Luis Fernando Chaves

A systematic review of mathematical models of mosquito-borne pathogen transmission: 1970-2010

Mathematical models of mosquito-borne pathogen transmission originated in the early twentieth century to provide insights into how to most effectively combat malaria. The foundations of the Ross–Macdonald theory were established by 1970. Since then, there has been a growing interest in reducing the public health burden of mosquito-borne pathogens and an expanding use of models to guide their control. To assess how theory has changed to confront evolving public health challenges, we compiled a bibliography of 325 publications from 1970 through 2010 that included at least one mathematical model of mosquito-borne pathogen transmission and then used a 79-part questionnaire to classify each of 388 associated models according to its biological assumptions. As a composite measure to interpret the multidimensional results of our survey, we assigned a numerical value to each model that measured its similarity to 15 core assumptions of the Ross–Macdonald model. Although the analysis illustrated a growing acknowledgement of geographical, ecological and epidemiological complexities in modelling transmission, most models during the past 40 years closely resemble the Ross–Macdonald model. Modern theory would benefit from an expansion around the concepts of heterogeneous mosquito biting, poorly mixed mosquito-host encounters, spatial heterogeneity and temporal variation in the transmission process.

Climate Change and Highland Malaria: Fresh Air for a Hot Debate

In recent decades, malaria has become established in zones at the margin of its previous distribution, especially in the highlands of East Africa. Studies in this region have sparked a heated debate over the importance of climate change in the territorial expansion of malaria, where positions range from its neglect to the reification of correlations as causes. Here, we review studies supporting and rebutting the role of climatic change as a driving force for highland invasion by malaria. We assessed the conclusions from both sides of the argument and found that evidence for the role of climate in these dynamics is robust. However, we also argue that over-emphasizing the importance of climate is misleading for setting a research agenda, even one which attempts to understand climate change impacts on emerging malaria patterns. We review alternative drivers for the emergence of this disease and highlight the problems still calling for research if the multidimensional nature of malaria is to be adequately tackled. We also contextualize highland malaria as an ongoing evolutionary process. Finally, we present Schmalhausens law, which explains the lack of resilience in stressed systems, as a biological principle that unifies the importance of climatic and other environmental factors in driving malaria patterns across different spatio-temporal scales.

Local impact of temperature and precipitation on West Nile virus infection in Culex species mosquitoes in northeast Illinois, USA

BackgroundModels of the effects of environmental factors on West Nile virus disease risk have yielded conflicting outcomes. The role of precipitation has been especially difficult to discern from existing studies, due in part to habitat and behavior characteristics of specific vector species and because of differences in the temporal and spatial scales of the published studies. We used spatial and statistical modeling techniques to analyze and forecast fine scale spatial (2000 m grid) and temporal (weekly) patterns of West Nile virus mosquito infection relative to changing weather conditions in the urban landscape of the greater Chicago, Illinois, region for the years from 2004 to 2008.ResultsIncreased air temperature was the strongest temporal predictor of increased infection in Culex pipiens and Culex restuans mosquitoes, with cumulative high temperature differences being a key factor distinguishing years with higher mosquito infection and higher human illness rates from those with lower rates. Drier conditions in the spring followed by wetter conditions just prior to an increase in infection were factors in some but not all years. Overall, 80% of the weekly variation in mosquito infection was explained by prior weather conditions. Spatially, lower precipitation was the most important variable predicting stronger mosquito infection; precipitation and temperature alone could explain the pattern of spatial variability better than could other environmental variables (79% explained in the best model). Variables related to impervious surfaces and elevation differences were of modest importance in the spatial model.ConclusionFinely grained temporal and spatial patterns of precipitation and air temperature have a consistent and significant impact on the timing and location of increased mosquito infection in the northeastern Illinois study area. The use of local weather data at multiple monitoring locations and the integration of mosquito infection data from numerous sources across several years are important to the strength of the models presented. The other spatial environmental factors that tended to be important, including impervious surfaces and elevation measures, would mediate the effect of rainfall on soils and in urban catch basins. Changes in weather patterns with global climate change make it especially important to improve our ability to predict how inter-related local weather and environmental factors affect vectors and vector-borne disease risk.Local impact of temperature and precipitation on West Nile virus infection in Culex species mosquitoes in northeast Illinois, USA.

Shifting patterns: malaria dynamics and rainfall variability in an African highland

The long-term patterns of malaria in the East African highlands typically involve not only a general upward trend in cases but also a dramatic increase in the size of epidemic outbreaks. The role of climate variability in driving epidemic cycles at interannual time scales remains controversial, in part because it has been seen as conflicting with the alternative explanation of purely endogenous cycles exclusively generated by the nonlinear dynamics of the disease. We analyse a long temporal record of monthly cases from 1970 to 2003 in a highland of western Kenya with both a time-series epidemiological model (time-series susceptible–infected–recovered) and a statistical approach specifically developed for non-stationary patterns. Results show that multiyear cycles of malaria outbreaks appear in the 1980s, concomitant with the timing of a regime shift in the dynamics of cases; the cycles become more pronounced in the 1990s, when the coupling between disease and rainfall is also stronger as the variance of rainfall increased at the frequencies of coupling. Disease dynamics and climate forcing play complementary and interacting roles at different temporal scales. Thus, these mechanisms should not be viewed as alternative and their interaction needs to be integrated in the development of future predictive models.

Blood feeding patterns of mosquitoes: random or structured?

BackgroundThe foraging behavior of blood-sucking arthropods is the defining biological event shaping the transmission cycle of vector-borne parasites. It is also a phenomenon that pertains to the realm of community ecology, since blood-feeding patterns of vectors can occur across a community of vertebrate hosts. Although great advances in knowledge of the genetic basis for blood-feeding choices have been reported for selected vector species, little is known about the role of community composition of vertebrate hosts in determining such patterns.Methods & ResultsHere, we present an analysis of feeding patterns of vectors across a variety of locations, looking at foraging patterns of communities of mosquitoes, across communities of hosts primarily comprised of mammals and birds. Using null models of species co-occurrence, which do not require ancillary information about host abundance, we found that blood-feeding patterns were aggregated in studies from multiple sites, but random in studies from a single site. This combination of results supports the idea that mosquito species in a community may rely primarily on host availability in a given landscape, and that contacts with specific hosts will be influenced more by the presence/absence of hosts than by innate mosquito choices. This observation stresses the importance of blood-feeding plasticity as a key trait explaining the emergence of many zoonotic mosquito transmitted diseases.DiscussionFrom an epidemiological perspective our observations support the idea that phenomena promoting synchronization of vectors and hosts can promote the emergence of vector-borne zoonotic diseases, as suggested by observations on the linkages between deforestation and the emergence of several human diseases.

Social exclusion modifies climate and deforestation impacts on a vector-borne disease.

Background The emergence of American Cutaneous Leishmaniasis (ACL) has been associated with changes in the relationship between people and forests, leading to the view that forest ecosystems increase infection risk and subsequent proposal that deforestation could reduce re-emergence of this disease. Methodology/Principal Findings We analyzed county-level incidence rates of ACL in Costa Rica (1996–2000) as a function of social and environmental variables relevant to transmission ecology with statistical models that incorporate breakpoints. Once social marginality was taken into account, the effect of living close to a forest on infection risk was small, and diminished exponentially above a breakpoint. Forest cover was associated with the modulation of temporal effects of El Niño Southern Oscillation (ENSO) at small spatial scales, revealing an additional complex interplay of environmental forces and disease patterns. Conclusions/Significance Social factors, which previously have not been evaluated rigorously together with environmental and climatic factors, appear to play a critical role that may ultimately determine disease risk.

Fine-Scale Variation in Vector Host Use and Force of Infection Drive Localized Patterns of West Nile Virus Transmission

The influence of host diversity on multi-host pathogen transmission and persistence can be confounded by the large number of species and biological interactions that can characterize many transmission systems. For vector-borne pathogens, the composition of host communities has been hypothesized to affect transmission; however, the specific characteristics of host communities that affect transmission remain largely unknown. We tested the hypothesis that vector host use and force of infection (i.e., the summed number of infectious mosquitoes resulting from feeding upon each vertebrate host within a community of hosts), and not simply host diversity or richness, determine local infection rates of West Nile virus (WNV) in mosquito vectors. In suburban Chicago, Illinois, USA, we estimated community force of infection for West Nile virus using data on Culex pipiens mosquito host selection and WNV vertebrate reservoir competence for each host species in multiple residential and semi-natural study sites. We found host community force of infection interacted with avian diversity to influence WNV infection in Culex mosquitoes across the study area. Two avian species, the American robin (Turdus migratorius) and the house sparrow (Passer domesticus), produced 95.8% of the infectious Cx. pipiens mosquitoes and showed a significant positive association with WNV infection in Culex spp. mosquitoes. Therefore, indices of community structure, such as species diversity or richness, may not be reliable indicators of transmission risk at fine spatial scales in vector-borne disease systems. Rather, robust assessment of local transmission risk should incorporate heterogeneity in vector host feeding and variation in vertebrate reservoir competence at the spatial scale of vector-host interaction.

Recasting the theory of mosquito-borne pathogen transmission dynamics and control

Mosquito-borne diseases pose some of the greatest challenges in public health, especially in tropical and sub-tropical regions of the world. Efforts to control these diseases have been underpinned by a theoretical framework developed for malaria by Ross and Macdonald, including models, metrics for measuring transmission, and theory of control that identifies key vulnerabilities in the transmission cycle. That framework, especially Macdonalds formula for R0 and its entomological derivative, vectorial capacity, are now used to study dynamics and design interventions for many mosquito-borne diseases. A systematic review of 388 models published between 1970 and 2010 found that the vast majority adopted the Ross–Macdonald assumption of homogeneous transmission in a well-mixed population. Studies comparing models and data question these assumptions and point to the capacity to model heterogeneous, focal transmission as the most important but relatively unexplored component in current theory. Fine-scale heterogeneity causes transmission dynamics to be nonlinear, and poses problems for modeling, epidemiology and measurement. Novel mathematical approaches show how heterogeneity arises from the biology and the landscape on which the processes of mosquito biting and pathogen transmission unfold. Emerging theory focuses attention on the ecological and social context for mosquito blood feeding, the movement of both hosts and mosquitoes, and the relevant spatial scales for measuring transmission and for modeling dynamics and control.

Host Life History Strategy, Species Diversity, and Habitat Influence Trypanosoma cruzi Vector Infection in Changing Landscapes

Background Anthropogenic land use may influence transmission of multi-host vector-borne pathogens by changing diversity, relative abundance, and community composition of reservoir hosts. These reservoir hosts may have varying competence for vector-borne pathogens depending on species-specific characteristics, such as life history strategy. The objective of this study is to evaluate how anthropogenic land use change influences blood meal species composition and the effects of changing blood meal species composition on the parasite infection rate of the Chagas disease vector Rhodnius pallescens in Panama. Methodology/Principal Findings R. pallescens vectors (N = 643) were collected in different habitat types across a gradient of anthropogenic disturbance. Blood meal species in DNA extracted from these vectors was identified in 243 (40.3%) vectors by amplification and sequencing of a vertebrate-specific fragment of the 12SrRNA gene, and T. cruzi vector infection was determined by pcr. Vector infection rate was significantly greater in deforested habitats as compared to contiguous forests. Forty-two different species of blood meal were identified in R. pallescens, and species composition of blood meals varied across habitat types. Mammals (88.3%) dominated R. pallescens blood meals. Xenarthrans (sloths and tamanduas) were the most frequently identified species in blood meals across all habitat types. A regression tree analysis indicated that blood meal species diversity, host life history strategy (measured as rmax, the maximum intrinsic rate of population increase), and habitat type (forest fragments and peridomiciliary sites) were important determinants of vector infection with T. cruzi. The mean intrinsic rate of increase and the skewness and variability of rmax were positively associated with higher vector infection rate at a site. Conclusions/Significance In this study, anthropogenic landscape disturbance increased vector infection with T. cruzi, potentially by changing host community structure to favor hosts that are short-lived with high reproductive rates. Study results apply to potential environmental management strategies for Chagas disease.

Combined Sewage Overflow Enhances Oviposition of Culex quinquefasciatus (Diptera: Culicidae) in Urban Areas

ABSTRACT Ecosystem changes caused by anthropogenic activities have modified the environment in ways that at times promote the emergence of vector-borne diseases. Here, we study the effects of combined sewage overflows (CSOs) from urban streams in Atlanta, GA, on oviposition site selection by Culex quinquefasciatus under seminatural field conditions. Counting egg rafts was a reliable indicator of oviposition preferences, and CSO water quality, especially when enriched, was a more attractive oviposition substrate than nonenriched water. Therefore, environmentally sound management of municipal waste water systems has the potential to diminish the risk of Culex-borne diseases in urban areas.