Characterizing dengue transmission in rural areas: A systematic review.

Dengue has historically been considered an urban disease associated with dense human populations and the built environment. Recently, studies suggest increasing dengue virus (DENV) transmission in rural populations. It is unclear whether these reports reflect recent spread into rural areas or ongoing transmission that was previously unnoticed, and what mechanisms are driving this rural transmission. We conducted a systematic review to synthesize research on dengue in rural areas and apply this knowledge to summarize aspects of rurality used in current epidemiological studies of DENV transmission given changing and mixed environments. We described how authors defined rurality and how they defined mechanisms for rural dengue transmission. We systematically searched PubMed, Web of Science, and Embase for articles evaluating dengue prevalence or cumulative incidence in rural areas. A total of 106 articles published between 1958 and 2021 met our inclusion criteria. Overall, 56% (n = 22) of the 48 estimates that compared urban and rural settings reported rural dengue incidence as being as high or higher than in urban locations. In some rural areas, the force of infection appears to be increasing over time, as measured by increasing seroprevalence in children and thus likely decreasing age of first infection, suggesting that rural dengue transmission may be a relatively recent phenomenon. Authors characterized rural locations by many different factors, including population density and size, environmental and land use characteristics, and by comparing their context to urban areas. Hypothesized mechanisms for rural dengue transmission included travel, population size, urban infrastructure, vector and environmental factors, among other mechanisms. Strengthening our understanding of the relationship between rurality and dengue will require a more nuanced definition of rurality from the perspective of DENV transmission. Future studies should focus on characterizing details of study locations based on their environmental features, exposure histories, and movement dynamics to identify characteristics that may influence dengue transmission.

The importance of community during rapid development: The influence of social networks on acute gastrointestinal illness in rural Ecuador.

Social networks are often measured as conduits of infection. Our prior cross-sectional analyses found that denser social ties among individuals reduces transmission of acute gastrointestinal illness (AGI) in coastal Ecuador; social networks can describe both risk and protection. We extend findings to examine how social connectedness influences AGI longitudinally in Ecuador from 2007 to 2013, a time of rapid development, using a two-stage Bayesian hierarchical model to estimate multiple network effects. A larger community network of people to discuss important matters with was consistently protective against AGI over time, and a network defined by people passing time together became a stronger measure of risk, due to increasing population density and travel. These networks were interdependent: the joint effect of having a small passing time network and large important matters network reduced the odds of AGI over time (2007: OR 1.16 (95% CI: 0.94, 1.44), 2013: OR 0.56 (95% CI: 0.45, 0.71)); and synergistic: the people an individual passed time with became the people they discussed important matters with. Focus groups emphasized that with greater remoteness came greater community cohesion resulting in safer WASH practices. Social networks can enhance and reduce health differently as social infrastructure evolves, highlighting the importance of community-level factors in a period of rapid development.

A dengue outbreak in a rural community in Northern Coastal Ecuador: An analysis using unmanned aerial vehicle mapping.

Dengue is recognized as a major health issue in large urban tropical cities but is also observed in rural areas. In these environments, physical characteristics of the landscape and sociodemographic factors may influence vector populations at small geographic scales, while prior immunity to the four dengue virus serotypes affects incidence. In 2019, a rural northwestern Ecuadorian community, only accessible by river, experienced a dengue outbreak. The village is 2-3 hours by boat away from the nearest population center and comprises both Afro-Ecuadorian and Indigenous Chachi households. We used multiple data streams to examine spatial risk factors associated with this outbreak, combining maps collected with an unmanned aerial vehicle (UAV), an entomological survey, a community census, and active surveillance of febrile cases. We mapped visible water containers seen in UAV images and calculated both the green-red vegetation index (GRVI) and household proximity to public spaces like schools and meeting areas. To identify risk factors for symptomatic dengue infection, we used mixed-effect logistic regression models to account for the clustering of symptomatic cases within households. We identified 55 dengue cases (9.5% of the population) from 37 households. Cases peaked in June and continued through October. Rural spatial organization helped to explain disease risk. Afro-Ecuadorian (versus Indigenous) households experience more symptomatic dengue (OR = 3.0, 95%CI: 1.3, 6.9). This association was explained by differences in vegetation (measured by GRVI) near the household (OR: 11.3 95% 0.38, 38.0) and proximity to the football field (OR: 13.9, 95% 4.0, 48.4). The integration of UAV mapping with other data streams adds to our understanding of these dynamics.

"Chicken dumping": Motivations and perceptions in shifting poultry production practices.

Non-governmental organizations (NGOs) often implement overseas development aid through intensive small-scale animal agriculture to alleviate food insecurity in low- and middle-income countries. Intensive animal farming can pose unclear outcomes to households engaged in the practice because of the reliance on industrial animal breeds that are reared with antibiotics and raised in higher densities compared to traditional scavenging husbandry systems. As a result, intensive small-scale farming operations that lack proper infrastructure, training, and financial resources could facilitate the spread of antimicrobial resistance and infectious diseases. We applied a mixed-methods framework towards analyzing the effectiveness of small-scale broiler chicken farming in northern Ecuador. First, from May 2016 - May 2017, our observational surveys indicated that intensive small-scale poultry farming follows a boom-and-bust cycle that is extremely vulnerable to environmental stressors. Second, in May 2016, we followed a cohort of households enrolled in a poultry development project led by an NGO. We observed a substantial decline in chicken survivorship from Survey period 1 to 2 (mean chicken count decrease from 50 to 35 corresponding to a 70% survivorship) and from Survey period 2 to 3 (mean chicken count decrease from 35 to 20.3 corresponding to a 58% survivorship). Heads of households were self-reporting broiler chicken survivorship substantially higher than our recorded observations during survey period two (46 compared to 35 respectively) and three (44.3 compared to 20.3 respectively). We speculate that if households continue to inaccurately report poultry demographics, then it could perpetuate a negative feedback loop where NGOs continue to conduct the same intervention practices without receiving accurate outcome metrics. Third, we used semi-structured questionnaires to determine that access to financial resources was the major motivation for determining when to farm broiler chickens. Intensive small-scale poultry farming can be unreliable and disease-enhancing, yet also associated with dubious self-reports of success.

Mass Gatherings and Diarrheal Disease Transmission Among Rural Communities in Coastal Ecuador.

Mass gatherings exacerbate infectious disease risks by creating crowded, high-contact conditions and straining the capacity of local infrastructure. While mass gatherings have been extensively studied in the context of epidemic disease transmission, the role of gatherings in incidence of high-burden, endemic infections has not been previously studied. Here, we examine diarrheal incidence among 17 communities in Esmeraldas, Ecuador, in relation to recurrent gatherings characterized using ethnographic data collected during and after the epidemiologic surveillance period (2004-2007). Using distributed-lag generalized estimating equations, adjusted for seasonality, trend, and heavy rainfall events, we found significant increases in diarrhea risk in host villages, peaking 2 weeks after an event's conclusion (incidence rate ratio, 1.21; confidence interval, adjusted for false coverage rate of ≤0.05: 1.02, 1.43). Stratified analysis revealed heightened risks associated with events where crowding and travel were most likely (2-week-lag incidence rate ratio, 1.51; confidence interval, adjusted for false coverage rate of ≤0.05: 1.09, 2.10). Our findings suggest that community-scale mass gatherings might play an important role in endemic diarrheal disease transmission and could be an important focus for interventions to improve community health in low-resource settings.

Writing Assignments in Epidemiology Courses: How Many and How Good?

OBJECTIVES: Schools and programs of public health are concerned about poor student writing. We determined the proportion of epidemiology courses that required writing assignments and the presence of 6 characteristics of these assignments. METHODS: We requested syllabi, writing assignments, and grading criteria from instructors of graduate and undergraduate epidemiology courses taught during 2016 or 2017. We assessed the extent to which these assignments incorporated 6 characteristics of effective writing assignments: (1) a description of the purpose of the writing or learning goals of the assignment, (2) a document type (eg, article, grant) used in public health, (3) an identified target audience, (4) incorporation of tasks that support the writing process (eg, revision), (5) a topic related to a public health problem that requires critical thinking (1-5 scale, 5 = most authentic), and (6) clear assignment expectations (1-5 scale, 5 = clearest). RESULTS: We contacted 594 instructors from 58 institutions and received at least some evaluable materials from 59 courses at 28 institutions. Of these, 47 of 53 (89%) courses required some writing. The purpose was adequately described in 11 of 36 assignments, the required document type was appropriate in 19 of 43 assignments, an audience was identified in 6 of 37 assignments, and tasks that supported a writing process were incorporated in 19 of 40 assignments. Median (interquartile range) scores were 5 (1-5) for an authentic problem that required critical thinking and 4 (2-5) for clarity of expectations. CONCLUSIONS: The characteristics of writing assignments in public health programs do not reflect best practices in writing instruction and should be improved.

Determinants of Latrine Use Behavior: The Psychosocial Proxies of Individual-Level Defecation Practices in Rural Coastal Ecuador.

There is increasing appreciation that latrine access does not imply use-many individuals who own latrines do not consistently use them. Little is known, however, about the determinants of latrine use, particularly among those with variable defecation behaviors. Using the integrated behavior model of water, sanitation, and hygiene framework, we sought to characterize determinants of latrine use in rural Ecuador. We interviewed 197 adults living in three communities with a survey consisting of 70 psychosocial defecation-related questions. Questions were excluded from analysis if responses lacked variability or at least 10% of respondents did not provide a definitive answer. All interviewed individuals had access to a privately owned or shared latrine. We then applied adaptive elastic nets (ENET) and supervised principal component analysis (SPCA) to a reduced dataset of 45 questions among 154 individuals with complete data to select determinants that predict self-reported latrine use. Latrine use was common, but not universal, in the sample (76%). The SPCA model identified six determinants and adaptive ENET selected five determinants. Three indicators were represented in both models-latrine users were more likely to report that their latrine is clean enough to use and also more likely to report daily latrine use; while those reporting that elderly men were not latrine users were less likely to use latrines themselves. Our findings suggest that social norms are important predictors of latrine use, whereas knowledge of the health benefits of sanitation may not be as important. These determinants are informative for promotion of latrine adoption.

Social cohesion and passive adaptation in relation to climate change and disease.

Climate change affects biophysical processes related to the transmission of many infectious diseases, with potentially adverse consequences for the health of communities. While our knowledge of biophysical associations between meteorological factors and disease is steadily improving, our understanding of the social processes that shape adaptation to environmental perturbations lags behind. Using computational modeling methods, we explore the ways in which social cohesion can affect adaptation of disease prevention strategies when communities are exposed to different environmental scenarios that influence transmission pathways for diseases such as diarrhea. We developed an agent-based model in which household agents can choose between two behavioral strategies that offer different levels of protection against environmentally mediated disease transmission. One behavioral strategy is initially set as more protective, leading households to adopt it widely, but its efficacy is sensitive to variable weather conditions and stressors such as floods or droughts that modify the disease transmission system. The efficacy of the second strategy is initially moderate relative to the first and is insensitive to environmental changes. We examined how social cohesion (defined as average number of household social network connections) influences health outcomes when households attempt to identify an optimal strategy by copying the behaviors of socially connected neighbors who seem to have adapted successfully in the past. Our simulation experiments suggest that high-cohesion communities are able to rapidly disseminate the initially optimal behavioral strategy compared to low-cohesion communities. This rapid and pervasive change, however, decreases behavioral diversity; i.e., once a high cohesion community settles on a strategy, most or all households adopt that behavior. Following environmental changes that reduce the efficacy of the initially optimal strategy, rendering it suboptimal relative to the alternative strategy, high-cohesion communities can fail to adapt. As a result, despite faring better early in the course of computational experiments, high-cohesion communities may ultimately experience worse outcomes. In the face of uncertainty in predicting future environmental stressors due to climate change, strategies to improve effective adaptation to optimal disease prevention strategies should balance between intervention efforts that promote protective behaviors based on current scientific understanding and the need to guard against the crystallization of inflexible norms. Developing generalizable models allows us to integrate a wide range of theories multiple datasets pertaining to the relationship between social mechanisms and adaptation, which can provide further understanding of future climate change impacts. Models such as the one we present can generate hypotheses about the mechanisms that underlie the dynamics of adaptation events and suggest specific points of measurement to assess the impact of these mechanisms. They can be incorporated as modules within predictive simulations for specific socio-ecological contexts.

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.

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.

Trends of child undernutrition in rural Ecuadorian communities with differential access to roads, 2004-2013.

Road access can influence protective and risk factors associated with nutrition by affecting various social and biological processes. In northern coastal Ecuador, the construction of new roads created a remoteness gradient among villages, providing a unique opportunity to examine the impact of roads on child nutritional outcomes 10 years after the road was built. Anthropometric and haemoglobin measurements were collected from 2,350 children <5 years in Esmeraldas, Ecuador, from 2004 to 2013 across 28 villages with differing road access. Logistic generalized estimating equation models assessed the longitudinal association between village remoteness and prevalence of stunting, wasting, underweight, overweight, obesity, and anaemia. We examined the influence of socio-economic characteristics on the pathway between remoteness and nutrition by comparing model results with and without household-level socio-economic covariates. Remoteness was associated with stunting (OR = 0.43, 95% CI [0.30, 0.63]) and anaemia (OR = 0.56, 95% CI [0.44, 0.70]). Over time, the prevalence of stunting was generally decreasing but remained higher in villages closer to the road compared to those farther away. Obesity increased (0.5% to 3%) over time; wasting was high (6%) but stable during the study period. Wealth and education partially explained the better nutritional outcomes in remote vs. road villages more than a decade after some communities gained road access. Establishing the extent to which these patterns persist requires additional years of observation.

Determinants of Short-term Movement in a Developing Region and Implications for Disease Transmission.

BACKGROUND: Human mobility is important for infectious disease spread. However, little is known about how travel varies by demographic groups and how this heterogeneity influences infectious disease risk. METHODS: We analyzed 10 years of survey data from 15 communities in a remote but rapidly changing region in rural Ecuador where road development in the past 15-20 years has dramatically changed travel. We identify determinants of travel and incorporate them into an infection transmission model. RESULTS: Individuals living in communities more remote at baseline had lower travel rates compared with less remote villages (adjusted odds ratio [OR] = 0.51; 95% confidence interval [CI] = 0.38, 0.67). Our model predicts that less remote villages are, therefore, at increased disease risk. Though road building and travel increased for all communities, this risk differential remained over 10 years of observation. Our transmission model also suggests that travelers and nontravelers have different roles in disease transmission. Adults travel more than children (adjusted OR = 1.73; 95% CI = 1.30, 2.31) and therefore disseminate infection from population centers to rural communities. Children are more likely than adults to be infected locally (attributable fraction = 0.24 and 0.09, respectively) and were indirectly affected by adult travel patterns. CONCLUSIONS: These results reinforce the importance of large population centers for regional transmission and show that children and adults may play different roles in disease spread. Changing transportation infrastructure and subsequent economic and social transitions are occurring worldwide, potentially causing increased regional risk of disease.

Antibiotic Resistance in Animal and Environmental Samples Associated with Small-Scale Poultry Farming in Northwestern Ecuador.

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. IMPORTANCE In developing countries, small-scale poultry farming employing antibiotics as growth promoters is being advanced as an inexpensive source of protein and income. Here, we present the results of a large ecoepidemiological study examining patterns of antibiotic resistance (AR) in E. coli isolates from small-scale poultry production environments versus domestic environments in rural Ecuador, where such backyard poultry operations have become established over the past decade. Our previous research in the region suggests that introduction of AR bacteria through travel and commerce may be an important source of AR in villages of this region. This report extends the prior analysis by examining small-scale production chicken farming as a potential source of resistant strains. Our results suggest that AR strains associated with poultry production likely originate from sources outside the study area and that these outside sources might be a better place to target control efforts than local management practices.

I get height with a little help from my friends: herd protection from sanitation on child growth in rural Ecuador.

BACKGROUND: Infectious disease interventions, such as vaccines and bed nets, have the potential to provide herd protection to non-recipients. Similarly, improved sanitation in one household may provide community-wide benefits if it reduces contamination in the shared environment. Sanitation at the household level is an important predictor of child growth, but less is known about the effect of sanitation coverage in the community. METHODS: From 2008 to 2013, we took repeated anthropometric measurements on 1314 children under 5 years of age in 24 rural Ecuadorian villages. Using mixed effects regression, we estimated the association between sanitation coverage in surrounding households and child growth. RESULTS: Sanitation coverage in the surrounding households was strongly associated with child height, as those with 100% coverage in their surroundings had a 67% lower prevalence of stunting [prevalence ratio (PR) 0.32, 95% CI 0.15-0.69] compared with those with 0% coverage. Children from households with improved sanitation had a lower prevalence of stunting (PR 0.86, 95% CI 0.64-1.15). When analysing height as a continuous outcome, the protective effect of sanitation coverage is manifested primarily among girls during the second year of life, the time at which growth faltering is most likely to occur. CONCLUSIONS: Our study highlights that a household's sanitation practices can provide herd protection to the overall community. Studies which fail to account for the positive externalities that sanitation provides will underestimate the overall protective effect. Future studies could seek to identify a threshold of sanitation coverage, similar to a herd immunity threshold, to provide coverage and compliance targets.

Effects of selection pressure and genetic association on the relationship between antibiotic resistance and virulence in Escherichia coli.

Antibiotic selection pressure and genetic associations may lead to the cooccurrence of resistance and virulence in individual pathogens. However, there is a lack of rigorous epidemiological evidence that demonstrates the cooccurrence 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) Escherichia coli isolates, classified by the presence or absence of known diarrheagenic virulence factor genes. The prevalences of resistance to single and multiple antibiotics were significantly higher for pathogenic isolates than for commensal isolates. Using a generalized estimating equation, antibiotic resistance was independently associated with virulence factor carriage, case status, and antibiotic use (for these respective factors: odds ratio [OR] = 3.0, with a 95% confidence interval [CI] of 1.7 to 5.1; OR = 2.0, with a 95% CI of 1.3 to 3.0; and OR = 1.5, with a 95% CI of 0.9 to 2.5). 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 cooccurrence of resistance and virulence in E. coli is partially due to antibiotic selection pressure, it is also genetically determined. These findings should be considered in developing strategies for treating infections and controlling for antibiotic resistance.

Ask when--not just whether--it's a risk: How regional context influences local causes of diarrheal disease.

Contemporary epidemiology is enriched when it incorporates ecological concepts about systems and dependencies. With regard to diarrheal disease, the causes of which are many and interacting, the dynamics of within- and between-community disease transmission have distinct components but are also linked in important ways. However, few investigators have studied how regional-scale disease dynamics affect local patterns of diarrheal disease transmission. Characterizing this dependence is important for identifying local- and regional-level transmission pathways. We used data from active surveillance of diarrheal disease prevalence gathered from February 2004 through July 2007 in 21 neighboring Ecuadorian villages to estimate how disease prevalence in spatially and temporally proximate villages modulates the influences of village-level risk and protective factors. We found that the impact of local, village-level interventions such as improved latrines and water treatment can be quite different under conditions of high and low regional disease prevalence. In particular, water treatment was effective only when regional disease prevalence was low, suggesting that person-to-person spread, not waterborne spread, is probably responsible for most between-village transmission in this region. Additional regional-scale data could enhance our understanding of how regional-scale transmission affects local-scale dynamics.

Heavy rainfall events and diarrhea incidence: the role of social and environmental factors.

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.

Transition in the cause of fever from malaria to dengue, Northwestern Ecuador, 1990-2011.

In tropical areas, the predominant cause of fever has historically been malaria. However by 2011, among febrile patients in northwestern Ecuador, dengue was identified in 42% and malaria in none. This finding suggests a transition in the cause of fever from malaria to other illnesses, such as dengue.