Anna M. Stewart-Ibarra

Climate and Non-Climate Drivers of Dengue Epidemics in Southern Coastal Ecuador

We report a statistical mixed model for assessing the importance of climate and non-climate drivers of interannual variability in dengue fever in southern coastal Ecuador. Local climate data and Pacific sea surface temperatures (Oceanic Niño Index [ONI]) were used to predict dengue standardized morbidity ratios (SMRs; 1995-2010). Unobserved confounding factors were accounted for using non-structured yearly random effects. We found that ONI, rainfall, and minimum temperature were positively associated with dengue, with more cases of dengue during El Niño events. We assessed the influence of non-climatic factors on dengue SMR using a subset of data (2001-2010) and found that the percent of households with Aedes aegypti immatures was also a significant predictor. Our results indicate that monitoring the climate and non-climate drivers identified in this study could provide some predictive lead for forecasting dengue epidemics, showing the potential to develop a dengue early-warning system in this region.

Spatiotemporal clustering, climate periodicity, and social-ecological risk factors for dengue during an outbreak in Machala, Ecuador, in 2010

BackgroundDengue fever, a mosquito-borne viral disease, is a rapidly emerging public health problem in Ecuador and throughout the tropics. However, we have a limited understanding of the disease transmission dynamics in these regions. Previous studies in southern coastal Ecuador have demonstrated the potential to develop a dengue early warning system (EWS) that incorporates climate and non-climate information. The objective of this study was to characterize the spatiotemporal dynamics and climatic and social-ecological risk factors associated with the largest dengue epidemic to date in Machala, Ecuador, to inform the development of a dengue EWS.MethodsThe following data from Machala were included in analyses: neighborhood-level georeferenced dengue cases, national census data, and entomological surveillance data from 2010; and time series of weekly dengue cases (aggregated to the city-level) and meteorological data from 2003 to 2012. We applied LISA and Moran’s I to analyze the spatial distribution of the 2010 dengue cases, and developed multivariate logistic regression models through a multi-model selection process to identify census variables and entomological covariates associated with the presence of dengue at the neighborhood level. Using data aggregated at the city-level, we conducted a time-series (wavelet) analysis of weekly climate and dengue incidence (2003-2012) to identify significant time periods (e.g., annual, biannual) when climate co-varied with dengue, and to describe the climate conditions associated with the 2010 outbreak.ResultsWe found significant hotspots of dengue transmission near the center of Machala. The best-fit model to predict the presence of dengue included older age and female gender of the head of the household, greater access to piped water in the home, poor housing condition, and less distance to the central hospital. Wavelet analyses revealed that dengue transmission co-varied with rainfall and minimum temperature at annual and biannual cycles, and we found that anomalously high rainfall and temperatures were associated with the 2010 outbreak.ConclusionsOur findings highlight the importance of geospatial information in dengue surveillance and the potential to develop a climate-driven spatiotemporal prediction model to inform disease prevention and control interventions. This study provides an operational methodological framework that can be applied to understand the drivers of local dengue risk.

A global map of suitability for coastal Vibrio cholerae under current and future climate conditions.

Vibrio cholerae is a globally distributed water-borne pathogen that causes severe diarrheal disease and mortality, with current outbreaks as part of the seventh pandemic. Further understanding of the role of environmental factors in potential pathogen distribution and corresponding V. cholerae disease transmission over time and space is urgently needed to target surveillance of cholera and other climate and water-sensitive diseases. We used an ecological niche model (ENM) to identify environmental variables associated with V. cholerae presence in marine environments, to project a global model of V. cholerae distribution in ocean waters under current and future climate scenarios. We generated an ENM using published reports of V. cholerae in seawater and freely available remotely sensed imagery. Models indicated that factors associated with V. cholerae presence included chlorophyll-a, pH, and sea surface temperature (SST), with chlorophyll-a demonstrating the greatest explanatory power from variables selected for model calibration. We identified specific geographic areas for potential V. cholerae distribution. Coastal Bangladesh, where cholera is endemic, was found to be environmentally similar to coastal areas in Latin America. In a conservative climate change scenario, we observed a predicted increase in areas with environmental conditions suitable for V. cholerae. Findings highlight the potential for vulnerability maps to inform cholera surveillance, early warning systems, and disease prevention and control.

Could the Recent Zika Epidemic Have Been Predicted

Given knowledge at the time, the recent 2015–2016 zika virus (ZIKV) epidemic probably could not have been predicted. Without the prior knowledge of ZIKV being already present in South America, and given the lack of understanding of key epidemiologic processes and long-term records of ZIKV cases in the continent, the best related prediction could be carried out for the potential risk of a generic Aedes-borne disease epidemic. Here we use a recently published two-vector basic reproduction number model to assess the predictability of the conditions conducive to epidemics of diseases like zika, chikungunya, or dengue, transmitted by the independent or concurrent presence of Aedes aegypti and Aedes albopictus. We compare the potential risk of transmission forcing the model with the observed climate and with state-of-the-art operational forecasts from the North American Multi Model Ensemble (NMME), finding that the predictive skill of this new seasonal forecast system is highest for multiple countries in Latin America and the Caribbean during the December-February and March-May seasons, and slightly lower—but still of potential use to decision-makers—for the rest of the year. In particular, we find that above-normal suitable conditions for the occurrence of the zika epidemic at the beginning of 2015 could have been successfully predicted at least 1 month in advance for several zika hotspots, and in particular for Northeast Brazil: the heart of the epidemic. Nonetheless, the initiation and spread of an epidemic depends on the effect of multiple factors beyond climate conditions, and thus this type of approach must be considered as a guide and not as a formal predictive tool of vector-borne epidemics.

Climate services for health: predicting the evolution of the 2016 dengue season in Machala, Ecuador

BACKGROUND El Niño and its effect on local meteorological conditions potentially influences interannual variability in dengue transmission in southern coastal Ecuador. El Oro province is a key dengue surveillance site, due to the high burden of dengue, seasonal transmission, co-circulation of all four dengue serotypes, and the recent introduction of chikungunya and Zika. In this study, we used climate forecasts to predict the evolution of the 2016 dengue season in the city of Machala, following one of the strongest El Niño events on record. METHODS We incorporated precipitation, minimum temperature, and Niño3·4 index forecasts in a Bayesian hierarchical mixed model to predict dengue incidence. The model was initiated on Jan 1, 2016, producing monthly dengue forecasts until November, 2016. We accounted for misreporting of dengue due to the introduction of chikungunya in 2015, by using active surveillance data to correct reported dengue case data from passive surveillance records. We then evaluated the forecast retrospectively with available epidemiological information. FINDINGS The predictions correctly forecast an early peak in dengue incidence in March, 2016, with a 90% chance of exceeding the mean dengue incidence for the previous 5 years. Accounting for the proportion of chikungunya cases that had been incorrectly recorded as dengue in 2015 improved the prediction of the magnitude of dengue incidence in 2016. INTERPRETATION This dengue prediction framework, which uses seasonal climate and El Niño forecasts, allows a prediction to be made at the start of the year for the entire dengue season. Combining active surveillance data with routine dengue reports improved not only model fit and performance, but also the accuracy of benchmark estimates based on historical seasonal averages. This study advances the state-of-the-art of climate services for the health sector, by showing the potential value of incorporating climate information in the public health decision-making process in Ecuador. FUNDING European Union FP7, Royal Society, and National Science Foundation.

Household Dengue Prevention Interventions, Expenditures, and Barriers to Aedes aegypti Control in Machala, Ecuador

The Aedes aegypti mosquito is an efficient vector for the transmission of Zika, chikungunya, and dengue viruses, causing major epidemics and a significant social and economic burden throughout the tropics and subtropics. The primary means of preventing these diseases is household-level mosquito control. However, relatively little is known about the economic burden of Ae. aegypti control in resource-limited communities. We surveyed residents from 40 households in a high-risk community at the urban periphery in the city of Machala, Ecuador, on dengue perceptions, vector control interventions, household expenditures, and factors influencing purchasing decisions. The results of this study show that households spend a monthly median of US

Rabies Epidemiology and Control in Ecuador

2.00, or 1.90% (range: 0.00%, 9.21%) of their family income on Ae. aegypti control interventions. Households reported employing, on average, five different mosquito control and dengue prevention interventions, including aerosols, liquid sprays, repellents, mosquito coils, and unimpregnated bed nets. We found that effectiveness and cost were the most important factors that influence people’s decisions to purchase a mosquito control product. Our findings will inform the development and deployment of new Ae. aegypti control interventions by the public health and private sectors, and add to prior studies that have focused on the economic burden of dengue-like illness.

The Social and Spatial Ecology of Dengue Presence and Burden during an Outbreak in Guayaquil, Ecuador, 2012

Objective: Describe the epidemiology and the control effort for rabies in Ecuador. Methods: This observational study included data from the Ecuadorian National Institute of Census and Statistics (INEC), and mortality and morbidity data reported by the Ministry of Public Health and the National Institute for Social Security. We conducted a phylogeny analyses to compare the N gene from the Challenge Virus Standard (CVS) vaccine strain used in Ecuador with published Cosmopolitan, Asian and Sylvatic strains. Descriptive and inferential statistics were used to determine the significance of the data. Results: In 1996 Ecuador suffered the highest rate of rabies per capita in the Americas, with an incidence rate of 0.56 cases per 100 000 people per year. Human and canine rabies showed a sharp decline until 2012. Between 1994 and 2014, we found a correlation of 0.925 (p<0.01) between annual cases of dog and human rabies. In 2011, there was an epidemic of sylvatic rabies transmitted to people by vampire bats (Desmodus rotundus) in the Amazon region, specifically in Morona Santiago, leading to 11 fatalities. Phylogenetic analyses of the CVS vaccine N gene showed an association with urban canine rabies strains (the Cosmopolitan lineage and Asian strains), whereas sylvatic rabies, like those reported in the Amazon region, were found to be grouped in a different clade represented mainly by bat-derived strains. Conclusions: This study presents the first compilation of epidemiological data on rabies in Ecuador. The incidence of human and canine rabies, also known as urban rabies, has clearly decreased due to massive canine vaccination campaigns. Phylogenetic analysis of the prevailing vaccine used in the country showed a clear separation from bat-derived rabies, the source of recent rabies outbreaks. Efforts are ongoing to develop rabies vaccines that are highly specific to the rabies virus genotype circulating in the region, including sylvatic rabies. These efforts include the implementation of reverse genetics to generate recombinant virus coding for the prevailing glycoprotein gene.

The high burden of dengue and chikungunya in southern coastal Ecuador: Epidemiology, clinical presentation, and phylogenetics from a prospective study in Machala in 2014 and 2015

Dengue fever, a mosquito-borne arbovirus, is a major public health concern in Ecuador. In this study, we aimed to describe the spatial distribution of dengue risk and identify local social-ecological factors associated with an outbreak of dengue fever in the city of Guayaquil, Ecuador. We examined georeferenced dengue cases (n = 4248) and block-level census data variables to identify social-ecological risk factors associated with the presence/absence and burden of dengue in Guayaquil in 2012. Local Indicators of Spatial Association (LISA), specifically Anselin’s Local Moran’s I, and Moran’s I tests were used to locate hotspots of dengue transmission, and multimodel selection was used to identify covariates associated with dengue presence and burden at the census block level. We identified significant dengue transmission hotspots near the North Central and Southern portions of Guayaquil. Significant risk factors for presence of dengue included poor housing conditions, access to paved roads, and receipt of remittances. Counterintuitive positive correlations with dengue presence were observed with several municipal services such as garbage collection and access to piped water. Risk factors for increased burden of dengue included poor housing conditions, garbage collection, receipt of remittances, and sharing a property with more than one household. Social factors such as education and household demographics were negatively correlated with increased dengue burden. These findings elucidate underlying differences with dengue presence versus burden, and suggest that vulnerability and risk maps could be developed to inform dengue prevention and control; this is information that is also relevant for emerging epidemics of chikungunya and Zika viruses.

Climate Variability, Vulnerability, and Natural Disasters: A Case Study of Zika Virus in Manabi, Ecuador Following the 2016 Earthquake

Background Dengue (DENV), chikugunya (CHIKV) and zika (ZIKV) viruses are arboviruses transmitted by the Ae. aegypti mosquito, that cause febrile illness and present a major public health challenge in tropical low– and middle-income countries such as Ecuador. Here we report the methods and findings from the first two years (January 1, 2014 to December 31, 2015) of an active and passive surveillance study conducted in the southern coastal city of Machala, Ecuador. Methods Individuals whom presented at one of four sentinel clinics or the central hospital of the Ministry of Health with suspected DENV (index cases) were recruited into the study (n = 324). Index cases with confirmed acute DENV infection triggered a cluster investigation (n = 44) of DENV infections in the index household and four neighboring households (associates) within 200 meters, (n = 397). We conducted genomic sequencing and phylogenetic analysis of select DENV positive samples from 2014. Results In 2014, 72.5% of index patients and 35.6% of associates had evidence of acute or recent DENV infections. In 2015, 28.3% and 12.85% of index patients and associates, respectively, had acute or recent infections. The first cases of CHIKV were detected in an associate on epidemiological week 12 in 2015. There were a total of 54 cases of acute CHIKV infections, including seven DENV/CHIKV co-infections. No cases of ZIKV were detected. DENV symptoms varied significantly by age and by primary versus secondary infections. Symptoms that were associated with DENV and CHIKV infections are presented. Phylogenetic analyses of isolates revealed genetic relatedness and shared ancestry of DENV1, DENV2 and DENV4 genomes from Ecuador with those from Venezuela and Colombia, as well as more than one introduction of the same serotype into Ecuador, indicating presence of viral flow between Ecuador and the surrounding countries. Discussion Findings from this study highlight the importance of (1) implementing rapid active surveillance protocols and (2) strengthening local molecular diagnostic capacities in resource-limited settings where DENV, CHIKV, and ZIKV co-circulate.