India) 149
Christian Medical College Hygiene Survey 149
Correlation between fecal contamination levels in different types of environmental samples 149
Table A2.1: Correlations between sample types within and outside the household 150
Further spatial analysis in Vellore, India 151
Final multivariate fecal contamination models 152
Fecal contamination associations with enteric infection 155
Table A2.3: Any enteric pathogen detection in child stool by E. coli concentrations in environmental samples 155
Aim 3 (Vellore, India) 156
Methods: Model for mixed-effects logistic regression (logistic regression with a random intercept) 156
Burden of enteric infection 156
Differences in burden of enteric infection by follow-up period 162
Incidence of enteric infection during the first two years of life 167
Tests of global autocorrelation, local autocorrelation, and spatial clustering for burden of enteric infection 173
Tests of global autocorrelation for residuals of final models in Aim 3 174
Spatial network-based clustering analysis of enteric infection 174
Tests of spatial, temporal, and space-time clustering of coinfections 183
Tests of spatial autocorrelation among mixed-effects logistic regression models 185
Modeling of symptomatic stool 186
Hazard analysis of enteric infection 187
Retesting of household and neighborhood risk factors, controlling for breastfeeding status 192
Further discussion of results from Aim 3: 198
Discussion of pathogen group-specific findings from Aim 3: 198
References 200
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