PUBLICATIONS
Dr. Levy's Google Scholar Page
(PDFs for personal use are available upon request)
TITLE & AUTHORS Abstract
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Ballard A. M., B. C. Angulo, N. Laramee , J. P. Gallagher, R. Haardörfer, M. C. Freeman, J. Trostle, J. N. S. Eisenberg, G. O. Lee, K. Levy, B. A. Caruso.
Multilevel factors drive child exposure to enteric pathogens in animal feces: A qualitative study in northwestern coastal Ecuador PLOS Global Public Health / 2024 |
Exposure to animal feces and associated enteric pathogens poses significant risks to child health. However, public health strategies to mitigate enteric infections among children largely aim to reduce exposure to human feces, overlooking transmission pathways related to animal feces. In this study we examine if and how children are exposed to enteric pathogens in animal feces in northwestern coastal Ecuador. We conducted qualitative interviews with mothers of children aged 10–18 months that owned (n = 32) and did not own (n = 26) animals in urban and rural communities. Using thematic analysis, we identified community, household, and child behavioral factors that influence exposure. We also compared child exposure by household animal ownership. Our findings revealed myriad opportunities for young children to be exposed to enteric pathogens in many locations and from multiple animal sources, regardless of household animal ownership. Animal feces management practices (AFM) used by mothers, such as rinsing feces into ditches and throwing feces into surrounding areas, may increase environmental contamination outside their homes and in their communities. Unsafe AFM practices were similar to unsafe child feces management practices reported in other studies, including practices related to defecation location, feces removal and disposal, environmental contamination cleaning, and handwashing. Findings suggest that animal feces may contaminate the environment along similar pathways as human feces. Identification and incorporation of safe AFM practices, similar to those developed for child feces management, would 1) mitigate child exposure to enteric pathogens by reducing animal feces contamination in domestic and public spaces; and 2) enable an integrated approach to address enteric pathogen exposure pathways related to animal and child feces.
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Ballard A. M., R. Haardörfer, B. C. Angulo, M. C. Freeman, J. N. S. Eisenberg, G. O. Lee, K. Levy, B. A. Caruso.
The development and validation of a survey to measure fecal-oral child exposure to zoonotic enteropathogens: The FECEZ Enteropathogens Index PLOS Global Public Health / 2024 |
Child exposure to animal feces and associated enteropathogens contribute to a significant burden of disease in low- and middle-income countries. However, there are no standardized, validated survey-based approaches to enable accurate assessment of child exposure to zoonotic enteropathogens. We developed and validated a survey-based measure of exposure, the fecal-oral child exposure to zoonotic enteropathogens Index (the FECEZ Enteropathogens Index). First, we identified critical attributes of child exposure through in-depth interviews (IDIs) in Ecuador among individuals who care for animals (n = 29) and mothers of children under two years old (n = 58), and through a systematic review of existing exposure measures. Second, based on these findings, we developed a 105-question survey and administered it to 297 mothers with children under age five. Third, we refined the survey, using principal component analysis to determine the optimal number of components. The final index consisted of 34 items across two sub-domains: the child Environment and child Behavior. Lastly, we compared index scores to two commonly used, unvalidated measures of child exposure–maternal reported household animal ownership and presence of animal feces. Using the FECEZ Enteropathogens Index revealed varying degrees of exposure in our study population, with only two children having no exposure. In contrast, if we had used animal ownership or the presence of animal feces as a measure of exposure, 44% and 33% of children would have been classified as having no exposure, respectively. These common binary exposure measures may be inadequate because they do not provide sufficient information to identify the relative risk of zoonotic pathogen exposure. The FECEZ Enteropathogens Index overcomes this limitation, advancing our ability to assess exposure by quantifying the multiple components of child exposure to zoonotic enteropathogens with higher resolution. Additional testing and evaluation of the index is needed to ensure its reliability, validity, and cross-cultural equivalence in other contexts.
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Calvopina M., D. Aguilar-Rodríguez, A. DeGroot, W. Cevallos, G.O. Lee, A. Lopez, T.B. Nutman, K. Levy, J.N.S. Eisenberg, W.J. Sears, P.J. Cooper
Anthroponotic and Zoonotic Hookworm DNA in an Indigenous Community in Coastal Ecuador: Potential Cross-Transmission between Dogs and Humans Pathogens / 2024 |
Humans can be infected with anthroponotic (Ancylostoma duodenale and Necator americanus) and with zoonotic (Ancylostoma ceylanicum, A. caninum, A. braziliense, and Uncinaria stenocephala) hookworms from dogs. Anthroponotic species are usually thought not to infect dogs. We used the internal transcribed spacer–1 (ITS1) gene in a quantitative PCR to detect anthroponotic and zoonotic hookworm species in fecal samples from 54 children and 79 dogs living in an indigenous community in tropical Northwestern Ecuador. Hookworm DNA was detected in 59.3% of children and 92.4% of dogs. Among samples from children, zoonotic hookworms were detected in 24.1% (A. ceylanicum 14.8%, A. caninum 11.1%, and A. braziliense 1.9%), whilst in dog samples, anthroponotic species were detected in 19.0% (N. americanus 12.4% and A. duodenale 6.3%). Sanger sequencing was performed successfully on 60 qPCR-positive samples (16 from children and 44 from dogs), and consensus sequences were obtained with >98% homology to GenBank references for hookworm spp. Phylogenetic analysis showed a close relationship between anthroponotic and zoonotic Ancylostoma species and no heterogeneity between A. duodenale and A. caninum; in human samples, we found A. ceylanicum but not A. braziliense sequences and we were unable to identify N. americanus in the dog samples. No infections with U. stenocephala were detected. Our data provide evidence for high rates of hookworm infections in indigenous children and dogs in a marginalized rural setting in coastal Ecuador. We also found evidence for potential cross-transmission of hookworm spp. between humans and dogs that represent a potential domestic reservoir for zoonotic and anthroponotic hookworms.
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O’Brien L.A., J.S. Snyder, J.V. Garn, R. Kann, A. Júnior, S. McGunegill, B. Muneme, J. L. Manuel, R. Nalá, K. Levy, M.C. Freeman.
Water, food, and mental well-being: Associations between drinking water source, household water and food insecurity, and mental well-being of low-income pregnant women in urban Mozambique PLOS WATER / 2024 |
Drinking water access and water and food insecurity have been linked to mental well-being, but few studies have comprehensively assessed potential pathways linking these associations. Understanding these mediation pathways is particularly important among pregnant women, as prenatal stress and poor mental well-being have been shown to negatively impact fetal development. In this study, we address this gap by analyzing the relationships between drinking water source and water and food insecurity with mental well-being amongst pregnant women living in low-income, urban neighborhoods of Beira, Mozambique. Data for this cross-sectional analysis were collected among third-trimester, pregnant women (n = 740) from February 2021 through October 2022 as part of a matched cohort study. Validated, cross-cultural measures of mental well-being and household water and food insecurity were administered in the survey. Drinking water source was determined by presence of a household drinking water source on-premises. We used logistic regression to characterize the associations between drinking water source, water and food insecurity, and mental well-being and causal mediation analysis to determine mediation by food and water insecurity along these pathways. We found evidence that water insecurity (OR 1.44; 95%CI 1.02, 2.02) and food insecurity (OR 2.27; 95%CI 1.57, 3.34) were individually associated with adverse mental well-being. Drinking water source was not associated with mental well-being (OR 1.00; 95%CI 0.71, 1.39), water insecurity (OR 0.86; 95%CI 0.60, 1.24), or food insecurity (OR 1.02; 95%CI 0.71, 1.47). Food insecurity may also mediate the relationship between water insecurity and mental well-being (ACME 0.05; 95%CI 0.02, 0.07; ADE 0.04; 95%CI -0.04, 0.13). Our findings support growing literature that water and food insecurity are important to mental well-being, a key aspect of overall health. Further research is needed to confirm causality along these pathways and determine specific mechanisms through which these interactions take place.
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Culquichicón C., D. Astudillo-Rueda, R. Niño-Garcia, R.N. Martinez-Rivera, N.M. Tsui, R.H. Gilman, K. Levy, A.G. Lescano
Post-traumatic stress disorder, food insecurity, and social capital after the 2017 coastal El Niño flooding among mothers from Piura, Peru: A mixed method study PLOS GLOBAL PUBLIC HEALTH / 2024 |
In order to understand the impacts in the post-disaster scenario of the 2017 El Niño events in the Piura region-Peru, we examined post-traumatic stress disorder (PTSD), food insecurity (FI), and social capital (SC) across three-time points in mothers in highly affected areas. In the Piura, Castilla, and Catacaos districts, we studied mothers combining mixed-method assessments at three (June-July 2017), eight and 12 months after the flooding. Each outcome was measured with the PTSD-Checklist-Civilian (PCL-C), the Household-Food-Insecurity-Access-Scale (HFIAS), the Adapted-Social-Capital-Assessment-Tool (SASCAT) surveys. In-depth interviews at the first evaluation were also conducted. At the first evaluation, 38.1% (n = 21) of 179 mothers reported PTSD; eight months and one year after the flooding, it dropped to 1.9% and virtually zero, respectively. Severe FI also declined over time, from 90.0% three months after the flooding to 31.8% eight months after, to 13.1% one year after. Conversely, high-cognitive SC was increased three months after the flooding (42.1%) and much greater levels at eight and 12 months after (86.7% and 77.7%, respectively). High levels of PTSD and severe FI three months after the flooding consistently decreased to nearly zero one-year post-disaster. High levels of high-cognitive SC may have helped mothers to recover from PTSD and FI in Piura.
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Royer C., N.V. Patin, K.J. Jesser, A. Peña-Gonzalez, J.K. Hatt, G. Trueba, K. Levy, K.T. Konstantinidis
Comparison of metagenomic and traditional methods for diagnosis of E. coli enteric infections mBio / 2024 |
Diarrheagenic Escherichia coli, collectively known as DEC, is a leading cause of diarrhea, particularly in children in low- and middle-income countries. Diagnosing infections caused by different DEC pathotypes traditionally relies on the cultivation and identification of virulence genes, a resource-intensive and error-prone process. Here, we compared culture-based DEC identification with shotgun metagenomic sequencing of whole stool using 35 randomly drawn samples from a cohort of diarrhea-afflicted patients. Metagenomic sequencing detected the cultured isolates in 97% of samples, revealing, overall, reliable detection by this approach. Genome binning yielded high-quality E. coli metagenome-assembled genomes (MAGs) for 13 samples, and we observed that the MAG did not carry the diagnostic DEC virulence genes of the corresponding isolate in 60% of these samples. Specifically, two distinct scenarios were observed: diffusely adherent E. coli (DAEC) isolates without corresponding DAEC MAGs appeared to be relatively rare members of the microbiome, which was further corroborated by quantitative PCR (qPCR), and thus unlikely to represent the etiological agent in 3 of the 13 samples (~23%). In contrast, ETEC virulence genes were located on plasmids and largely escaped binning in associated MAGs despite being prevalent in the sample (5/13 samples or ~38%), revealing limitations of the metagenomic approach. These results provide important insights for diagnosing DEC infections and demonstrate how metagenomic methods can complement isolation efforts and PCR for pathogen identification and population abundance.
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Ghahyazi, K., I. Familiar-Lopez, O. Culbert, J. Uruchima, A. Van Engen, W. Cevallos, J.N.S. Eisenberg, K. Levy, G.O. Lee
Correlates of maternal depression, anxiety and functioning across an urban-rural gradient in northern Ecuador Global Public Health / 2024 |
Maternal depression remains under characterised in many low- and middle-income countries, especially in rural settings. We aimed to describe maternal depression and anxiety symptoms in rural and urban communities in northern Ecuador and to identify socioeconomic and demographic factors associated with these symptoms. Data from 508 mothers participating in a longitudinal cohort study were included. Depression and anxiety symptoms were assessed using the Hopkins Symptom Checklist (HSCL-25), and maternal psychological functioning was assessed using a checklist of daily activities. Tobit regression models were used to examine associations with sociodemographic variables and urbanicity. The median HSCL-25 score was 1.2 (IQR: 0.4) and 14% of women scored above the threshold for clinically relevant symptoms. Rural women reported similar food insecurity, less education, younger age of first pregnancy, and lower socio-economic status compared to their urban counterparts. After adjusting for these factors, rural women reported lower HSCL-25 scores compared to women in urban areas (β = −0.48, 95%CI:0.65, −0.31). Rural residence was also associated with lower depression and anxiety HSCL-25 sub-scale scores, and similar levels of maternal functioning, compared to urban residence. Our results suggest that both household and community-level factors are risk factors for maternal depression and anxiety in this context.
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Jesser, K. J., G. Trueba, K. T. Konstantinidis, K. Levy
Why are so many enteric pathogen infections asymptomatic? Pathogen and gut microbiome characteristics associated with diarrhea symptoms and carriage of diarrheagenic E. coli in northern Ecuador Gut Microbes / 2023 |
A high proportion of enteric infections, including those caused by diarrheagenic Escherichia coli (DEC), are asymptomatic for diarrhea. The factors responsible for the development of diarrhea symptoms, or lack thereof, remain unclear. Here, we used DEC isolate genome and whole stool microbiome data from a case–control study of diarrhea in Ecuador to examine factors associated with diarrhea symptoms accompanying DEC carriage. We investigated i) pathogen abundance, ii) gut microbiome characteristics, and iii) strain-level pathogen characteristics from DEC infections with diarrhea symptoms (symptomatic infections) and without diarrhea symptoms (asymptomatic infections). We also included data from individuals with and without diarrhea who were not infected with DEC (uninfected cases and controls). i) E. coli relative abundance in the gut microbiome was highly variable, but higher on-average in individuals with symptomatic compared to asymptomatic DEC infections. Similarly, the number and relative abundances of virulence genes in the gut were higher in symptomatic than asymptomatic DEC infections. ii) Measures of microbiome diversity were similar regardless of diarrhea symptoms or DEC carriage. Proteobacterial families that have been described as pathobionts were enriched in symptomatic infections and uninfected cases, whereas potentially beneficial taxa, including the Bacteroidaceae and Bifidobacteriaceae, were more abundant in individuals without diarrhea. An analysis of high-level gene functions recovered in metagenomes revealed that genes that were differentially abundant by diarrhea and DEC infection status were more abundant in symptomatic than asymptomatic DEC infections. iii) DEC isolates from symptomatic versus asymptomatic individuals showed no significant differences in virulence or accessory gene content, and there was no phylogenetic signal associated with diarrhea symptoms. Together, these data suggest signals that distinguish symptomatic from asymptomatic DEC infections. In particular, the abundance of E. coli, the virulence gene content of the gut microbiome, and the taxa present in the gut microbiome have an apparent role.
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Lamar F., H.N. Mucache, A. Mondlane-Milisse, K.J. Jesser, C. Victor, J.M. Fafetine, J.Â.O. Saíde, E.M. Fèvre, B.A. Caruso, M.C. Freeman, K. Levy
Quantifying Enteropathogen Contamination along Chicken Value Chains in Maputo, Mozambique: A Multidisciplinary and Mixed-Methods Approach to Identifying High Exposure Settings Environmental Health Perspectives / 2023 |
Small-scale poultry production is widespread and increasing in low- and middle-income countries (LMICs). Exposure to enteropathogens in poultry feces increases the hazard of human infection and related sequela, and the burden of disease due to enteric infection in children <5 y in particular is substantial. Yet, the containment and management of poultry-associated fecal waste in informal settings in LMICs is largely unregulated. To improve the understanding of potential exposures to enteropathogens carried by chickens, we used mixed methods to map and quantify microbial hazards along production value chains among broiler, layer, and indigenous chickens in Maputo, Mozambique. To map and describe the value chains, we conducted 77 interviews with key informants working in locations where chickens and related products are sold, raised, and butchered. To quantify microbial hazards, we collected chicken carcasses (n=75) and fecal samples (n=136) from chickens along the value chain and assayed them by qPCR for the chicken-associated bacterial enteropathogens C. jejuni/coli and Salmonella spp. We identified critical hazard points along the chicken value chains and identified management and food hygiene practices that contribute to potential exposures to chicken-sourced enteropathogens. We detected C. jejuni/coli in 84 (76%) of fecal samples and 52 (84%) of carcass rinses and Salmonella spp. in 13 (11%) of fecal samples and 16 (21%) of carcass rinses. Prevalence and level of contamination increased as chickens progressed along the value chain, from no contamination of broiler chicken feces at the start of the value chain to 100% contamination of carcasses with C. jejuni/coli at informal markets. Few hazard mitigation strategies were found in the informal sector. High prevalence and concentration of C. jejuni/coli and Salmonella spp. contamination along chicken value chains suggests a high potential for exposure to these enteropathogens associated with chicken production and marketing processes in the informal sector in our study setting. We identified critical control points, such as the carcass rinse step and storage of raw chicken meat, that could be intervened in to mitigate risk, but regulation and enforcement pose challenges. This mixed-methods approach can also provide a model to understand animal value chains, sanitary risks, and associated exposures in other settings.
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Shioda K., A.F. Brouwer, F. Lamar, H.N. Mucache, K. Levy, M.C. Freeman
Opportunities to Interrupt Transmission of Enteropathogens of Poultry Origin in Maputo, Mozambique: A Transmission Model Analysis Environmental Health Perspectives / 2023 |
The burden of diarrheal diseases remains high among children in low-income countries. Enteropathogens are challenging to control because they are transmitted via multiple pathways. Chickens are an important animal protein source, but live chickens and their products are often highly contaminated with enteropathogens. We conducted this study to a) understand the contribution of multiple transmission pathways to the force of infection of Campylobacter spp. and nontyphoidal Salmonella spp., b) quantify the potential impact of reducing each pathway on human infection, and c) quantify hypothesized pathway reduction from the context of Maputo, Mozambique. We developed transmission models for Campylobacter and Salmonella that captured person-to-person, water-to-person, food-to-person, soil-to-person, animal-to-person, and all-other-sources-to-person in an urban, low-income setting in Mozambique. We calibrated these models using prevalence data from Maputo, Mozambique and estimates of attributable fraction of transmission pathways for the region. We simulated the prevalence of human infection after reducing transmission through each pathway. Simulation results indicated that if foodborne transmission were reduced by 90%, the prevalence of Campylobacter and Salmonella infection would decline by [52.2%; 95% credible interval (CrI): 39.7, 63.8] and (46.9%; 95% CrI: 39, 55.4), respectively. Interruption of any other pathway did not have a substantial impact. Combined with survey and microbiology data, if contamination of broiler chicken meat at informal markets in Maputo could be reduced by 90%, the total infection of Campylobacter and Salmonella could be reduced by 21% (16–26%) and 12% (10–13%), respectively. Our transmission models showed that the foodborne transmission has to be reduced to control enteropathogen infections in our study site, and likely in other similar contexts, but mitigation of this transmission pathway has not received sufficient attention. Our model can serve as a tool to identify effective mitigation opportunities to control zoonotic enteropathogens.
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Valenzuela X., H. Hedman, A. Villagomez, P. Cardenas, J.N.S. Eisenberg, K. Levy, L. Zhang, G. Trueba
Distribution of blaCTX-M-gene variants in E. coli from different origins in Ecuador. Medicine in Microecology / 2023 |
The increasing abundance of extended spectrum β-lactamase (ESBL) genes in E. coli, and other commensal and pathogenic bacteria, endangers the utility of third or more recent generation cephalosporins, which are major tools for fighting deadly infections. The role of domestic animals in the transmission of ESBL carrying bacteria has been recognized, especially in low- and middle-income countries, however the horizontal gene transfer of these genes is difficult to assess. Here we investigate blaCTX-M gene diversity (and flanking nucleotide sequences) in E. coli from chicken and humans, in an Ecuadorian rural community and from chickens in another location in Ecuador. The blaCTX-M associated sequences in isolates from humans and chickens in the same remote community showed greater similarity than those found in E. coli in a chicken industrial operation 200 km away. Our study may provide evidence of blaCTX-M transfer between chickens and humans in the community.
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Montero L., S.M. Smith, K.J. Jesser, M. Paez , E. Ortega, A. Peña-Gonzalez, M.J. Soto-Girón, J.K. Hatt, X. Sánchez, E. Puebla, P. Endara, W. Cevallos, K.T. Konstantinidis, G. Trueba, K. Levy
Distribution of Escherichia coli Pathotypes along an Urban-Rural Gradient in Ecuador. American Journal of Tropical Medicine and Hygiene / 2023 |
Diarrheal diseases are a leading cause of mortality and morbidity in low- and middle-income countries. Diarrhea is associated with a wide array of etiological agents including bacterial, viral, and parasitic enteropathogens. Previous studies have captured between- but not within-country heterogeneities in enteropathogen prevalence and severity. We conducted a case-control study of diarrhea to understand how rates and outcomes of infection with diarrheagenic pathotypes of Escherichia coli vary across an urban-rural gradient in four sites in Ecuador. We found variability by site in enteropathogen prevalence and infection outcomes. Any pathogenic E. coli infection, coinfections, diffuse adherent E. coli (DAEC), enteroinvasive E. coli (EIEC), and rotavirus were significantly associated with acute diarrhea. DAEC was the most common pathotype overall and was more frequently associated with disease in urban areas. Enteropathogenic E. coli (EPEC) and enterotoxigenic E. coli (ETEC) were more common in rural areas. ETEC was only associated with diarrhea in one site. Phylogenetic analysis revealed that associations with disease were not driven by any single clonal complex. Higher levels of antibiotic resistance were detected in rural areas. Enteropathogen prevalence, virulence, and antibiotic resistance patterns vary substantially by site within Ecuador. The variations in E. coli pathotype prevalence and virulence in this study have important implications for control strategies by context and demonstrate the importance of capturing within-country differences in enteropathogen disease dynamics.
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Rothstein A.P., K. J. Jesser, D. J. Feistel, K.T. Konstantinidis, G. Trueba, K. Levy
Population genomics of diarrheagenic Escherichia coli uncovers high connectivity between urban and rural communities in Ecuador Infection, Genetics and Evolution / 2023 |
Human movement may be an important driver of transmission dynamics for enteric pathogens but has largely been underappreciated except for international ‘travelers’ diarrhea or cholera. Phylodynamic methods, which combine genomic and epidemiological data, are used to examine rates and dynamics of disease matching underlying evolutionary history and biogeographic distributions, but these methods often are not applied to enteric bacterial pathogens. We used phylodynamics to explore the phylogeographic and evolutionary patterns of diarrheagenic E. coli in northern Ecuador to investigate the role of human travel in the geographic distribution of strains across the country. Using whole genome sequences of diarrheagenic E. coli isolates, we built a core genome phylogeny, reconstructed discrete ancestral states across urban and rural sites, and estimated migration rates between E. coli populations. We found minimal structuring based on site locations, urban vs. rural locality, pathotype, or clinical status. Ancestral states of phylogenomic nodes and tips were inferred to have 51% urban ancestry and 49% rural ancestry. Lack of structuring by location or pathotype E. coli isolates imply highly connected communities and extensive sharing of genomic characteristics across isolates. Using an approximate structured coalescent model, we estimated rates of migration among circulating isolates were 6.7 times larger for urban towards rural populations compared to rural towards urban populations. This suggests increased inferred migration rates of diarrheagenic E. coli from urban populations towards rural populations. Our results indicate that investments in water and sanitation prevention in urban areas could limit the spread of enteric bacterial pathogens among rural populations.
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Fuhrmeister E.R., A.P Harvey, M.L. Nadimpalli, K. Gallandat, A. Ambelu, B.F. Arnold, J.Brown, O. Cumming, A.M. Earl, G. Kang, S. Kariuki, K. Levy, C.E.P. Jimenez, J.M. Swarthout, G. Trueba, P.Tsukayama, C.J. Worby, A.J. Pickering
Evaluating the relationship between community water and sanitation access and the global burden of antibiotic resistance: an ecological study The Lancet Microbe / 2023 |
Abstract: Antibiotic resistance is a leading cause of death, with the highest burden occurring in low-resource settings. There is little evidence on the potential for water, sanitation, and hygiene (WASH) access to reduce antibiotic resistance in humans. We aimed to determine the relationship between the burden of antibiotic resistance in humans and community access to drinking water and sanitation. In this ecological study, we linked publicly available, geospatially tagged human faecal metagenomes (from the US National Center for Biotechnology Information Sequence Read Archive) with georeferenced household survey datasets that reported access to drinking water sources and sanitation facility types. We used generalised linear models with robust SEs to estimate the relationship between the abundance of antibiotic resistance genes (ARGs) in human faecal metagenomes and community-level coverage of improved drinking water and sanitation within a defined radii of faecal metagenome coordinates.
We identified 1589 metagenomes from 26 countries. The mean abundance of ARGs, in units of log10 ARG fragments per kilobase per million mapped reads classified as bacteria, was highest in Africa compared with Europe (p=0·014), North America (p=0·0032), and the Western Pacific (p=0·011), and second highest in South-East Asia compared with Europe (p=0·047) and North America (p=0·014). Increased access to improved water and sanitation was associated with lower ARG abundance (effect estimate –0·22, [95% CI –0·39 to –0·05]) and the association was stronger in urban (–0·32 [–0·63 to 0·00]) than in rural (–0·16 [–0·38 to 0·07]) areas. Although additional studies to investigate causal effects are needed, increasing access to water and sanitation could be an effective strategy to curb the proliferation of antibiotic resistance in low-income and middle-income countries. |
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Uruchima J., C. Renehan, N. Castro, W. Cevallos, K. Levy, J.N.S. Eisenberg, G.O. Lee.
A qualitative study of food choice in urban coastal Esmeraldas, Ecuador Current Developments in Nutrition / 2023 |
Abstract: Constraints on food choice increase the risk of malnutrition worldwide. Residents of secondary cities within Low- and Middle-Income Countries are a population of particular concern because they often face high rates of food insecurity and multiple nutritional burdens. Within this context, effective and equitable interventions to support healthy diets must be based on an understanding of the lived experience of individuals and their interactions with the food environment. The primary objectives of this study were to describe considerations that drive household decision-making around food choice in the city of Esmeraldas, Ecuador; to identify trade-offs between these considerations; and to understand how an evolving urban environment influences these trade-offs. Semi-structured interviews were conducted with 20 mothers of young children to explore drivers in food choice throughout the purchase, preparation, and consumption chain. Interviews were transcribed and coded to identify key themes. Personal preference, economic access (costs), convenience, and perceptions of food safety were key influencers of decision making related to food. In addition, concerns about personal safety in the urban environment limited physical access to food. This, combined with the need to travel long distances to obtain desirable foods, increased men’s participation in food purchasing. Women’s increasing engagement in the workforce also increased men’s participation in food preparation. Policies to promote healthy food behaviors in this context should focus on increasing access to health foods, such as affordable fresh produce, in convenient and physically safe locations.
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Levy K., J.V. Garn, Z.A. Cumbe, B. Muneme, C.S. Fagnant-Sperati, S. Hubbard, A. Júnior, J. L. Manuel, M. Mangamela, S. McGunegill, M.K. Miller-Petrie, J.S. Snyder, C. Victor, L. Waller, K.T. Konstantinis, T. Clasen, J. Brown, R. Nalá, M.C. Freeman.
Study design and rationale for the PAASIM project: a matched cohort study on urban water supply improvements and infant enteric pathogen infection, gut microbiome development and health in Mozambique BMJ Open / 2023 |
Abstract: Despite clear linkages between provision of clean water and improvements in child health, limited information exists about the health impacts of large water infrastructure improvements in low-income settings. Billions of dollars are spent annually to improve urban water supply, and rigorous evaluation of these improvements, especially targeting informal settlements, is critical to guide policy and investment strategies. Objective measures of infection and exposure to pathogens, and measures of gut function, are needed to understand the effectiveness and impact of water supply improvements. In the PAASIM study, we examine the impact of water system improvements on acute and chronic health outcomes in children in a low-income urban area of Beira, Mozambique, comprising 62 sub-neighbourhoods and ~26 300 households. This prospective matched cohort study follows 548 mother–child dyads from late pregnancy through 12 months of age. Primary outcomes include measures of enteric pathogen infections, gut microbiome composition and source drinking water microbiological quality, measured at the child’s 12-month visit. Additional outcomes include diarrhoea prevalence, child growth, previous enteric pathogen exposure, child mortality and various measures of water access and quality. Our analyses will compare (1) subjects living in sub-neighbourhoods with the improved water to those living in sub-neighbourhoods without these improvements; and (2) subjects with household water connections on their premises to those without such a connection. This study will provide critical information to understand how to optimise investments for improving child health, filling the information gap about the impact of piped water provision to low-income urban households, using novel gastrointestinal disease outcomes.
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Ballard A.M., N. Laramee, R. Haardörfer, M.C. Freeman, K. Levy, B.A. Caruso.
Measurement in the study of human exposure to animal feces: A systematic review and audit International Journal of Hygiene and Environmental Health / 2023 |
Abstract: Human exposure to animal feces is increasingly recognized as an important transmission route of enteric pathogens. Yet, there are no consistent or standardized approaches to measurement of this exposure, limiting assessment of the human health effects and scope of the issue. To inform and improve approaches to the measurement of human exposure to animal feces, we audited existing measurement in low- and middle-income countries. We systematically searched peer-reviewed and gray literature databases for studies with quantitative measures of human exposure to animal feces and we classified measures in two ways. First, using a novel conceptual model, we categorized measures into three ‘Exposure Components’ identified a priori (i.e., Animal, Environmental, Human Behavioral); one additional Component (Evidence of Exposure) inductively emerged. Second, using the exposure science conceptual framework, we determined where measures fell along the source-to-outcome continuum. We identified 1,428 measures across 184 included studies. Although studies overwhelmingly included more than one single-item measure, the majority only captured one Exposure Component. For example, many studies used several single-item measures to capture the same attribute for different animals, all of which were classified as the same Component. Most measures captured information about the source (e.g. animal presence) and contaminant (e.g. animal-sourced pathogens), which are most distal from exposure on the source-to-outcome continuum. We found that measurement of human exposure to animal feces is diverse and largely distal from exposure. To facilitate better assessment of the human health effects of exposure and scope of the issue, rigorous and consistent measures are needed. We recommend a list of key factors from the Animal, Environmental, and Human Behavioral Exposure Components to measure. We also propose using the exposure science conceptual framework to identify proximal measurement approaches.
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Levy K.
Invited Perspective: Environmental Health Interventions Are Only as Good as Their Adoption Evnironmental Health Perspectives / 2023 |
This article is a companion to Adoption of Point-of-Use Chlorination for Household Drinking Water Treatment: A Systematic Review, and discusses the importance of understanding consumer's needs and interests in relation to the use of household water treatment technology.
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Amin M.B, P.K. Talukdar, M. Asaduzzaman, S. Roy, B.M. Flatgard, M.R. Islam, S.R. Saha, Z.H. Mahmud, T. Navab-Daneshmand, M.L. Kile, K. Levy, T.R. Julian, M.A. Islam.
Effects of chronic exposure to arsenic on the fecal carriage of antibiotic-resistant Escherichia coli among people in rural Bangladesh PLOS Pathogens / 2022 |
Abstract: Antibiotic resistance is a leading cause of hospitalization and death worldwide. Heavy metals such as arsenic have been shown to drive co-selection of antibiotic resistance, suggesting arsenic-contaminated drinking water is a risk factor for antibiotic resistance carriage. This study aimed to determine the prevalence and abundance of antibiotic-resistant Escherichia coli (AR-Ec) among people and drinking water in high (Hajiganj, >100 μg/L) and low arsenic-contaminated (Matlab, <20 μg/L) areas in Bangladesh. Drinking water and stool from mothers and their children (<1 year) were collected from 50 households per area. AR-Ec was detected via selective culture plating and isolates were tested for antibiotic resistance, arsenic resistance, and diarrheagenic genes by PCR. Whole-genome sequencing (WGS) analysis was done for 30 E. coli isolates from 10 households. Prevalence of AR-Ec was significantly higher in water in Hajiganj (48%) compared to water in Matlab (22%, p <0.05) and among children in Hajiganj (94%) compared to children in Matlab (76%, p <0.05), but not among mothers. A significantly higher proportion of E. coli isolates from Hajiganj were multidrug-resistant (83%) compared to isolates from Matlab (71%, p <0.05). Co-resistance to arsenic and multiple antibiotics (MAR index >0.2) was observed in a higher proportion of water (78%) and child stool (100%) isolates in Hajiganj than in water (57%) and children (89%) in Matlab (p <0.05). The odds of arsenic-resistant bacteria being resistant to third-generation cephalosporin antibiotics were higher compared to arsenic-sensitive bacteria (odds ratios, OR 1.2-7.0, p <0.01). WGS-based phylogenetic analysis of E. coli isolates did not reveal any clustering based on arsenic exposure and no significant difference in resistome was found among the isolates between the two areas. The positive association detected between arsenic exposure and antibiotic resistance carriage among children in arsenic-affected areas in Bangladesh is an important public health concern that warrants redoubling efforts to reduce arsenic exposure.
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Nguyen K.H., A. Smith, A. Roundtree, D.J. Feistel, A.E. Kirby, K. Levy, M.C. Mattioli
Fecal indicators and antibiotic resistance genes exhibit diurnal trends in the Chattahoochee River: Implications for water quality monitoring Frontiers in Microbiology / 2022 |
Abstract: Water bodies that serve as sources of drinking or recreational water are routinely monitored for fecal indicator bacteria (FIB) by state and local agencies. Exceedances of monitoring thresholds set by those agencies signal likely elevated human health risk from exposure, but FIB give little information about the potential source of contamination. To improve our understanding of how within-day variation could impact monitoring data interpretation, we conducted a study at two sites along the Chattahoochee River that varied in their recreational usage and adjacent land-use (natural versus urban), collecting samples every 30 min over one 24-h period. We assayed for three types of microbial indicators: FIB (total coliforms and Escherichia coli); human fecal-associated microbial source tracking (MST) markers (crAssphage and HF183/BacR287); and a suite of clinically relevant antibiotic resistance genes (ARGs; blaCTX-M, blaCMY, MCR, KPC, VIM, NDM) and a gene associated with antibiotic resistance (intl1). Mean levels of FIB and clinically relevant ARGs (blaCMY and KPC) were similar across sites, while MST markers and intI1 occurred at higher mean levels at the natural site. The human-associated MST markers positively correlated with antibiotic resistant-associated genes at both sites, but no consistent associations were detected between culturable FIB and any molecular markers. For all microbial indicators, generalized additive mixed models were used to examine diurnal variability and whether this variability was associated with environmental factors (water temperature, turbidity, pH, and sunlight). We found that FIB peaked during morning and early afternoon hours and were not associated with environmental factors. With the exception of HF183/BacR287 at the urban site, molecular MST markers and intI1 exhibited diurnal variability, and water temperature, pH, and turbidity were significantly associated with this variability. For blaCMY and KPC, diurnal variability was present but was not correlated with environmental factors. These results suggest that differences in land use (natural or urban) both adjacent and upstream may impact overall levels of microbial contamination. Monitoring agencies should consider matching sample collection times with peak levels of target microbial indicators, which would be in the morning or early afternoon for the fecal associated indicators. Measuring multiple microbial indicators can lead to clearer interpretations of human health risk associated with exposure to contaminated water.
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Delahoy, M.J., S. Hubbard, M. Mattioli, C. Culquichicón, J. Knee, J. Brown, L. Cabrera, D.B. Barr, P.B. Ryan, A.G. Lescano, R.H. Gilman, K. Levy
High Prevalence of Chemical and Microbiological Drinking Water Contaminants in Households with Infants Enrolled in a Birth Cohort-Piura, Peru, 2016 American Journal of Tropical Medicine and Hygiene / 2022 |
Abstract: Chemical and microbiological drinking water contaminants pose risks to child health but are not often evaluated concurrently. At two consecutive visits to 96 households in Piura, Peru, we collected drinking water samples, administered health and exposure questionnaires, and collected infant stool samples. Standard methods were used to quantify heavy metals/metalloids, pesticides, and Escherichia coli concentrations in water samples. Stool samples were assayed for bacterial, viral, and parasitic enteropathogens. The primary drinking water source was indoor piped water for 70 of 96 households (73%); 36 households (38%) stored drinking water from the primary source in containers in the home. We found high prevalence of chemical and microbiological contaminants in household drinking water samples: arsenic was detected in 50% of 96 samples, ≥ 1 pesticide was detected in 65% of 92 samples, and E. coli was detected in 37% of 319 samples. Drinking water samples that had been stored in containers had higher odds of E. coli detection (adjusted odds ratio [aOR]: 4.50; 95% CI: 2.04-9.95) and pesticide detection (OR: 6.55; 95% CI: 2.05-21.0) compared with samples collected directly from a tap. Most infants (68%) had ≥ 1 enteropathogen detected in their stool. Higher odds of enteropathogen infection at the second visit were observed among infants from households where pesticides were detected in drinking water at the first visit (aOR: 2.93; 95% CI: 1.13-7.61). Results show concurrent risks of exposure to microbiological and chemical contaminants in drinking water in a low-income setting, despite high access to piped drinking water.
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Miller, A.G., S. Ebelt, K. Levy
Combined Sewer Overflows and Gastrointestinal Illness in Atlanta, 2002–2013: Evaluating the Impact of Infrastructure Improvements Environmental Health Perspectives / 2022 |
Abstract: Combined sewer overflows (CSOs) discharge untreated sewage into surface and recreational water, often following heavy precipitation. Given projected increases in frequency and intensity of precipitation due to climate change, it is important to understand the health impacts of CSOs and mediating effects of sewerage systems.
In this study we estimate associations of CSO events and emergency department (ED) visits for gastrointestinal (GI) illness among City of Atlanta, Georgia, residents and explore how these associations vary with sewerage improvements. We estimate associations using Poisson generalized linear models, controlling for time trends. We categorized CSOs by overflow volume and assessed effects of CSO events prior to ED visits with 1-, 2- and 3-wk lags. Similarly, we evaluated effects of weekly cumulative precipitation greater than the 90th percentile at the same lags. We also evaluated effect modification by ZIP Code Tabulation Area (ZCTA)-level poverty and infrastructure improvement period using interaction terms. Occurrence of a large volume CSO in the previous week was associated with a 9% increase in daily ED visits for GI illness. We identified significant interaction by ZCTA-level poverty, with stronger CSO–GI illness associations in low than high poverty areas. Among areas with low poverty, we observed associations at 1-wk and longer lags, following both large and lower volume CSO events. We did not observe significant interaction by infrastructure improvement period for CSO– nor precipitation–GI illness associations; however, the number of CSO events decreased from 2.31 per week before improvements to 0.49 after improvements. Our findings suggest that CSOs contribute to acute GI illness burden in Atlanta and that the magnitude of this risk may be higher among populations living in areas of low poverty. We did not find a protective effect of sewerage system improvements. Nonetheless, observed reductions in CSO frequency may lower the absolute burden of GI illness attributable to these events. |
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Sosa-Moreno A., G.O. Lee, A. Van Engen, K. Sun, J. Uruchima, L.H Kwong, E. Ludwig-Borycz, B.A. Caruso, W. Cevallos, K. Levy, J.N.S. Eisenberg
Characterizing Behaviors Associated with Enteric Pathogen Exposure among Infants in Rural Ecuador through Structured Observations American Journal of Tropical Medicine and Hygiene / 2022 |
Abstract: The relative importance of environmental pathways that results in enteropathogen transmission may vary by context. However, measurement of contact events between individuals and the environment remains a challenge, especially for infants and young children who may use their mouth and hands to explore their environment. Using a mixed-method approach, we combined 1) semistructured observations to characterize key behaviors associated with enteric pathogen exposure and 2) structured observations using Livetrak, a customized software application, to quantify the frequency and duration of contacts events among infants in rural Ecuador. After developing and iteratively piloting the structured observation instrument, we loaded the final list of prompts onto a LiveTrak pallet to assess environmental exposures of 6-month infants (N = 19) enrolled in a prospective cohort study of diarrheal disease. Here we provide a detailed account of the lessons learned. For example, in our field site, 1) most mothers reported washing their hands after diaper changes (14/18, 77.8%); however only a third (4/11, 36.4%) were observed washing their hands; 2) the observers noted that animal ownership differed from observed animal exposure because animals owned by neighboring households were reported during the observation; and 3) using Livetrak, we found that infants frequently mouthed their hands (median = 1.9 episodes/hour, median duration: 1.6 min) and mouthed surroundings objects (1.8 episodes/hour, 1.9 min). Structured observations that track events in real time, can complement environmental sampling, quantitative survey data and qualitative interviews. Customizing these observations enabled us to quantify enteric exposures most relevant to our rural Ecuadorian context.
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Victor C., D.V. Ocasio, Z.A. Cumbe, J.V. Garn, S. Hubbard, M. Mangamela, S. McGunegill, R. Nalá, J.S. Snyder, K. Levy, M.C. Freeman
Spatial Heterogeneity of Neighborhood-Level Water and Sanitation Access in Informal Urban Settlements: A Cross-Sectional Case Study in Beira, Mozambique PLOS WATER / 2022 |
Abstract: Rapid urbanization, resulting in population growth within informal settlements, has worsened exclusion and inequality in access to water and sanitation (WASH) services in the poorest and most marginalized communities. In this study, we describe the heterogeneity in water service satisfaction and WASH access in low-income, peri-urban neighborhoods of Beira, Mozambique, and examine whether this heterogeneity can be explained by distance to water distribution mains. Using spatial statistics and regression analyses, we identified statistical spatial heterogeneity in household WASH access, as well as consumer-reported satisfaction with water services (services, pressure, quality, and sufficient quantity). We found that as distance from the water main increased, both access to an improved water source at the household and satisfaction with water pressure decreased, controlling for household density and socioeconomic status. The odds of a household having access to a water source at the household or on the compound decreased with every 100-meter increase in distance from a water main pipe (odds ratio [OR] 0.87, 95% confidence interval [CI]: 0.82, 0.92). Satisfaction with water services also decreased with every 100-meter increase in distance from a water main pipe (OR: 0.80; 95% CI: 0.69, 0.94). Findings from this study highlight the unequal household access to water and sanitation in urban informal settlements, even within low-income neighborhoods. Describing this heterogeneity of access to water services, sanitation, and satisfaction – and the factors influencing them - can inform stakeholders and guide the development of infrastructural solutions to reduce water access inequities within urban settings.
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Cromar K.R., S.C. Anenberg, J.R. Balmes, A.A. Fawcett, M. Ghazipura, J.M. Gohlke, M. Hashizume, P. Howard, E. Lavigne, K. Levy, J. Madrigano, J.A. Martinich, E.A. Mordecai, M.B. Rice, S. Saha, N.C. Scovronick, F. Sekercioglu, E.R. Svendsen, B.F. Zaitchik, G. Ewart.
Global Health Impacts for Economic Models of Climate Change: A Systematic Review and Meta-Analysis Annals of the American Thoracic Society / 2022 |
Abstract: Avoiding excess health damages attributable to climate change is a primary motivator for policy interventions to reduce greenhouse gas emissions. However, the health benefits of climate mitigation, as included in the policy assessment process, have been estimated without much input from health experts. In accordance with recommendations from the National Academies in a 2017 report on approaches to update the social cost of greenhouse gases (SC-GHG), an expert panel of 26 health researchers and climate economists gathered for a virtual technical workshop in May 2021 to conduct a systematic review and meta-analysis and recommend improvements to the estimation of health impacts in economic-climate models. Regionally-resolved effect estimates of unit increases in temperature on net all-cause mortality risk were generated through random-effects pooling of studies identified through a systematic review. Effect estimates, and associated uncertainties, varied by global region, but net increases in mortality risk associated with increased average annual temperatures (ranging from 0.1-1.1% per 1 degree C) was estimated for all global regions. Key recommendations for the development and utilization of health damage modules were provided by the expert panel, and include: not relying on individual methodologies in estimating health damages; incorporating a broader range of cause-specific mortality impacts; improving the climate parameters available in economic models; accounting for socio-economic trajectories and adaptation factors when estimating health damages; and carefully considering how air pollution impacts should be incorporated in economic-climate models. This work provides an example for how subject-matter experts can work alongside climate economists in making continued improvements to SC-GHG estimates.
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Lee G.O., J.N.S. Eisenberg, J. Uruchima, G. Vasco, S.M. Smith, A. Van Engen, C. Victor, E. Reynolds, R. MacKay, K.J. Jesser, N. Castro, M. Calvopiña, K.T. Konstantinidis, W. Cevallos, G. Trueba, K. Levy
Gut microbiome, enteric infections and child growth across a rural–urban gradient: protocol for the ECoMiD prospective cohort study BMJ Open / 2021 |
Abstract: The functional consequences of the bacterial gut microbiome for child health are not well understood. Characteristics of the early child gut microbiome may influence the course of enteric infections, and enteric infections may change the composition of the gut microbiome, all of which may have long-term implications for child growth and development. We are conducting a community-based birth cohort study to examine interactions between gut microbiome conditions and enteric infections, and how environmental conditions affect the development of the gut microbiome. We will follow 360 newborns from 3 sites along a rural–urban gradient in northern coastal Ecuador, characterising enteric infections and gut microbial communities in the children every 3 to 6 months over their first 2 years of life. We will use longitudinal regression models to assess the correlation between environmental conditions and gut microbiome diversity and presence of specific taxa, controlling for factors that are known to be associated with the gut microbiome, such as diet. From 6 to 12 months of age, we will collect weekly stool samples to compare microbiome conditions in diarrhoea stools versus stools from healthy children prior to, during and after acute enteric infections, using principal-coordinate analysis and other multivariate statistical methods.
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Capone D., D. Berendes, O. Cumming, D. Holcomb, J. Knee, K. T. Konstantinidis, K. Levy, R. Nalá, B. B. Risk, J. Stewart, J. Brown
Impact of an Urban Sanitation Intervention on Enteric Pathogen Detection in Soils Environmental Science and Technology / 2021 |
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 (preintervention) and after 24 months (postintervention) as part of the Maputo Sanitation Trial. We tested soils for the presence of nucleic acids associated with 18 enteric pathogens using a multiplex reverse transcription qPCR platform. We detected at least one pathogen-associated gene target in 91% (163/179) of soils and a median of 3 (IQR = 1, 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 detecting ≥1 pathogen gene by 15% (adjusted prevalence ratio, aPR = 0.85; 95% CI: 0.70, 1.0) and the total number of pathogens 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.
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Soto-Girón, M.J., A. Peña-Gonzalez, J. K. Hatt, L. Montero, M. Páez, E. Ortega, S. Smith, W. Cevallos, G. Trueba, K.T. Konstantinidis, K. Levy
Gut Microbiome Changes with Acute Diarrheal Disease in Urban Versus Rural Settings in Northern Ecuador American Journal of Tropical Medicine and Hygiene / 2021 |
Abstract: Previous studies have reported lower fecal bacterial diversity in urban populations compared with those living in rural settings. However, most of these studies compare geographically distant populations from different countries and even continents. The extent of differences in the gut microbiome in adjacent rural versus urban populations, and the role of such differences, if any, during enteric infections remain poorly understood. To provide new insights into these issues, we sampled the gut microbiome of young children with and without acute diarrheal disease (ADD) living in rural and urban areas in northern Ecuador. Shotgun metagenomic analyses of non-ADD samples revealed small but significant differences in the abundance of microbial taxa, including a greater abundance of Prevotella and a lower abundance of Bacteroides and Alistipes in rural populations. Greater and more significant shifts in taxon abundance, metabolic pathway abundance, and diversity were observed between ADD and non-ADD status when comparing urban to rural sites (Welch's t-test, P < 0.05). Collectively our data show substantial functional, diversity, and taxonomic shifts in the gut microbiome of urban populations with, ADD supporting the idea that the microbiome of rural populations may be more resilient to ADD episodes.
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Meziti, A., L.M. Rodriguez-R, J.K. Hatt, A. Peña-Gonzalez, K. Levy, K.T. Konstantinidis
The Reliability of Metagenome-Assembled Genomes (MAGs) in Representing Natural Populations: Insights from Comparing MAGs against Isolate Genomes Derived from the Same Fecal Sample Applied and Environmental Microbiology / 2021 |
Abstract: The recovery of metagenome-assembled genomes (MAGs) from metagenomic data has recently become a common task for microbial studies. The strengths and limitations of the underlying bioinformatics algorithms are well appreciated by now based on performance tests with mock data sets of known composition. However, these mock data sets do not capture the complexity and diversity often observed within natural populations, since their construction typically relies on only a single genome of a given organism. Further, it remains unclear if MAGs can recover population-variable genes (those shared by >10% but <90% of the members of the population) as efficiently as core genes (those shared by >90% of the members). To address these issues, we compared the gene variabilities of pathogenic Escherichia coli isolates from eight diarrheal samples, for which the isolate was the causative agent, against their corresponding MAGs recovered from the companion metagenomic data set. Our analysis revealed that MAGs with completeness estimates near 95% captured only 77% of the population core genes and 50% of the variable genes, on average. Further, about 5% of the genes of these MAGs were conservatively identified as missing in the isolate and were of different (non-Enterobacteriaceae) taxonomic origin, suggesting errors at the genome-binning step, even though contamination estimates based on commonly used pipelines were only 1.5%. Therefore, the quality of MAGs may often be worse than estimated, and we offer examples of how to recognize and improve such MAGs to sufficient quality by (for instance) employing only contigs longer than 1,000 bp for binning. IMPORTANCE Metagenome assembly and the recovery of metagenome-assembled genomes (MAGs) have recently become common tasks for microbiome studies across environmental and clinical settings. However, the extent to which MAGs can capture the genes of the population they represent remains speculative. Current approaches to evaluating MAG quality are limited to the recovery and copy number of universal housekeeping genes, which represent a small fraction of the total genome, leaving the majority of the genome essentially inaccessible. If MAG quality in reality is lower than these approaches would estimate, this could have dramatic consequences for all downstream analyses and interpretations. In this study, we evaluated this issue using an approach that employed comparisons of the gene contents of MAGs to the gene contents of isolate genomes derived from the same sample. Further, our samples originated from a diarrhea case-control study, and thus, our results are relevant for recovering the virulence factors of pathogens from metagenomic data sets.
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Delahoy M.J., C. Cárcamo, A. Huerta, W. Lavado, Y. Escajadillo, L. Ordoñez, V. Vasquez, B. Lopman, T. Clasen, G. F. Gonzales, K. Steenland, K. Levy
Meteorological factors and childhood diarrhea in Peru, 2005–2015: a time series analysis of historic associations, with implications for climate change Environmental Health / 2021 |
Background: Global temperatures are projected to rise by ≥2 °C by the end of the century, with expected impacts on infectious disease incidence. Establishing the historic relationship between temperature and childhood diarrhea is important to inform future vulnerability under projected climate change scenarios. Methods: We compiled a national dataset from Peruvian government data sources, including weekly diarrhea surveillance records, annual administered doses of rotavirus vaccination, annual piped water access estimates, and daily temperature estimates. We used generalized estimating equations to quantify the association between ambient temperature and childhood (< 5 years) weekly reported clinic visits for diarrhea from 2005 to 2015 in 194 of 195 Peruvian provinces. We estimated the combined effect of the mean daily high temperature lagged 1, 2, and 3 weeks, in the eras before (2005–2009) and after (2010–2015) widespread rotavirus vaccination in Peru and examined the influence of varying levels of piped water access. Results: Nationally, an increase of 1 °C in the temperature across the three prior weeks was associated with a 3.8% higher rate of childhood clinic visits for diarrhea [incidence rate ratio (IRR): 1.04, 95% confidence interval (CI): 1.03–1.04]. Controlling for temperature, there was a significantly higher incidence rate of childhood diarrhea clinic visits during moderate/strong El Niño events (IRR: 1.03, 95% CI: 1.01–1.04) and during the dry season (IRR: 1.01, 95% CI: 1.00–1.03). Nationally, there was no evidence that the association between temperature and the childhood diarrhea rate changed between the pre- and post-rotavirus vaccine eras, or that higher levels of access to piped water mitigated the effects of temperature on the childhood diarrhea rate. Conclusions: Higher temperatures and intensifying El Niño events that may result from climate change could increase clinic visits for childhood diarrhea in Peru. Findings underscore the importance of considering climate in assessments of childhood diarrhea in Peru and globally, and can inform regional vulnerability assessments and mitigation planning efforts.
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Jesser, K., and K. Levy
Updates on Defining and Detecting Diarrheagenic Escherichia coli Pathotypes Current Opinion in Infectious Diseases / 2020 |
Purpose of review: Several types of Escherichia coli cause acute diarrhea in humans and are responsible for a large burden of disease globally. The purpose of this review is to summarize diarrheagenic Escherichia coli (DEC) pathotype definitions and discuss existing and emerging molecular, genomic, and gut microbiome methods to detect, define, and study DEC pathotypes. Recent findings: DEC pathotypes are currently diagnosed by molecular detection of unique virulence genes. However, some pathotypes have defied coherent molecular definitions because of imperfect gene targets, and pathotype categories are complicated by hybrid strains and isolation of pathotypes from asymptomatic individuals. Recent progress toward more efficient, sensitive, and multiplex DEC pathotype detection has been made using emerging PCR-based technologies. Genomics and gut microbiome detection methods continue to advance rapidly and are contributing to a better understanding of DEC pathotype diversity and functional potential. Summary: DEC pathotype categorizations and detection methods are useful but imperfect. The implementation of molecular and sequence-based methods and well designed epidemiological studies will continue to advance understanding of DEC pathotypes. Additional emphasis is needed on sequencing DEC genomes from regions of the world where they cause the most disease and from the pathotypes that cause the greatest burden of disease globally.
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Kraay A.N.M., O. Man, M.C. Levy, K. Levy, E. Ionides, and J.N.S. Eisenberg
Understanding the Impact of Rainfall on Diarrhea: Testing the Concentration-Dilution Hypothesis Using a Systematic Review and Meta-Analysis Environmental Health Perspectives / 2020 |
Background: Projected increases in extreme weather may change relationships between rain-related climate exposures and diarrheal disease. Whether rainfall increases or decreases diarrhea rates is unclear based on prior literature. The concentration-dilution hypothesis suggests that these conflicting results are explained by the background level of rain: Rainfall following dry periods can flush pathogens into surface water, increasing diarrhea incidence, whereas rainfall following wet periods can dilute pathogen concentrations in surface water, thereby decreasing diarrhea incidence. Objectives: In this analysis, we explored the extent to which the concentration-dilution hypothesis is supported by published literature. Methods: To this end, we conducted a systematic search for articles assessing the relationship between rain, extreme rain, flood, drought, and season (rainy vs. dry) and diarrheal illness. Results: A total of 111 articles met our inclusion criteria. Overall, the literature largely supports the concentration-dilution hypothesis. In particular, extreme rain was associated with increased diarrhea when it followed a dry period [incidence rate ratio (IRR)=1.26(IRR)=1.26; 95% confidence interval (CI): 1.05, 1.51], with a tendency toward an inverse association for extreme rain following wet periods, albeit nonsignificant, with one of four relevant studies showing a significant inverse association (IRR=0.911IRR=0.911; 95% CI: 0.771, 1.08). Incidences of bacterial and parasitic diarrhea were more common during rainy seasons, providing pathogen-specific support for a concentration mechanism, but rotavirus diarrhea showed the opposite association. Information on timing of cases within the rainy season (e.g., early vs. late) was lacking, limiting further analysis. We did not find a linear association between nonextreme rain exposures and diarrheal disease, but several studies found a nonlinear association with low and high rain both being associated with diarrhea. Discussion: Our meta-analysis suggests that the effect of rainfall depends on the antecedent conditions. Future studies should use standard, clearly defined exposure variables to strengthen understanding of the relationship between rainfall and diarrheal illness.
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Steele M.K., M.E. Wikswo, A.J. Hall, K. Koelle, A. Handel, K. Levy, L.A. Waller, B.A. Lopman
Characterizing Norovirus Transmission from Outbreak Data, United States Emerging Infectious Diseases / 2020 |
Norovirus is the leading cause of acute gastroenteritis outbreaks in the United States. We estimated the basic (R0) and effective (Re) reproduction numbers for 7,094 norovirus outbreaks reported to the National Outbreak Reporting System (NORS) during 2009–2017 and used regression models to assess whether transmission varied by outbreak setting. The median R0 was 2.75 (interquartile range [IQR] 2.38–3.65), and median Re was 1.29 (IQR 1.12–1.74). Long-term care and assisted living facilities had an R0 of 3.35 (95% CI 3.26–3.45), but R0 did not differ substantially for outbreaks in other settings, except for outbreaks in schools, colleges, and universities, which had an R0 of 2.92 (95% CI 2.82–3.03). Seasonally, R0 was lowest (3.11 [95% CI 2.97–3.25]) in summer and peaked in fall and winter. Overall, we saw little variability in transmission across different outbreaks settings in the United States.
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Delahoy, M.J., C. Cárcamo, L. Ordoñez, V. Vasquez, B. Lopman, T. Clasen, G.F. Gonzales, K. Steenland, K. Levy
Impact of Rotavirus Vaccination Varies by Level of Access to Piped Water and Sewerage: An Analysis of Childhood Clinic Visits for Diarrhea in Peru, 2005-2015 Pediatric Infectious Disease Journal / 2020 |
Background: We conducted a national impact evaluation of routine rotavirus vaccination on childhood diarrhea in Peru, accounting for potential modifying factors. Methods: We utilized a dataset compiled from Peruvian governmental sources to fit negative binomial models investigating the impact of rotavirus vaccination, piped water access, sewerage access and poverty on the rate of diarrhea clinic visits in children under 5 years old in 194 Peruvian provinces. We considered the interaction between these factors to assess whether water access, sanitation access, or poverty modified the association between ongoing rotavirus vaccination and childhood diarrhea clinic visits. We compared the "pre-vaccine" (2005-2009) and "post-vaccine" (2010-2015) eras. Results: The rate of childhood diarrhea clinic visits was 7% [95% confidence interval (CI): 3%-10%] lower in the post-vaccine era compared with the pre-vaccine era, controlling for long-term trend and El Niño seasons. No impact of rotavirus vaccination was identified in provinces with the lowest access to piped water (when <40% of province households had piped water) or in the lowest category of sewerage (when <17% of province households had a sewerage connection). Accounting for long-term and El Niño trends, the rate of childhood diarrhea clinic visits was lower in the post-vaccine era by 7% (95% CI: 2%-12%), 13% (95% CI: 7%-19%) and 15% (95% CI: 10%-20%) in the second, third and fourth (highest) quartiles of piped water access, respectively (compared with the pre-vaccine era); results for sewerage access were similar. Conclusion: Improved water/sanitation may operate synergistically with rotavirus vaccination to reduce childhood clinic visits for diarrhea in Peru.
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Goddard, F., R. Ban, D.B. Barr, J. Brown, J. Cannon, J.M. Colford, J.N.S. Eisenberg, A. Ercumen, H. Petach, M.C. Freeman, K. Levy, S.P. Luby, C. Moe, A.J. Pickering, J.A. Sarnat, J.R. Stewart, E.A. Thomas, M. Taniuchi, T.F. Clasen
Measuring environmental exposure to enteric pathogens in low-income settings: review and recommendations of an interdisciplinary working group Environmental Science & Technology / 2020 |
Infections with enteric pathogens impose a heavy disease burden, especially among young children in low-income countries. Recent findings from randomized controlled trials of water, sanitation and hygiene interventions have raised questions about current methods for assessing environmental exposure to enteric pathogens. Approaches for estimating sources and doses of exposure suffer from a number of shortcomings, including reliance on imperfect indicators of fecal contamination instead of actual pathogens and estimating exposure indirectly from imprecise measurements of pathogens in the environment and human interaction therewith. These shortcomings limit the potential for effective surveillance of exposures, identification of important sources and modes of transmission, and evaluation of the effectiveness of interventions. In this review, we summarize current and emerging approaches used to characterize enteric pathogen hazards in different environmental media as well as human interaction with those media (external measures of exposure), and review methods that measure human infection with enteric pathogens as a proxy for past exposure (internal measures of exposure). We draw from lessons learned in other areas of environmental health to highlight how external and internal measures of exposure can be used to more comprehensively assess exposure. We conclude by recommending strategies for advancing enteric pathogen exposure assessments.
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Deshpande, A., H.H. Chang, K. Levy
Heavy Rainfall Events and Diarrheal Diseases: The Role of Urban–Rural Geography American Journal of Tropical Medicine and Hygiene / 2020 |
Diarrheal diseases remain a significant contributor to the global burden of disease. Climate change may increase their incidence by altering the epidemiology of waterborne pathogens through changes in rainfall patterns. To assess potential impacts of future changes in rainfall patterns, we analyzed 33,927 cases of diarrhea across all Ministry of Health clinical facilities in Esmeraldas Province, Ecuador, for a 24-month period from 2013 to 2014, using mixed-effects Poisson regression. We assessed the association between the incidence of diarrheal diseases and heavy rainfall events (HREs) and antecedent rainfall conditions. In rural areas, we found no significant associations between HREs and incidence. In urban areas, dry antecedent conditions were associated with higher incidence than wet conditions. In addition, HREs with dry antecedent conditions were associated with elevated incidence by up to 1.35 (incidence rate ratio, 95% CI: 1.14–1.60) times compared with similar conditions without HREs. These patterns may be driven by accumulation of fecal contamination during dry periods, followed by a flushing effect during HREs. This phenomenon is more important in dense urban environments with more impervious surfaces. These findings suggest that projected increases in rainfall variability and HREs may increase diarrhea burden in urban regions, which are rapidly expanding globally.
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Chard A.N., K. Levy, K.K. Baker, K. Tsai, H.H. Chang, V. Thongpaseuth, J.R. Sistrunk, M.C. Freeman
Environmental and spatial determinants of enteric pathogen infection in rural Lao People’s Democratic Republic: A cross-sectional study PLOS Neglected Tropical Diseases / 2020 |
Though the health risks associated with poor access to water, sanitation, and hygiene (WASH) are well established, recent large-scale WASH trials have found limited impact on enteric disease. The aims of this study were to: 1. estimate the prevalence of enteropathogens among children <5, school-aged children, and adults; 2. model associations between WASH transmission pathways and enteropathogen infections; and 3. quantify clustering of enteropathogen infections at the household- and village-level. We conducted a cross-sectional survey in 50 villages in Saravane Province, Lao People’s Democratic Republic. From 297 households, we collected 891 fecal samples from one child <5, one school-aged child, and one adult living in the same household, and collected survey and observational data on household demographics, WASH access, and animal ownership. Fecal samples were analyzed for 25 enteropathogens using a qRT-PCR assay. We observed near universal infection with at least one enteropathogen (98.3%). Few household or village-level WASH covariates were statistically associated with enteropathogen infection. Concordant household infection was higher than expected under the independence assumption for 14 of the 21 pathogens for which we had sufficient data, indicating strong household correlation for many infections. Median odds ratios (MORs), a measure of cluster-level (e.g. village and household) influence on an individual’s odds of infection, were elevated at the village level, particularly for viruses (MOR: 3.89; 95% confidence interval [CI]: 2.64, 6.69), protozoa (MOR: 2.07; 95% CI: 1.59, 3.10), and soil-transmitted helminths (MOR: 2.46; 95% CI: 1.89, 3.56), indicating strong village-level differences in individuals' odds of enteric infections. WASH access, as hypothesized, is associated with fewer enteroinfections, but WASH access as currently defined does not reveal a measurably protective association with infection for many etiologies. Household- and community-level factors beyond WASH access, such as intra-household pathogen transmission, exposure to animal feces, and contextual factors in the public domain may be important risk factors for enteric infections.
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Lee, G.O., H.J. Whitney, A. Blum, N. Lybik, W. Cevallos, G. Trueba, K. Levy, J.N.S. Eisenberg
Household coping strategies associated with unreliable water supplies and diarrhea in Ecuador, an upper-middle-income country Water Research / 2020 |
The Sustainable Development Goals recognize that the availability and quality of improved water sources affect how households use and benefit from these sources. Although unreliability in piped water supplies in low- and middle-income countries (LMICs) has been described, few studies have assessed household coping strategies in response to unreliable water supplies and associated health outcomes. We characterized unreliability in the piped water supply of the town of Borbón, Ecuador over the twelve years following a major upgrade, as well as household coping strategies and associations with diarrhea. We examined trends in primary and secondary drinking water sources, water storage, and water treatment using longitudinal data collected from 2005 to 2012. In 2017, a follow-up survey was administered (N = 202) and a subset of 84 household water samples were tested for chlorine residual levels and microbial contamination. From 2005 to 2017, access to a household water connection increased from 19.4% to 90.3%. However, reliability decreased over time, as in the latter half of 2009, households had access to piped water 79% of the time, compared to 63% by 2017. Piped water samples were highly contaminated with total coliforms (100% of samples) and Escherichia coli (89% of samples). From 2005 to 2017, households less likely to report drinking water treatment (50.6%–5.0%). And from 2009 to 2017, bottled water was increasingly consumed as the primary drinking water source (18.8%–62.4%). From 2005 to 2012, having a household connection was not statistically significantly associated with diarrhea case status (OR: 0.86 95%CI: 0.53, 1.39). Neither household water treatment nor bottled water consumption were negatively associated with diarrhea. Increased water storage was associated with diarrhea (OR: 1.33 per 10L of water stored, 95%CI: 1.05, 1.69). Household water treatment, and consumption of purchased bottled water, two coping strategies that households may have undertaken in response to an unreliable water supply, were not associated with a reduced likelihood of diarrhea. These data suggest a need to understand how impoverished rural households in LMICs respond to unreliable water supplies, and to develop heath messaging appropriate for this context.
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Salinas-Castro R.V., W. Cevallos, K. Levy
Afrodescendientes e indígenas vulnerables al cambio climático: desacuerdos frente a medidas preventivas estatales ecuatorianas Íconos / 2019 |
El presente artículo analiza la situación de la provincia de Esmeraldas, ubicada al noroeste del Ecuador, y poblada por afrodescendientes e indígenas chachi. Esta provincia es una de las más afectadas por la alta frecuencia e intensidad de inundaciones, las cuales ocasionan innumerables pérdidas materiales, económicas y humanas. El objetivo de este estudio es reconocer la situación de las mencionadas poblaciones, identificar sus prácticas y representaciones, analizar cómo se generan condiciones de vulnerabilidad frente a los riesgos ocasionados por las inundaciones, así como identificar los direccionamientos bajo los cuales las instituciones gubernamentales han desarrollado políticas de prevención y adaptación ante este tipo de desastres. El estudio utiliza una metodología cualitativa de tipo exploratoria y descriptiva para dar cuenta de la problemática experimentada, identificando que estas poblaciones reconocen el nivel de vulnerabilidad y riesgo del área, pero siguen manteniendo su forma de vida porque su accionar responde a construcciones socioculturales y económicas propias. En este sentido, se concluye que las medidas preventivas entregadas por el Estado, con proyectos de reubicación de las poblaciones, son sesgadas, segmentadas y autoritarias. La falta de comunicación, respeto y entendimiento de las formas de interacción de la comunidad son, en gran parte, la razón del fracaso de estas iniciativas.
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Lee, D., M. Tertuliano, C. Harris, G. Vellidis, K. Levy (corresponding author), T. Coolong
Salmonella Survival in Soil and Transfer onto Produce via Splash Events Journal of Food Protection / 2019 |
Nearly one-half of foodborne illnesses in the United States can be attributed to fresh produce consumption. The preharvest stage of production presents a critical opportunity to prevent produce contamination in the field from contaminating postharvest operations and exposing consumers to foodborne pathogens. One produce-contamination route that is not often explored is the transfer of pathogens in the soil to edible portions of crops via splash water. We report here on the results from multiple field and microcosm experiments examining the potential for Salmonella contamination of produce crops via splash water, and the effect of soil moisture content on Salmonella survival in soil and concentration in splash water. In field and microcosm experiments, we detected Salmonella for up to 8 to 10 days after inoculation in soil and on produce. Salmonella and suspended solids were detected in splash water at heights of up to 80 cm from the soil surface. Soil-moisture conditions before the splash event influenced the detection of Salmonella on crops after the splash events--Salmonella concentrations on produce after rainfall were significantly higher in wet plots than in dry plots (geometric mean difference = 0.43 CFU/g; P = 0.03). Similarly, concentrations of Salmonella in splash water in wet plots trended higher than concentrations from dry plots (geometric mean difference = 0.67 CFU/100 mL; P = 0.04). These results indicate that splash transfer of Salmonella from soil onto crops can occur and that antecedent soil-moisture content may mediate the efficiency of microbial transfer. Splash transfer of Salmonella may, therefore, pose a hazard to produce safety. The potential for the risk of splash should be further explored in agricultural regions in which Salmonella and other pathogens are present in soil. These results will help inform the assessment of produce safety risk and the development of management practices for the mitigation of produce contamination.
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Peña-Gonzalez, A., M.J. Soto-Girón, S. Smith, J. Sistrunk, L. Montero, M. Páez, E.Ortega, J.K. Hatt, W. Cevallos, G. Trueba, K. Levy, K.T. Konstantinidis
Metagenomic signatures of gut infection caused by different Escherichia Coli pathotypes Applied and Environmental Microbiology / 2019 |
Escherichia coli is a leading contributor to infectious diarrhea and child mortality worldwide but it remains unknown how alterations in the gut microbiome vary for distinct E. coli pathotypes and whether these signatures can be used for diagnostic purposes. Further, the majority of enteric diarrheal infections are not diagnosed with respect to their etiological agent(s) due to technical challenges. Towards addressing these issues, we devised a novel approach that combined traditional, isolate-based and molecular biology techniques with metagenomics analysis of stool samples and epidemiological data. Application of this pipeline to children enrolled in a case-control study of diarrhea in Ecuador showed that, in about half of the cases where an E. coli pathotype was detected by culture and PCR, E. coli was likely not the causative agent based on metagenomic-derived low relative abundance, level of clonality and/or virulence gene content. Our results also showed that diffuse adherent E. coli (DAEC), a pathotype that is generally underrepresented in previous studies of diarrhea and thus, thought to not be highly virulent, caused several small-scale diarrheal outbreaks across a rural to urban gradient in Ecuador. DAEC infections were uniquely accompanied by co-elution of high amounts of human DNA and conferred significant shifts in the gut microbiome composition relative to controls or infections caused by other E. coli pathotypes. Our study shows that diarrheal infections can be efficiently diagnosed for their etiological agent and categorized based on their effects on the gut microbiome using metagenomic tools, which opens new possibilities for diagnostics and treatment.
Importance E. coli infectious diarrhea is an important contributor to child mortality worldwide. However, diagnosing and thus, treating E. coli infections remains challenging due to technical and other reasons associated with the limitations of the traditional culture-based techniques and the requirement to apply Koch's postulates. In this study, we integrated traditional microbiology techniques with metagenomics and epidemiology data in order to identify cases of diarrhea where E. coli was most likely the causative disease agent and evaluate specific signatures in the disease-state gut microbiome that distinguish between DAEC, ETEC and EPEC E. coli pathotypes. Therefore, our methodology and results should be highly relevant for diagnosing and treating diarrheal infections, and have important applications in public health. |
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Lee, D., H.H.Chang, S.E. Sarnat, K. Levy
Precipitation and Salmonellosis Incidence in Georgia, USA: Interactions between Extreme Rainfall Events and Antecedent Rainfall Conditions Environmental Health Perspectives / 2019 |
Background: The southeastern United States consistently has high salmonellosis incidence, but disease drivers remain unknown. Salmonella is regularly detected in this region’s natural environment, leading to numerous exposure opportunities. Rainfall patterns may impact the survival/transport of environmental Salmonella in ways that can affect disease transmission. Objectives: This study investigated associations between short-term precipitation (extreme rainfall events) and longer-term precipitation (rainfall conditions antecedent to these extreme events) on salmonellosis counts in the state of Georgia in the United States. Methods: For the period 1997–2016, negative binomial models estimated associations between weekly county-level extreme rainfall events (≥90th≥90th percentile of daily rainfall) and antecedent conditions (8-week precipitation sums, categorized into tertiles) and weekly county-level salmonellosis counts. Results:In Georgia’s Coastal Plain counties, extreme and antecedent rainfall were associated with significant differences in salmonellosis counts. In these counties, extreme rainfall was associated with a 5% increase in salmonellosis risk (95% CI: 1%, 10%) compared with weeks with no extreme rainfall. Antecedent dry periods were associated with a 9% risk decrease (95% CI: 5%, 12%), whereas wet periods were associated with a 5% increase (95% CI: 1%, 9%), compared with periods of moderate rainfall. In models considering the interaction between extreme and antecedent rainfall conditions, wet periods were associated with a 13% risk increase (95% CI: 6%, 19%), whereas wet periods followed by extreme events were associated with an 11% increase (95% CI: 5%, 18%). Associations were substantially magnified when analyses were restricted to cases attributed to serovars commonly isolated from wildlife/environment (e.g., Javiana). For example, wet periods followed by extreme rainfall were associated with a 34% risk increase (95% CI: 20%, 49%) in environmental serovar infection. Conclusions:Given the associations of short-term extreme rainfall events and longer-term rainfall conditions on salmonellosis incidence, our findings suggest that avoiding contact with environmental reservoirs of Salmonella following heavy rainfall events, especially during the rainy season, may reduce the risk of salmonellosis.
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Chard, A.N., K.K. Baker, K. Tsai, K. Levy, J.R. Sistrunk, H.H. Chang, M.C. Freeman Associations between soil-transmitted helminthiasis and viral, bacterial, and protozoal enteroinfections: a cross-sectional study in rural Laos Parasites & Vectors / 2019 |
Background: Humans are susceptible to over 1400 pathogens. Co-infection by multiple pathogens is common, and can result in a range of neutral, facilitative, or antagonistic interactions within the host. Soil-transmitted helminths (STH) are powerful immunomodulators, but evidence of the effect of STH infection on the direction and magnitude of concurrent enteric microparasite infections is mixed. Methods: We collected fecal samples from 891 randomly selected children and adults in rural Laos. Samples were analyzed for 5 STH species, 6 viruses, 9 bacteria, and 5 protozoa using a quantitative reverse transcription polymerase chain reaction (qRT-PCR) assay. We utilized logistic regression, controlling for demographics and household water, sanitation, and hygiene access, to examine the effect of STH infection on concurrent viral, bacterial, and protozoal infection. Results: We found that STH infection was associated with lower odds of concurrent viral infection [odds ratio (OR): 0.48, 95% confidence interval (CI): 0.28–0.83], but higher odds of concurrent bacterial infections (OR: 1.81, 95% CI: 1.06–3.07) and concurrent protozoal infections (OR: 1.50, 95% CI: 0.95–2.37). Trends were consistent across STH species. Conclusions: The impact of STH on odds of concurrent microparasite co-infection may differ by microparasite taxa, whereby STH infection was negatively associated with viral infections but positively associated with bacterial and protozoal infections. Results suggest that efforts to reduce STH through preventive chemotherapy could have a spillover effect on microparasite infections, though the extent of this impact requires additional study. The associations between STH and concurrent microparasite infection may reflect a reverse effect due to the cross-sectional study design. Additional research is needed to elucidate the exact mechanism of the immunomodulatory effects of STH on concurrent enteric microparasite infection.
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Islam, M.A, M.B. Amin, S. Roy, M. Asaduzzaman, M.R. Islam, T. Navab-Daneshmand, M.C. Mattioli, M.L. Kile, K. Levy, T.R. Julian
Fecal Colonization With Multidrug-Resistant E. coli Among Healthy Infants in Rural Bangladesh Frontiers in Microbiology / 2019 |
Third generation cephalosporins (3GC) are one of the main choices for treatment of infections caused by multidrug-resistant (MDR) Gram-negative bacteria. Due to their overuse, an increasing trend of resistance to 3GC has been observed in developing countries. Here, we describe fecal colonization of 3GC-resistant (3GCr) Escherichia coli in healthy infants (1–12 months old) living in rural areas of Bangladesh. We found that stool samples of 82% of infants (n = 100) were positive for 3GCr E. coli with a mean ± standard deviation of 6.21 ± 1.32 log10 CFU/g wet weight of stool. 3GCr E. coli encompasses an average one third (33%) of the total E. coli of stool. Almost 77% (n = 63) of these 3GCr E. coli were MDR (or resistant to ≥3 classes of antibiotics). Around 90% (n = 74) of 3GCr E. coli were extended spectrum beta-lactamase (ESBL)-producing in which blaCTX–M–group–1 was the predominant (96%, n = 71) ESBL-gene followed by blaTEM (41%, n = 30) and blaOXA–1 (11%, n = 8). A significant proportion (26.5%, n = 22) of 3GCr E. coli was pathogenic, comprising two types, enteroaggregative (EAEC, n = 19) and enteropathogenic (EPEC, n = 3). Colonization of 3GCr E. coli in infant guts was not associated with demographic characteristics such as age, sex, mode of delivery, maternal and infant antibiotic use, disease morbidity, and feeding practices. The high rate of colonization of 3GCr E. coli in infants’ guts is a serious public health concern which needs immediate attention and warrants further studies to explore the cause.
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Smith, S.M., L. Montero, M. Paez, E. Ortega, E. Hall, K. Bohnert, X. Sanchez, E. Puebla, P. Endara, W. Cevallos, G. Trueba, K. Levy
Locals Get Travelers' Diarrhea too: Risk factors for diarrheal illness and pathogenic E. coli infection across an urban-rural gradient in Ecuador Tropical Medicine & International Health / 2018 |
Objectives: Diarrhea is a common and well‐studied cause of illness afflicting international travelers. However, traveler's diarrhea can also result from travel between high and low disease transmission regions within a country, which is the focus of this study. Methods: We recruited participants for a case‐control study of diarrhea at four sites along an urban‐rural gradient in Northern Ecuador: Quito, Esmeraldas, Borbón and rural communities outside of Borbón. At each of these sites, approximately 100 subjects with diarrhea (cases) were recruited from Ministry of Health clinics and were age‐matched with subjects visiting the same clinics for other complaints (controls). Results: Travelers to urban destinations had higher risk of diarrhea and diarrheagenic E. coli (DEC) infections. Travel to Quito was associated with diarrhea (aOR = 2.01, 95% CI = 1.10‐3.68) and travel to Guayaquil (another urban center in Ecuador) was associated with Diffuse Adherent E. coli infection (OR = 2.09, 95% CI = 1.01‐4.33). Compared to those not traveling, urban origins were also associated with greater risk of diarrhea in Esmeraldas (aOR = 2.28, 95% CI = 1.20‐4.41), and with higher risk of diarrheagenic E. coli infections in Quito (aOR = 2.61, 95% CI = 1.16‐5.86), with >50% of travel from Quito and Esmeraldas specified as to another urban destination. Conclusions: This study suggests that individuals traveling from lower transmission regions (rural areas) to higher transmission regions (urban centers) within a single country are at a greater risk of acquiring a diarrhea‐related illness. Investments to improve water, sanitation and hygiene conditions in urban areas could have impacts on outlying rural areas within a given country.
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Lee, D., M. Tertuliano, G. Vellidis, C. Harris, M.K. Grossman, S. Rajeev, K. Levy
Evaluation of Grower-Friendly, Science-Based Sampling Approaches for the Detection of Salmonella in Ponds Used for Irrigation of Fresh Produce Foodborne Pathogens & Disease / 2018 |
The recognition that irrigation water sources contribute to preharvest contamination of produce has led to new regulations on testing microbial water quality. To best identify contamination problems, growers who depend on irrigation ponds need guidance on how and where to collect water samples for testing. In this study, we evaluated several sampling strategies to identify Salmonella and Escherichia coli contamination in five ponds used for irrigation on produce farms in southern Georgia. Both Salmonella and E. coli were detected regularly in all the ponds over the 19-month study period, with overall prevalence and concentrations increasing in late summer and early fall. Of 507 water samples, 217 (42.8%) were positive for Salmonella, with a very low geometric mean (GM) concentration of 0.06 most probable number (MPN)/100 mL, and 442 (87.1%) tested positive for E. coli, with a GM of 6.40 MPN/100 mL. We found no significant differences in Salmonella or E. coli detection rates or concentrations between sampling at the bank closest to the pump intake versus sampling from the bank around the pond perimeter, when comparing with results from the pump intake, which we considered our gold standard. However, samples collected from the bank closest to the intake had a greater level of agreement with the intake (Cohen's kappa statistic = 0.53; p < 0.001) than the samples collected around the pond perimeter (kappa = 0.34; p = 0.009). E. coli concentrations were associated with increased odds of Salmonella detection (odds ratio = 1.31; 95% confidence interval = 1.10–1.56). All the ponds would have met the Produce Safety Rule standards for E. coli, although Salmonella was also detected. Results from this study provide important information to growers and regulators about pathogen detection in irrigation ponds and inform best practices for surface water sampling.
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Levy, K., S. Smith, E.J. Carlton
Climate Change Impacts on Waterborne Diseases: Moving Toward Designing Interventions Current Environmental Health Reports / 2018 |
PURPOSE: Climate change threatens progress achieved in global reductions of infectious disease rates over recent decades. This review summarizes literature on potential impacts of climate change on waterborne diseases, organized around a framework of questions that can be addressed depending on available data. RECENT FINDINGS: A growing body of evidence suggests that climate change may alter the incidence of waterborne diseases, and diarrheal diseases in particular. Much of the existing work examines historical relationships between weather and diarrhea incidence, with a limited number of studies projecting future disease rates. Some studies take social and ecological factors into account in considerations of historical relationships, but few have done so in projecting future conditions. The field is at a point of transition, toward incorporating social and ecological factors into understanding the relationships between climatic factors and diarrheal diseases and using this information for future projections. The integration of these components helps identify vulnerable populations and prioritize adaptation strategies.
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Delahoy, M., B. Wodnik, L. McAliley, G. Penakalapati, J. Swarthout, M.C. Freeman, K. Levy
Pathogens Transmitted in Animal Feces in Low- and Middle-Income Countries International Journal of Hygiene and Environmental Health / 2018. |
Animals found in close proximity to humans in low-and middle-income countries (LMICs) harbor many pathogens capable of infecting humans, transmissible via their feces. Contact with animal feces poses a currently unquantified—though likely substantial—risk to human health. In LMIC settings, human exposure to animal feces may explain some of the limited success of recent water, sanitation, and hygiene interventions that have focused on limiting exposure to human excreta, with less attention to containing animal feces. We conducted a review to identify pathogens that may substantially contribute to the global burden of disease in humans through their spread in animal feces in the domestic environment in LMICs. Of the 65 potentially pathogenic organisms considered, 15 were deemed relevant, based on burden of disease and potential for zoonotic transmission. Of these, five were considered of highest concern based on a substantial burden of disease for which transmission in animal feces is potentially important: Campylobacter, non-typhoidal Salmonella (NTS), Lassa virus, Cryptosporidium, and Toxoplasma gondii. Most of these have a wide range of animal hosts, except Lassa virus, which is spread through the feces of rats indigenous to sub-Saharan Africa. Combined, these five pathogens cause close to one million deaths annually. More than half of these deaths are attributed to invasive NTS. We do not estimate an overall burden of disease from improperly managed animal feces in LMICs, because it is unknown what proportion of illnesses caused by these pathogens can be attributed to contact with animal feces. Typical water quantity, water quality, and handwashing interventions promoted in public health and development address transmission routes for both human and animal feces; however, sanitation interventions typically focus on containing human waste, often neglecting the residual burden of disease from pathogens transmitted via animal feces. This review compiles evidence on which pathogens may contribute to the burden of disease through transmission in animal feces; these data will help prioritize intervention types and regions that could most benefit from interventions aimed at reducing human contact with animal feces.
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Harris, C.S., M. Tertuliano, S. Rajeev, G. Vellidis, K. Levy
Impact of storm runoff on Salmonella and Escherichia coli prevalence in irrigation ponds of fresh produce farms in southern Georgia Journal of Applied Microbiology / 2018. |
AIMS: To examine Salmonella and Escherichia coli in storm runoff and irrigation ponds used by fresh produce growers, and compare Salmonella serovars with those found in cases of human salmonellosis. METHODS AND RESULTS: We collected water before and after rain events at two irrigation ponds on farms in southern Georgia, USA, and collected storm runoff/storm flow within the contributing watershed of each pond. Salmonella and E. coli concentrations were higher in ponds after rain events by an average of 0.46 (P < 0.01) and 0.61 (P < 0.05) log10 most probable number (MPN) 100 ml-1 , respectively. Salmonella concentrations in storm runoff from fields and forests were not significantly higher than in ponds before rain events, but concentrations in storm flow from streams and ditches were higher by an average of 1.22 log10 MPN 100 ml-1 (P < 0.001). Eighteen Salmonella serovars were identified from 155 serotyped isolates, and eight serovars were shared between storm runoff/storm flow and ponds. Seven of the serovars, including five of the shared serovars, were present in cases of human illness in the study region in the same year. However, several serovars most commonly associated with human illness in the study region (e.g. Javiana, Enteritidis, and Montevideo) were not found in any water samples. CONCLUSIONS: Salmonella and E. coli concentrations in irrigation ponds were higher, on average, after rain events, but concentrations of Salmonella were low, and the ponds met FDA water quality standards based on E. coli. Some similarities and notable differences were found between Salmonella serovars in water samples and in cases of human illness.
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Penakalapati, G., J. Swarthout, M.J. Delahoy, L. McAliley, B. Wodnik, K. Levy, M.C. Freeman
Exposure to Animal Feces and Human Health: A Systematic Review and Proposed Research Priorities Environmental Science & Technology / 2017. |
Humans can be exposed to pathogens from poorly managed animal feces, particularly in communities where animals live in close proximity to humans. This systematic review of peer-reviewed and gray literature examines the human health impacts of exposure to poorly managed animal feces transmitted via water, sanitation, and hygiene (WASH)-related pathways 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 measures to reduce human exposure, and propose research priorities for further inquiry. Exposure to animal feces has been associated with diarrhea, soil-transmitted helminth infection, trachoma, environmental enteric dysfunction, and growth faltering. Few studies have evaluated control measures, but interventions include reducing cohabitation with animals, provision of animal feces scoops, controlling animal movement, creating safe child spaces, improving veterinary care, and hygiene promotion. Future research should evaluate: behaviors related to points of contact with animal feces; animal fecal contamination of food; cultural behaviors of animal fecal management; acute and chronic health risks associated with exposure to animal feces; and factors influencing concentrations and shedding rates of pathogens originating from animal feces.
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Moser, K.A., L. Zhang, I. Spicknall, N.P. Braykov, K. Levy, C.F. Marrs, B. Foxman, G. Trueba, W. Cevallos, J. Goldstick, J. Trostle, J.N.S. Eisenberg
The role of mobile genetic elements in the spread of antimicrobial-resistant Escherichia coli from chickens to humans in small-scale production poultry operations in rural Ecuador American Journal of Epidemiology / 2018. |
Small-scale production poultry operations are increasingly common worldwide. To investigate how these operations influence antimicrobial resistance and mobile genetic elements (MGEs), Escherichia coli isolates were sampled from small-scale production birds (raised in confined spaces with antibiotics in feed), household birds (no movement constraints; fed on scraps), and humans associated with these birds in rural Ecuador (2010–2012). Isolates were screened for genes associated with MGEs as well as phenotypic resistance to 12 antibiotics. Isolates from small-scale production birds had significantly elevated odds of resistance to 7 antibiotics and presence of MGE genes compared with household birds (adjusted odds ratio (OR) range = 2.2–87.9). Isolates from humans associated with small-scale production birds had elevated odds of carrying an integron (adjusted OR = 2.0; 95% confidence interval (CI): 1.06, 3.83) compared with humans associated with household birds, as well as resistance to sulfisoxazole (adjusted OR = 1.9; 95% CI: 1.01, 3.60) and trimethoprim/sulfamethoxazole (adjusted OR = 2.1; 95% CI: 1.13, 3.95). Stratifying by the presence of MGEs revealed antibiotic groups that are explained by biological links to MGEs; in particular, resistance to sulfisoxazole, trimethoprim/sulfamethoxazole, or tetracycline was highest among birds and humans when MGE exposures were present. Small-scale production poultry operations might select for isolates carrying MGEs, contributing to elevated levels of resistance in this setting.
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Muñoz, M.T., B. Lucero, K. Levy, V. Iglesias
Exposure to organophosphate (OP) pesticides and health conditions in agricultural and non-agricultural workers from Maule, Chile International Journal of Environmental Health Research / 2017. |
The objective was to evaluate the characteristics of exposure to OP pesticides and health status in Chilean farm workers from the Maule Region. An occupational health questionnaire was administered in 207 agricultural and non-agricultural workers. For the group of agricultural workers, we asked about speci c occupational exposure history and symptoms of OP pesticide poisoning. The main health problem of the exposed group was previous OP pesticide poisoning (p < 0.001). Fifty-six percent of agricultural workers reported symptoms consistent with acute OP pesticide poisoning. The use of respiratory personal protective equipment and younger age were protective against these symptoms, and number of years of OP pesticide exposure was positively associated with reporting symptoms of poisoning. Of the pesticide applicators 47 % reported using chlorpyrifos. The regulations regarding use and application of pesticides should be strengthened, as should training and intervention with workers to improve the use of personal protective equipment.
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(Excerpt) There is ample work to do to develop new strategies to adapt to the specific infectious disease threats posed by climate change, such as developing enhanced surveillance programs and early warning systems for extreme events. We must seek out these creative solutions to combat the particular threats of climate change. At the same time, we should not forget the many off-the-shelf tools already at our disposal--such as water and sanitation infrastructure, mosquito abatement, and sustained vaccination campaigns, and use new research to apply these existing strategies more effectively.
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Antaki, E.M., G. Vellidis, C. Harris, P. Aminabadi, K. Levy, M.T. Jay-Russell
Low concentrations of Salmonella enterica and generic Escherichia coli in farm ponds and irrigation distribution systems used for mixed produce production in southern Georgia Food Pathogens & Disease / 2016. |
Studies have shown that irrigation water can be a vector for pathogenic bacteria. Due to this, the Food Safety Modernization Act's (FSMA) produce safety rule requires that agricultural water directly applied to produce be safe and of adequate sanitary quality for use, which may pose a challenge for some farmers. The purpose of this research was to assess the presence and concentration of Salmonella and generic Escherichia coli in irrigation water from distribution systems in a mixed produce production region of southern Georgia. Water samples were collected during three growing seasons at three farms irrigating crops with surface water (Pond 1, Pond 2) or groundwater (Well) during 2012–2013. Salmonella and generic E. coli populations were monitored by culture and Most Probable Number (MPN). Confirmed isolates were characterized by pulsed-field gel electrophoresis and serotyping. In Pond 1, Salmonella was detected in 2/21 surface, 5/26 subsurface, 10/50 center pivot, and 0/16 solid set sprinkler head water samples. In Pond 2, Salmonella was detected in 2/18 surface, 1/18 subsurface, 6/36 drip line start, and 8/36 drip line end water samples. Twenty-six well pumps and 64 associated drip line water samples were negative. The overall mean Salmonella concentration for positive water samples was 0.03 MPN/100 mL (range <0.0011–1.8 MPN/100 mL). Nine Salmonella serovars comprising 22 pulsotypes were identified. Identical serovars and subtypes were found three times on the same day and location: Pond 1-Pivot-Cantaloupe (serovar Rubislaw), Pond 1-Pivot-Peanut (serovar Saintpaul), and Pond 2-Drip Line Start-Drip Line End-Yellow Squash (serovar III_16z10:e,n,x,z15). Generic E. coli was detected in water from both farm ponds and irrigation distribution systems, but the concentrations met FSMA microbial water quality criteria. The results from this study will allow producers in southern Georgia to better understand how potential pathogens move through irrigation distribution systems.
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Levy, K., A.P. Woster, R.S. Goldstein, E. Carlton
Untangling the impacts of climate change on waterborne diseases: A systematic review of relationships between meteorological factors and diarrheal diseases. Environmental Science & Technology / 2016. |
Global climate change is expected to affect waterborne enteric diseases, yet to date there has been no comprehensive, systematic review of the epidemiological literature examining the relationship between meteorological conditions and diarrheal diseases. We searched PubMed, Embase, Web of Science, and the Cochrane Collection for studies describing the relationship between diarrheal diseases and four meteorological conditions that are expected to increase with climate change: ambient temperature, heavy rainfall, drought, and flooding. We synthesized key areas of agreement and evaluated the biological plausibility of these findings, drawing from a diverse, multidisciplinary evidence base. We identified 141 articles that met our inclusion criteria. Key areas of agreement include a positive association between ambient temperature and diarrheal diseases, with the exception of viral diarrhea and an increase in diarrheal disease following heavy rainfall and flooding events. Insufficient evidence was available to evaluate the effects of drought on diarrhea. There is evidence to support the biological plausibility of these associations, but publication bias is an ongoing concern. Future research evaluating whether interventions, such as improved water and sanitation access, modify risk would further our understanding of the potential impacts of climate change on diarrheal diseases and aid in the prioritization of adaptation measures.
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Levy, K., M. Klein, S.E. Sarnat, S. Panwhar, A. Huttinger, P. Tolbert, C. Moe
Refined assessment of associations between drinking water residence time and emergency department visits for gastrointestinal illness in metro Atlanta, Georgia Journal of Water & Health / 2016. |
Recent outbreak investigations suggest that a substantial proportion of waterborne disease outbreaks are attributable to water distribution system issues. In this analysis, we examine the relationship between modeled water residence time (WRT), a proxy for probability of microorganism intrusion into the distribution system, and emergency department visits for gastrointestinal (GI) illness for two water utilities in Metro Atlanta, USA during 1993–2004. We also examine the association between proximity to the nearest distribution system node, based on patients' residential address, and GI illness using logistic regression models. Comparing long (≥90th percentile) with intermediate WRTs (11th to 89th percentile), we observed a modestly increased risk for GI illness for Utility 1 (OR = 1.07, 95% CI: 1.02–1.13), which had substantially higher average WRT than Utility 2, for which we found no increased risk (OR = 0.98, 95% CI: 0.94–1.02). Examining finer, 12-hour increments of WRT, we found that exposures >48 h were associated with increased risk of GI illness, and exposures of >96 h had the strongest associations, although none of these associations was statistically significant. Our results suggest that utilities might consider reducing WRTs to <2–3 days or adding booster disinfection in areas with longer WRT, to minimize risk of GI illness from water consumption.
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Philipsborn, R., S. Ahmed, B.J. Brosi, K. Levy
Climatic drivers of diarrheagenic Escherichia coli: A systematic review and meta-analysis Journal of Infectious Diseases / 2016. |
BACKGROUND: Positive associations have been noted between temperature and diarrhea but considerable uncertainty surrounds quantitative estimates of this relationship because of pathogen-specific factors and a scarcity of climate-disease data. Quantifying this relationship is important for disease prevention and climate change adaptation. METHODS: To address these issues, we carried out a systematic literature review of studies that reported monthly diarrheagenic Escherichia coliincidence for at least a full year. We characterized seasonal patterns of disease incidence from 28 studies. In addition, using monthly time- and location-specific weather data for 18 studies, we carried out univariate Poisson models on individual studies and a meta-analysis using a generalized estimating equation (GEE) on the entire dataset. RESULTS: We found an 8% increase in incidence of diarrheagenic E. coli(95% confidence interval: 5-11%; p<0.0001) for a 1°C increase in mean monthly temperature. We found a modest positive association between 1-month lagged mean rainfall and diarrheagenic E. coli, which was not statistically significant when controlling for temperature. CONCLUSIONS: These results suggest that increases in ambient temperature correspond to elevated incidence of diarrheagenic E. coliinfections and underscore the need to redouble efforts to prevent the transmission of these pathogens in the face of increasing global temperatures.
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Braykov, N., J.N.S. Eisenberg, M. Grossman, L. Zhang, K. Vasco, W. Cevallos, D. Muñoz, A. Acevedo, K. A. Moser, C. F. Marrs, B. Foxman, J. Trostle, G. Trueba, K. Levy
Antibiotic Resistance in Animal and Environmental Samples Associated with Small-Scale Poultry Farming in Northwestern Ecuador mSphere / 2016. |
The effects of animal agriculture on the spread of antibiotic resistance (AR) are cross-cutting and thus require a multidisciplinary perspective. Here we use ecological, epidemiological, and ethnographic methods to examine populations of Escherichia coli circulating in the production poultry farming environment versus the domestic environment in rural Ecuador, where small-scale poultry production employing nontherapeutic antibiotics is increasingly common. We sampled 262 “production birds” (commercially raised broiler chickens and laying hens) and 455 “household birds” (raised for domestic use) and household and coop environmental samples from 17 villages between 2010 and 2013. We analyzed data on zones of inhibition from Kirby-Bauer tests, rather than established clinical breakpoints for AR, to distinguish between populations of organisms. We saw significantly higher levels of AR in bacteria from production versus household birds; resistance to either amoxicillin-clavulanate, cephalothin, cefotaxime, and gentamicin was found in 52.8% of production bird isolates and 16% of household ones. A strain jointly resistant to the 4 drugs was exclusive to a subset of isolates from production birds (7.6%) and coop surfaces (6.5%) and was associated with a particular purchase site. The prevalence of AR in production birds declined with bird age (P < 0.01 for all antibiotics tested except tetracycline, sulfisoxazole, and trimethoprim-sulfamethoxazole). Farming status did not impact AR in domestic environments at the household or village level. Our results suggest that AR associated with small-scale poultry farming is present in the immediate production environment and likely originates from sources outside the study area. These outside sources might be a better place to target control efforts than local management practices.
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Mellor, J., K. Levy, J. Zimmerman, M. Elliott, J. Bartram, E. Carlton, T. Clasen, R. Dillingham, J. Eisenberg, R. Guerrant, D. Lantagne, J. Mihelcic, K. Nelson
Planning for climate change: The need for mechanistic systems-based approaches to study climate change impacts on diarrheal diseases Science of the Total Environment / 2016. |
Increased precipitation and temperature variability as well as extreme events related to climate change are predicted to affect the availability and quality of water globally. Already heavily burdened with diarrheal diseases due to poor access to water, sanitation and hygiene facilities, communities throughout the developing world lack the adaptive capacity to sufficiently respond to the additional adversity caused by climate change. Studies suggest that diarrhea rates are positively correlated with increased temperature, and show a complex relationship with precipitation. Although climate change will likely increase rates of diarrheal diseases on average, there is a poor mechanistic understanding of the underlying disease transmission processes and substantial uncertainty surrounding current estimates. This makes it difficult to recommend appropriate adaptation strategies. We review the relevant climate-related mechanisms behind transmission of diarrheal disease pathogens and argue that systems-based mechanistic approaches incorporating human, engineered and environmental components are urgently needed. We then review successful systems-based approaches used in other environmental health fields and detail one modeling framework to predict climate change impacts on diarrheal diseases and design adaptation strategies.
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Lu, J., I. Struewing, E. Vereen, A.E. Kirby, K. Levy, C. Moe, N. Ashbolt
Molecular Detection of Legionella spp. and their associations with Mycobacterium app., Pseudomonas aeruginosa and amoeba hosts in a drinking water distribution system Journal of Applied Microbiology / 2016. |
AIMS: This study investigated waterborne opportunistic pathogens (OPs) including potential hosts, and evaluated the use of Legionella spp. for indicating microbial water quality for OPs within a full-scale operating drinking water distribution system (DWDS). METHODS & RESULTS: To investigate the occurrence of specific microbial pathogens within a major city DWDS we examined large volume (90 l drinking water) ultrafiltration (UF) concentrates collected from six sites between February, 2012 and June, 2013. The detection frequency and concentration estimates by qPCR were: Legionella spp. (57%/85 cell equivalent, CE l−1), Mycobacterium spp. (88%/324 CE l−1), Pseudomonas aeruginosa (24%/2 CE l−1), Vermamoeba vermiformis (24%/2 CE l−1) and Acanthamoeba spp. (42%/5 cyst equivalent, CE l−1). There was no detection of the following microorganisms: human faecal indicator Bacteroides (HF183), Salmonella enterica, Campylobacterspp., Escherichia coli O157:H7, Giardia intestinalis, Cryptosporidium spp. or Naegleria fowleri. There were significant correlations between the qPCR signals of Legionella spp. and Mycobacterium spp., and their potential hosts V. vermiformis and Acanthamoeba spp. Sequencing of Legionella spp. demonstrated limited diversity, with most sequences coming from two dominant groups, of which the larger dominant group was an unidentified species. Other known species including Legionella pneumophila were detected, but at low frequency. The densities of Legionella spp. and Mycobacterium spp. were generally higher (17 and 324 folds, respectively) for distal sites relative to the entry point to the DWDS. CONCLUSIONS: Legionella spp. occurred, had significant growth and were strongly associated with free-living amoebae (FLA) and Mycobacterium spp., suggesting that Legionella spp. could provide a useful DWDS monitoring role to indicate potential conditions for non-faecal OPs. SIGNIFICANCE AND IMPACT OF THE STUDY: The results provide insight into microbial pathogen detection that may aid in the monitoring of microbial water quality within DWDS prior to customer exposures.
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Carlton, E.J., A.P. Woster, P. DeWitt, R.S. Goldstein, K. Levy
A systematic review and meta-analysis of ambient temperature and diarrhea diseases International Journal of Epidemiology / 2015. |
BACKGROUND: Global climate change is expected to increase the risk of diarrhoeal diseases, a leading cause of childhood mortality. However, there is considerable uncertainty about the magnitude of these effects and which populations bear the greatest risks. METHODS: We conducted a systematic review using defined search terms across four major databases and, additionally, examined the references of 54 review articles captured by the search. We evaluated sources of heterogeneity by pathogen taxon, exposure measure, study quality, country income level and regional climate, and estimated pooled effect estimates for the subgroups identified in the heterogeneity analysis, using meta-analysis methods. RESULTS: We identified 26 studies with 49 estimates. Pathogen taxa were a source of heterogeneity. There was a positive association between ambient temperature and all-cause diarrhoea (incidence rate ratio (IRR) 1.07; 95% confidence interval (CI) 1.03, 1.10) and bacterial diarrhoea (IRR 1.07; 95% CI 1.04, 1.10), but not viral diarrhoea (IRR 0.96; 95% CI 0.82, 1.11). These associations were observed in low-, middle- and high-income countries. Only one study of protozoan diarrhoea was identified. CONCLUSIONS: Changes in temperature due to global climate change can and may already be affecting diarrhoeal disease incidence. The vulnerability of populations may depend, in part, on local pathogen distribution. However, evidence of publication bias and the uneven geographical distribution of studies limit the precision and generalizability of the pooled estimates.
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Levy, K.
Does Poor Water Quality Cause Diarrheal Disease? American Journal of Tropical Medicine and Hygiene / 2015. |
AJTMH editorial on Luby and others article, Microbiological Contamination of Drinking Water Associated with Subsequent Child Diarrhea.
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Pino, P., V. Iglesias, R. Garreaud, S. Cortés, M. Canals, W. Folch, S. Burgos, K. Levy, L. Naeher, K. Steenland.
Chile Confronts its Environmental Health Future After 25 Years of Accelerated Growth Annals of Global Health / 2015. |
BACKGROUND: Chile has recently been reclassified by the World Bank from an upper-middle-income country to a high-income country. There has been great progress in the last 20 to 30 years in relation to air and water pollution in Chile. Yet after 25 years of unrestrained growth, there remain clear challenges posed by air and water, as well as climate change. METHODS: In late 2013, a 3-day workshop on environmental health was held in Santiago, Chile, bringing together researchers and government policymakers. As a follow-up to that workshop, here we review the progress made in environmental health in the past 20 to 30 years and discuss the challenges of the future. We focus on air and water pollution and climate change, which we believe are among the most important areas of environmental health in Chile. RESULTS: Air pollution in some cities remains among the highest in the continent. Potable water is generally available, but weak state supervision has led to serious outbreaks of infectious disease and ongoing issues with arsenic exposure in some regions. Climate change modeling in Chile is quite sophisticated, and a number of the impacts of climate change can be reasonably predicted in terms of which areas of the country are most likely to be affected by increased temperature and decreased availability of water, as well as expansion of vector territory. Some health effects, including changes in vector-borne diseases and excess heat mortality, can be predicted. However, there has yet to be an integration of such research with government planning. CONCLUSIONS: Although great progress has been made, currently there are a number of problems. We suspect that the Chilean experience in environmental health may be of some use for other Latin American countries with rapid economic development.
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Armas-Freire, P.I., G. Trueba, C. Proaño-Bolaños, K. Levy, L. Zhang, C.F. Marrs, W. Cevallos, J.N.S. Eisenberg.
Unexpected distribution of the fluroquinolon-resistance gene qnrB in Escherichia coli isolates from different human and poultry origins in Ecuador International Microbiology / 2015. |
Fluoroquinolone resistance can be conferred through chromosomal mutations or by the acquisition of plasmids carrying genes such as the quinolone resistance gene (qnr). In this study, 3,309 strains of commensal Escherichia coli were isolated in Ecuador from: (i) humans and chickens in a rural northern coastal area (n = 2368, 71.5%) and (ii) chickens from an industrial poultry operation (n = 827, 25%). In addition, 114 fluoroquinolone-resistant strains from patients with urinary tract infections who were treated at three urban hospitals in Quito, Ecuador were analyzed. All of the isolates were subjected to antibiotic susceptibility screening. Fluoroquinolone-resistant isolates (FRIs) were then screened for the presence of qnrB genes. A significantly higher phenotypic resistance to fluoroquinolones was determined in E. coli strains from chickens in both the rural area (22%) and the industrial operation (10%) than in strains isolated from humans in the rural communities (3%). However, the rates of qnrB genes in E. coli isolates from healthy humans in the rural communities (11 of 35 isolates, 31%) was higher than in chickens from either the industrial operations (3 of 81 isolates, 6%) or the rural communities (7 of 251 isolates, 2.8%). The occurrence of qnrB genes in human FRIs obtained from urban hospitals was low (1 of 114 isolates, 0.9%). These results suggested that the qnrB gene is more widely distributed in rural settings, where antibiotic usage is low, than in urban hospitals and industrial poultry operations. The role of qnrB in clinical resistance to fluoroquinolones is thus far unknown.
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Zhang, L., K. Levy, G. Trueba, W. Cevallos, J. Trostle, B. Foxman, C.F. Marrs, J.N.S. Eisenberg
The effects of selection pressure and genetic association on the relationship between antibiotic resistance and virulence in Escherichia coli Antimicrobial Agents & Chemotherapy / 2015. |
Antibiotic selection pressure and genetic associations may lead to the co-occurrence of resistance and virulence in individual pathogens. However, there is a lack of rigorous epidemiological evidence that demonstrates co-occurrence of resistance and virulence at the population level. Using samples from a population-based case-control study in 25 villages in rural Ecuador, we characterized resistance to 12 antibiotics among pathogenic (n=86) and commensal (n=761) E. coli isolates, classified by the presence or absence of known diarrheagenic virulence factor genes. Prevalence of resistance to single and multiple antibiotics was significantly higher in pathogenic compared to commensal isolates. Using a generalized estimating equation, antibiotic resistance was independently associated with virulence factor carriage, case status and antibiotic use (OR = 3.0, 95% CI (1.7 – 5.1); OR = 2.0, 95% CI (1.3 – 3.0); OR = 1.5, 95% CI (0.9 – 2.5) respectively). Virulence factor carriage was more strongly related to antibiotic resistance than antibiotic use for all antibiotics examined, with the exception of fluoroquinolones, gentamicin, and cefotaxime. This study provides epidemiological evidence that antibiotic resistance and virulence factor carriage are linked in E. coli populations in a community setting. Further, these data suggest that, while the co-occurrence of resistance and virulence in E. coli is partially due to antibiotic selection pressure, it is also genetically determined. These findings should be considered when developing strategies for treating infections and controlling for antibiotic resistance.
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Berendes, D., K. Levy, J. Knee, T. Handzel, V. Hill.
Ascaris and Escherichia coli Inactivation in an Ecological Sanitation System in Port-au- Prince, Haiti PLoS One / 2015. |
The goal of this study was to evaluate the microbial die-off in a latrine waste composting system in Port-au-Prince, Haiti. Temperature data and samples were collected from compost aged 0 – 12+ months. Samples collected from compost bin centers and corners at two depths were assessed for moisture content, E. coli concentration, and Ascaris spp. viability. Center temperatures in compost bins were all above 58 °C, while corner temperatures were 10 – 20 °C lower. Moisture content was 67 ± 10% in all except the oldest compost. A 4-log reduction in E. coli was observed over the first sixteen weeks of composting at both locations and depths, after which E. coli was undetectable (LOD: 142 MPN g-1 dry weight). In new compost, 10.4%and 8.3% of Ascaris eggs were viable and fully embryonated, respectively. Percent viability dropped to zero in samples older than six weeks. These findings indicate that the Haitian EcoSan composting process was effective in inactivating E. coli and Ascaris spp. in latrine waste within sixteen weeks. This study is one of the first to document efficacy of an ecological sanitation system under field conditions and provides insight into composting methods and monitoring for other international settings.
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Streby, A., B. Mull, K. Levy, V. Hill.
Comparison of real-time PCR methods for the detection of Naegleria fowleri in surface water and sediment Parasitology Research / 2015. |
Naegleria fowleri is a thermophilic free-living ameba found in freshwater environments worldwide. It is the cause of a rare but potentially fatal disease in humans known as primary amebic meningoencephalitis. Established N. fowleri detection methods rely on conventional culture techniques and morphological examination followed by molecular testing. Multiple alternative real-time PCR assays have been published for rapid detection of Naegleria spp. and N. fowleri. Foursuch assays were evaluated for the detection of N. fowleri from surface water and sediment. The assays were compared for thermodynamic stability, analytical sensitivity and specificity, detection limits, humic acid inhibition effects, and performance with seeded environmental matrices. Twenty-one ameba isolates were included in the DNA panel used for analytical sensitivity and specificity analyses. N. fowleri genotypes I and III were used for method performance testing. Two of the real-time PCR assays were determined to yield similar performance data for specificity and sensitivity for detecting N. fowleri in environmental matrices.
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Rao, G., J.N.S. Eisenberg, D.G. Kleinbaum, W. Cevallos, G. Trueba, K. Levy.
Spatial Variability of Escherichia coli in Rivers of Northern Coastal Ecuador Water / 2015. |
The use of contaminated surface water continues to be a pressing issue in areas of the world where people lack improved drinking water sources. In northern coastal Ecuador, many communities rely on untreated surface water as their primary source of drinking water. We undertook a study to explore how microscale river hydrodynamics affect microbial water quality at community water collection locations at three rivers with varying stream velocity and turbidity profiles. To examine how the distance from river shore and physiochemical water quality variables affect microbial contamination levels in the rivers; we collected a total of 355 water samples within six villages on three rivers; and tested for Escherichia coli concentrations using the IDEXX Quanti-tray method. We found that log10 E. coli concentrations decreased with increasing distance from shore (β = −0.017; p = 0.003). Water in the main channel had E. coli concentrations on average 0.12 log10 lower than within eddies along the river shore and 0.27 log10 lower between the sample closest to shore and any sample >6 m from the shore. Higher E. coli concentrations were also significantly associated with increased turbidity (β = 0.003; p < 0.0001) and decreased dissolved oxygen levels (β = −0.310; p < 0.0001). The results of this study can help inform community members about the safest locations to collect drinking water and also provide information on watershed scale transport of microbial contaminants between villages.
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Blumstein, D., K. Levy, E. Mayer, J. Harte.
Clinical Brief: Gastrointestinal Dysbiosis Evolution, Medicine & Public Health / 2014. |
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Zambrano, L, K. Levy, N.P. Menezes, M.C. Freeman
Human diarrhea infections associated with domestic animal husbandry: a systematic review and meta-analysis Transactions of the Royal Society of Tropical Medicine & Hygiene / 2014. *Editor's Choice |
Domestic animal husbandry, a common practice globally, can lead to zoonotic transmission of enteric pathogens. However, this risk has received little attention to date. This systematic review and meta-analysis examines the evidence for an association between domestic exposure to food-producing animals and cases of human diarrhea and specific enteric infections. We performed a systematic review of available literature to examine domestic livestock and poultry as risk factors for diarrhea and applied pre-determined quality criteria. Where possible, we carried out meta-analysis of specific animal–pathogen pairs. We found consistent evidence of a positive association between exposure to domestic food-producing animals and diarrheal illness across a range of animal exposures and enteric pathogens. Out of 29 studies included in the review, 20 (69.0%) reported a positive association between domestic animal exposure and diarrhea. Domestic exposure to poultry revealed a substantial association with human campylobacteriosis (OR 2.73, 95% CI 1.90–3.93). Our results suggest that domestic poultry and livestock exposures are associated with diarrheal illness in humans. Failure to ascertain the microbial cause of disease may mask this effect. Exposure to domestic animals should be considered a risk factor for human diarrheal illness and additional studies may identify potential mitigation strategies to address this risk.
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Levy, K., L. Anderson, K.A. Robb, W. Cevallos, G. Trueba, J.N.S Eisenberg
Household effectiveness vs. laboratory efficacy of point-of-use chlorination Water Research / 2014. |
Treatment of water at the household level offers a promising approach to combat the global burden of diarrheal diseases. In particular, chlorination of drinking water has been a widely promoted strategy due to persistence of residual chlorine after initial treatment. However, the degree to which chlorination can reduce microbial levels in a controlled setting (efficacy) or in a household setting (effectiveness) can vary as a function of chlorine characteristics, source water characteristics, and household conditions. To gain more understanding of these factors, we carried out an observational study within households in rural communities of northern coastal Ecuador. We found that the efficacy of chlorine treatment under controlled conditions was significantly better than its household effectiveness when evaluated both by ability to meet microbiological safety standards and by log reductions. Water treated with chlorine achieved levels of microbial contamination considered safe for human consumption after 24 h of storage in the household only 39-51% of the time, depending on chlorine treatment regimen. Chlorine treatment would not be considered protective against diarrheal disease according to WHO log reduction standards. Factors that explain the observed compromised effectiveness include: source water turbidity, source water baseline contamination levels, and in-home contamination. Water in 38% of the households that had low turbidity source water (<10 NTU) met the safe water standard as compared with only 17% of the households that had high turbidity source water (>10 NTU). A 10 MPN/100 mL increase in baseline Escherichia coli levels was associated with a 2.2% increase in failure to meet the E. coli standard. Higher mean microbial contamination levels were seen in 54% of household samples in comparison to their matched controls, which is likely the result of in-home contamination during storage. Container characteristics (size of the container mouth) did not influence chlorine effectiveness. We found no significant differences between chlorine treatment regimens in ability to meet the safe water standards or in overall log reductions, although chlorine dosage did modify the effect of source conditions. These results underscore the importance of measuring both source water and household conditions to determine appropriate chlorine levels, as well as to evaluate the appropriateness of chlorine treatment and other point-of-use water quality improvement interventions.
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Gonzales, G., A. Zevallos, C. Gonzales-Castañeda, D. Nuñez, C. Gastañaga, C. Cabezas, L. Naeher, K. Levy, K. Steenland
Contaminación Ambiental, Variabilidad Climática y Cambio Climático: Una Revisión del Impacto en la Salud de la Población Peruana Rev. Per. Med. Exp. Salud Publica / 2014. |
El presente artículo es una revisión sobre la contaminación del agua, el aire y el efecto del cambio climático en la salud de la población peruana. Uno de los principales contaminantes del aire es el material particulado menor de 2,5 μ (PM 2,5), en la ciudad de Lima, anualmente 2300 muertes prematuras son atribuibles a este contaminante. Otro problema es la contaminación del aire domiciliario por el uso de cocinas con combustible de biomasa, donde la exposición excesiva a PM 2,5 dentro de las casas es responsable de aproximadamente 3000 muertes prematuras anuales entre adultos, con otro número desconocido de muertes entre niños debido a infecciones respiratorias. La contaminación del agua tiene como principales causas los desagües vertidos directamente a los ríos, minerales (arsénico) de varias fuentes, y fallas de las plantas de tratamiento. En el Perú, el cambio climático puede impactar en la frecuencia y severidad del fenómeno de El Niño oscilación del sur (ENSO) que se ha asociado con un incremento en los casos de enfermedades como cólera, malaria y dengue. El cambio climático incrementa la temperatura y puede extender las áreas afectadas por enfermedades transmitidas por vectores, además de tener efecto en la disponibilidad del agua y en la contaminación del aire. En conclusión, el Perú, pasa por una transición de factores de riesgo ambientales, donde coexisten riesgos tradicionales y modernos, y persisten los problemas infecciosos y crónicos, algunos de los cuales se asocian con problemas de contaminación de agua y de aire.
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Tallis, H., J. Lubchenco … K. Levy … et al. (one of 238 authors).
Working Together: A call for inclusive participation Nature / 2014. |
Heather Tallis, Jane Lubchenco and 238 co-signatories petition for an end to the infighting that is stalling progress in protecting the planet.
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Carlton, E.J., J.N.S. Eisenberg, J. Goldstick, W. Cevallos, J. Trostle, K. Levy
Heavy Rainfall Events and Diarrhea Incidence: The Role of Social and Environmental Factors American Journal of Epidemiology / 2013. |
The impact of heavy rainfall events on waterborne diarrheal diseases is uncertain. We conducted weekly, active surveillance for diarrhea in 19 villages in Ecuador from February 2004 to April 2007 in order to evaluate whether biophysical and social factors modify vulnerability to heavy rainfall events. A heavy rainfall event was defined as 24-hour rainfall exceeding the 90th percentile value (56 mm) in a given 7-day period within the study period. Mixed-effects Poisson regression was used to test the hypothesis that rainfall in the prior 8 weeks, water and sanitation conditions, and social cohesion modified the relationship between heavy rainfall events and diarrhea incidence. Heavy rainfall events were associated with increased diarrhea incidence following dry periods (incidence rate ratio = 1.39, 95% confidence interval: 1.03, 1.87) and decreased diarrhea incidence following wet periods (incidence rate ratio = 0.74, 95% confidence interval: 0.59, 0.92). Drinking water treatment reduced the deleterious impacts of heavy rainfall events following dry periods. Sanitation, hygiene, and social cohesion did not modify the relationship between heavy rainfall events and diarrhea. Heavy rainfall events appear to affect diarrhea incidence through contamination of drinking water, and they present the greatest health risks following periods of low rainfall. Interventions designed to increase drinking water treatment may reduce climate vulnerability.
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Ahmed, S.M., B.A. Lopman, K. Levy
A Systematic Review and Meta-Analysis of the Global Seasonality of Norovirus PLoS ONE / 2013. |
BACKGROUND:Noroviruses are the most common cause of acute gastroenteritis across all ages worldwide. These pathogens are generally understood to exhibit a wintertime seasonality, though a systematic assessment of seasonal patterns has not been conducted in the era of modern diagnostics. METHODS:We conducted a systematic review of the Pubmed Medline database for articles published between 1997 and 2011 to identify and extract data from articles reporting on monthly counts of norovirus. We conducted a descriptive analysis to document seasonal patterns of norovirus disease, and we also constructed multivariate linear models to identify factors associated with the strength of norovirus seasonality. RESULTS:The searched identified 293 unique articles, yielding 38 case and 29 outbreak data series. Within these data series, 52.7% of cases and 41.2% of outbreaks occurred in winter months, and 78.9% of cases and 71.0% of outbreaks occurred in cool months. Both case and outbreak studies showed an earlier peak in season-year 2002-03, but not in season-year 2006-07, years when new genogroup II type 4 variants emerged. For outbreaks, norovirus season strength was positively associated with average rainfall in the wettest month, and inversely associated with crude birth rate in both bivariate and multivariate analyses. For cases, none of the covariates examined was associated with season strength. When case and outbreaks were combined, average rainfall in the wettest month was positively associated with season strength. CONCLUSIONS:Norovirus is a wintertime phenomenon, at least in the temperate northern hemisphere where most data are available. Our results point to possible associations of season strength with rain in the wettest month and crude birth rate.
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Muñoz-Quezada, M.T., B.A. Lucero, D.B. Barr, K. Steenland, K. Levy, P.B. Ryan, V. Iglesias, S. Alvarado, C. Concha, E. Rojas, C. Vega
Neurodevelopmental effects in children associated with exposure to organo-phosphate pesticides: A Systematic Review Neurotoxicology / 2013. |
Many studies have investigated the neurodevelopmental effects of prenatal and early childhood exposures to organophosphate (OP) pesticides among children, but they have not been collectively evaluated. The aim of the present article is to synthesize reported evidence over the last decade on OP exposure and neurodevelopmental effects in children. The Data Sources were PubMed, Web of Science, EBSCO, SciVerse Scopus, SpringerLink, SciELO and DOAJ. The eligibility criteria considered were studies assessing exposure to OP pesticides and neurodevelopmental effects in children from birth to 18 years of age, published between 2002 and 2012 in English or Spanish. Twenty-seven articles met the eligibility criteria. Studies were rated for evidential consideration as high, intermediate, or low based upon the study design, number of participants, exposure measurement, and neurodevelopmental measures. All but one of the 27 studies evaluated showed some negative effects of pesticides on neurobehavioral development. A positive dose-response relationship between OP exposure and neurodevelopmental outcomes was found in all but one of the 12 studies that assessed dose-response. In the ten longitudinal studies that assessed prenatal exposure to OPs, cognitive deficits (related to working memory) were found in children at age 7 years, behavioral deficits (related to attention) seen mainly in toddlers, and motor deficits (abnormal reflexes) seen mainly in neonates. No meta-analysis was possible due to different measurements of exposure assessment and outcomes. Eleven studies (all longitudinal) were rated high, 14 studies were rated intermediate, and two studies were rated low. Evidence of neurological deficits associated with exposure to OP pesticides in children is growing. The studies reviewed collectively support the hypothesis that exposure to OP pesticides induces neurotoxic effects. Further research is needed to understand effects associated with exposure in critical windows of development.
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Levy, K., K.L. Nelson, A. Hubbard, J.N.S. Eisenberg
Rethinking Indicators of Microbial Drinking Water Quality for Health Studies in Tropical Developing Countries: Case Study in Northern Coastal Ecuador American Journal of Tropical Medicine and Hygiene / 2012. |
To address the problem of the health impacts of unsafe drinking water, methods are needed to assess micro- biologic contamination in water. However, indicators of water quality have provided mixed results. We evaluate five assays (three for Escherichia coli and one each for enterococci and somatic coliphage) of microbial contamination in vil- lages in rural Ecuador that rely mostly on untreated drinking water. Only membrane filtration for E. coli using mI agar detected a significant association with household diarrheal disease outcome (odds ratio = 1.29, 95% confidence interval = 1.02–1.65 in household containers and odds ratio = 1.18, 95% confidence interval = 1.02–1.37) in source samples. Our analysis and other published research points to the need for further consideration of study design factors, such as sample size and variability in measurements, when using indicator organisms, especially when relating water quality exposure to health outcomes. Although indicator organisms are used extensively in health studies, we argue that their use requires a full understanding of their purposes and limitations.
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Muñoz-Quezada, M.T., V. Iglesias, B. Lucero, K. Steenland, D.B. Barr, K. Levy, P.B. Ryan, S. Alvarado, C. Concha
Predictors of exposure to organophosphate pesticides in schoolchildren in the Province of Talca, Chile Environment International / 2012. |
Background: Few data exist in Latin America concerning the association between organophosphate (OP) urinary metabolites and the consumption of fruits and vegetables and other exposure risk variables in schoolchildren. Methods: We collected samples of urine from 190 Chilean children aged 6–12 years, fruits and vegetables, water and soil from schools and homes, and sociodemographic data through a questionnaire. We measured urinary dialkylphosphate (DAP) OP metabolites and OP pesticide residues in food consumed by these 190 children during two seasons: December 2010 (summer) and May 2011 (fall). We analyzed the relationship between urinary DAP concentrations and pesticide residues in food, home pesticide use, and residential location. Results: Diethylalkylphosphates (DEAP) and dimethylalkylphosphates (DMAP) were detected in urine in 76% and 27% of the samples, respectively. Factors associated with urinary DEAP included chlorpyrifos in consumed fruits (p < 0.0001), urinary creatinine (p < 0.0001), rural residence (p = 0.02) and age less than 9 years (p = 0.004). Factors associated with urinary DMAP included the presence of phosmet residues in fruits (p < 0.0001), close proximity to a farm (p = 0.002), home fenitrothion use (p = 0.009), and season (p < 0.0001). Conclusions: Urinary DAP levels in Chilean school children were high compared to previously reported studies. The presence of chlorpyrifos and phosmet residues in fruits was the major factor predicting urinary DAP metabolite concentrations in children.
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Markovitz, A.R., J.E. Goldstick, K. Levy, W. Cevallos, B. Mukherjee, J.A. Trostle, J.N.S. Eisenberg
Where science meets policy: Comparing longitudinal and cross-sectional designs to address diarrheal disease burden in the developing world International Journal of Epidemiology / 2012 |
Background: Longitudinal studies are considered preferable to cross-sectional studies for informing public health policy. However, when resources are limited, the trade-off between an accurate cross-section of the population and an understanding of the temporal variation should be optimized. When risk factors vary more across space at a fixed moment in time than at a fixed location across time, cross-sectional studies will tend to give more precise estimates of risk factor effects and thus may be a better source of data for policy judgments. Methods: We conducted a diarrhoeal disease surveillance of 5616 individuals within 19 Ecuadorian villages. This data set was used to mimic cross-sectional and longitudinal studies by restricting focus to a single week and a single village, respectively. We compared the variability in risk factor effect estimates produced from each type of study. Results: For household risk factors, the effect estimates produced by the longitudinal studies were more variable than their cross-sectional counterparts, which can be explained by greater spatial than temporal variability in the risk factor distribution. For example, the effect estimate of improved sanitation was almost twice as variable in longitudinal studies. Conclusions: In our study, cross-sectional designs yielded more consistent evaluations of diarrhoea disease risk factors when those factors varied more between villages than over time. Cross-sectional studies can provide information that is representative across large geographic regions and therefore can provide insight for local, regional and national policy decisions. The value of the cross-sectional study should be reconsidered in the public health community.
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Levy, K., G. Daily, S.S. Myers
Human Health as an Ecosystem Service: A Conceptual Framework Human Health as an Ecosystem Service, A Conceptual Framework / 2012 |
To live in good health and, in many ways, to live at all, people need a wide array of life-support benefits that derive from ecosystems. Collectively these are called ecosystem services, a term referring to the conditions and processes through which ecosystems, and the species that make them up, sustain and fulfill human life (Ehrlich and Ehrlich 1981; Daily 1997; Millennium Ecosystem Assessment 2005). These processes underpin the production of goods (such as seafood and timber), life-support functions (water purification and flood control), and life-fulfilling conditions (beauty and inspiration), as well as the preservation of options (such as genetic diversity for future use).
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Eisenberg, J.N.S., J. Goldstick, W. Cevallos, G. Trueba, K. Levy, J. Scott, B. Percha, R. Segovia, K. Ponce, A. Hubbard, C. Marrs, B. Foxman, D.L. Smith, J. Trostle
In-roads to the spread of antibiotic resistance: regional patterns of microbial transmission in northern coastal Ecuador Journal of the Royal Society Interface / 2012 |
The evolution of antibiotic resistance (AR) increases treatment cost and probability of failure, threatening human health worldwide. The relative importance of individual antibiotic use, environmental transmission and rates of introduction of resistant bacteria in explaining community AR patterns is poorly understood. Evaluating their relative importance requires studying a region where they vary. The construction of a new road in a previously roadless area of northern coastal Ecuador provides a valuable natural experiment to study how changes in the social and natural environment affect the epidemiology of resistant Escherichia coli. We conducted seven bi-annual 15 day surveys of AR between 2003 and 2008 in 21 villages. Resistance to both ampicillin and sulphamethoxazole was the most frequently observed profile, based on antibiogram tests of seven antibiotics from 2210 samples. The prevalence of enteric bacteria with this resistance pair in the less remote communities was 80 per cent higher than in more remote communities (OR = 1.8 [1.3, 2.3]). This pattern could not be explained with data on individual antibiotic use. We used a transmission model to help explain this observed discrepancy. The model analysis suggests that both transmission and the rate of introduction of resistant bacteria into communities may contribute to the observed regional scale AR patterns, and that village-level antibiotic use rate determines which of these two factors predominate. While usually conceived as a main effect on individual risk, antibiotic use rate is revealed in this analysis as an effect modifier with regard to community-level risk of resistance.
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Levy,K., A.E. Hubbard, J.N.S. Eisenberg
Seasonality of Rotavirus Disease in the Tropics: A Systematic Review and Meta-analysis International Journal of Epidemiology / 2009 |
Background: To date little conclusive evidence exists on the seasonality of rotavirus incidence in the tropics. We present a systematic review and meta-analysis on the seasonal epidemiology of rotavirus in the tropics, including 26 studies reporting continuous monthly rotavirus incidence for which corresponding climatological data was available. Methods: Using linear regression models that account for serial correlation between months, monthly rotavirus incidence was significantly negatively correlated with temperature, rainfall and relative humidity in 65%, 55% and 60% of studies, respectively. We carried out pooled analyses using a generalized estimating equation (GEE) that accounts for correlation from between-study variation and serial correlation between months within a given study. Results: For every 1°C (1.8°F) increase in mean temperature, 1 cm (0.39 in.) increase in mean monthly rainfall, and 1% increase in relative humidity (22%) this analysis showed reductions in rotavirus incidence of 10% (95% CI: 6–13%), 1% (95% CI: 0–1%), and 3% (95% CI:0–5%), respectively. Conclusions: On the basis of the evidence, we conclude that rotavirus responds to changes in climate in the tropics, with the highest number of infections found at the colder and drier times of the year.
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McLaughlin, L.A., K. Levy, N.K. Beck, G. Shin, J.S. Meschke, J.N.S. Eisenberg
An Observational Study on the Effectiveness of Point-of-use Chlorination Journal of Environmental Health / 2009 |
Although the efficacy of chlorine disinfection under controlled laboratory conditions is well known, the effectiveness of chlorine under field point-of-use (POU) conditions is still not clearly understood and may be impacted by a variety of factors. This study evaluated the effectiveness of POU chlorine disinfection in rural Ecuador under typical use conditions and compared this effectiveness with the efficacy in controlled laboratory conditions. While reductions of indicator organisms were slightly higher in households that used chlorination, no significant differences were seen between households employing POU chlorination and the households with no chlorination (1–1.5 log10 median reductions for chlorinating households and 0.31–0.55 log10 for nonchlorinating households, depending on the indicator organism). In contrast, significant reduction of all test organisms was found when simulating POU conditions in the laboratory. This study demonstrates that POU chlorination can be considerably less effective under actual field conditions than would be predicted based on its laboratory efficacy (3–5 log10 median reductions for chlorinated and 0–0.3 log10 for non-chlorinated samples). Human factors (including improper storage and chlorine dosing) and uncontrolled water quality effects are hypothesized to impact significantly the effectiveness of chlorine disinfection.
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Levy, K., A.E. Hubbard, K.L. Nelson, J.N.S. Eisenberg
Drivers of water quality variability in northern coastal Ecuador Environmental Science & Technology / 2009 |
Microbiological safety of water is commonly measured using indicator organisms, but the spatiotemporal variability of these indicators can make interpretation of data difficult. Here, we systematically explore the variability in Escherichia coli concentrations in surface source and household drinking water in a rural Ecuadorian village over one year. We observed more variability in water quality on an hourly basis (up to 2.4 log difference) than on a daily (2.2 log difference) or weekly basis (up to 1.8 log difference). E. coli counts were higher in the wet season than in the dry season for source (0.42 log difference, p < 0.0001) and household (0.11 log difference, p = 0.077) samples. In the wet season, a 1 cm increase in weekly rainfall was associated with a 3% decrease (p = 0.006) in E. coli counts in source samples and a 6% decrease (p = 0.012) in household samples. Each additional person in the river when source samples were collected was associated with a 4% increase (p = 0.026) in E. coli counts in the wet season. Factors affecting household water quality included rainfall, water source, and covering the container. The variability can be understood as a combination of environmental (e.g., seasonal and soil processes) and other drivers (e.g., human river use, water practices, and sanitation), each working at different time scales
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Levy, K., K.L. Nelson, A. Hubbard, J.N.S. Eisenberg
Following the water: a controlled study of drinking water storage in northern coastal Ecuador Environmental Health Perspectives / 2008 |
Background: To design the most appropriate interventions to improve water quality and supply, information is needed to assess water contamination in a variety of community settings, including those that rely primarily on unimproved surface sources of drinking water. Objectives: We explored the role of initial source water conditions as well as household factors in determining household water quality, and how levels of contamination of drinking water change over time, in a rural setting in northern coastal Ecuador. Methods: We sampled source waters concurrently with water collection by household members and followed this water over time, comparing Escherichia coli and enterococci concentrations in water stored in households with water stored under controlled conditions. Results: We observed significant natural attenuation of indicator organisms in control containers and significant, although less pronounced, reductions of indicators between the source of drinking water and its point of use through the third day of sampling. These reductions were followed by recontamination in approximately half of the households. Conclusions: Water quality improved after water was transferred from the source to household storage containers, but then declined because of recontamination in the home. Our experimental design allowed us to observe these dynamics by controlling for initial source water quality and following changes in water quality over time. These data, because of our controlled experimental design, may explain why recontamination has been reported in the literature as less prominent in areas or households with highly contaminated source waters. Our results also suggest that efforts to improve source water quality and sanitation remain important.
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Eisenberg, J.N.S., M.A. Desai, K. Levy, S.J. Bates, S. Liang, K. Naumoff, J.C. Scott
Environmental determinants of infectious disease: a framework for tracking causal links and guiding public health research Environmental Health Perspectives / 2007 |
Background: Discoveries that emerging and re-emerging pathogens have their origin in environmental change has created an urgent need to understand how these environmental changes impact disease burden. In this article we present a framework that provides a context from which to examine the relationship between environmental changes and disease transmission and a structure from which to unite disparate pieces of information from a variety of disciplines. Methods: The framework integrates three interrelated characteristics of environment–disease relationships: a) Environmental change manifests in a complex web of ecologic and social factors that may ultimately impact disease; these factors are represented as those more distally related and those more proximally related to disease. b) Transmission dynamics of infectious pathogens mediate the effects that environmental changes have on disease. c) Disease burden is the outcome of the interplay between environmental change and the transmission cycle of a pathogen. Results: To put this framework into operation, we present a matrix formulation as a means to define important elements of this system and to summarize what is known and unknown about the these elements and their relationships. The framework explicitly expresses the problem at a systems level that goes beyond the traditional risk factor analysis used in public health, and the matrix provides a means to explicitly express the coupling of different system components. Conclusion: This coupling of environmental and disease transmission processes provides a much-needed construct for furthering our understanding of both specific and general relationships between environmental change and infectious disease
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Eisenberg, J.N.S., W. Cevallos, K. Ponce, K. Levy, S.J. Bates, J.C. Scott, A. Hubbard, N. Vieira, P. Endara, M. Espinel, G. Trueba, L.W. Riley, J. Trostle
Environmental change and infectious disease: how new roads affect the transmission of diarrheal pathogens in rural Ecuador Proceedings of the National Academy of the Sciences / 2006 |
Environmental change plays a large role in the emergence of infectious disease. The construction of a new road in a previously roadless area of northern coastal Ecuador provides a valuable natural experiment to examine how changes in the social and natural environment, mediated by road construction, affect the epidemiology of diarrheal diseases. Twenty-one villages were randomly selected to capture the full distribution of village population size and distance from a main road (remoteness), and these were compared with the major population center of the region, Borbón, that lies on the road. Estimates of enteric pathogen infection rates were obtained from case-control studies at the village level. Higher rates of infection were found in nonremote vs. remote villages [pathogenic Escherichia coli: odds ratio (OR) = 8.4, confidence interval (CI) 1.6, 43.5; rotavirus: OR = 4.0, CI 1.3, 12.1; and Giardia: OR = 1.9, CI 1.3, 2.7]. Higher rates of all-cause diarrhea were found in Borbón compared with the 21 villages (RR = 2.0, CI 1.5, 2.8), as well as when comparing nonremote and remote villages (OR = 2.7, CI 1.5, 4.8). Social network data collected in parallel offered a causal link between remoteness and disease. The significant and consistent trends across viral, bacterial, and protozoan pathogens suggest the importance of considering a broad range of pathogens with differing epidemiological patterns when assessing the environmental impact of new roads. This study provides insight into the initial health impacts that roads have on communities and into the social and environmental processes that create these impacts.
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Levy, K.
Neglected consequences: role of introduced aquatic species in the spread of infectious diseases EcoHealth / 2004 |
Introduction of aquatic organisms to new ecosystems has led to massive alterations to the structure and function of natural ecosystems, and to extinction of native flora and fauna. The ecological impacts caused by exotic aquatic species worldwide have been widely recognized, but the past and potential human health impacts of these introductions have been largely ignored. This review identifies several modes by which introduced aquatic species negatively impact human health: a) the direct introduction of human pathogens and/or their hosts; b) the introduction of pathogens of species upon which humans depend; and c) structural and functional alterations of ecosystems that affect other aquatic species upon which humans depend. The literature review presented here focuses on the first of these modes, presenting examples of either pathogens or hosts of pathogens (or both) that are documented to have been introduced, and that either affect or have the potential to affect human health, and occur in aquatic environments. Documented or suspected cases of introduced species that have caused human health impacts include: a) introduced dinoflagellates, which cause the accumulation of human neurotoxins in shellfish; b) various species of freshwater snails hosting a variety of human disease organisms, includingSchistosoma mansoni (the cause of intestinal schistosomiasis), schistosomes that cause “swimmer’s itch” (cercarial dermatitis), the liver fluke Fasciola hepatica, and others; c) Vibrio cholerae, the agent of infection of cholera disease; and d) introduced mitten crabs, which can carry a human lung fluke.
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Levy, K., T.F. Young, R.M. Fujita, D.J. Rapport, W.L. Lasley, D.E. Rolston, N.O. Nielsen, C.O. Qualset, A.B. Damania
A conceptual framework for choosing indicators of ecological integrity: case study of the San Francisco Bay-Delta-River system. Managing for Health Ecosystems / 2003 |
This chapter addresses the challenge of operationalizing the emerging paradigm of ecosystem management, using a case study of the San Francisco-Delta-River system, California, USA, as an illustration. A methodology is proposed to implement part of this challenge - describing a large system in order to evaluate its overall health or sustainable ecological integrity - and report on the experience of the case study. Issues pertaining to the decision-making process involved, specifically the attempt to achieve broad stakeholder consensus on scientific ideas are discussed
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