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Symposium 17. How Does Having a Vector Matter?

2009; Ecological Society of America; Volume: 91; Issue: 1 Linguagem: Inglês

10.1890/0012-9623-91.1.100

2327-6096

Juliet R. C. Pulliam,

Insect symbiosis and bacterial influences

Symposium 17, “How does having a vector matter? Perspectives on vector biology and disease ecology for prediction and control of emerging diseases,” was organized by Juliet R. C. Pulliam (RAPIDD Program, NIH), F. Ellis McKenzie (RAPIDD Program, NIH), and Andrew P. Dobson (Princeton University), and was held during the 2009 ESA Annual Meeting in Albuquerque, New Mexico, on 6 August. Juliet R. C. Pulliam, RAPIDD Program, Fogarty International Center, National Institutes of Health, “Introductory remarks” David L. Smith, University of Florida, “The buzzing in my ear: mosquito biology and the dynamics of disease transmission” Richard S. Ostfeld, Cary Institute of Ecosystem Studies; Jesse Brunner, SUNY College of Environmental Science and Forestry; Shannon T. K. Duerr, Cary Institute of Ecosystem Studies; Mary Killiea, New York University; Kathleen LoGuidice, Union College; Kenneth Schmidt, Texas Tech University; Holly Vuong, Rutgers University and Cary Institute of Ecosystem Studies; Felicia Keesing, Bard College; “Host communities as regulators of vector abundance and disease transmission” A. Marm Kilpatrick, University of California at Santa Cruz; Juliet R. C. Pulliam, RAPIDD Program, Fogarty International Center, National Institutes of Health; Matt J. Jones, New York State Department of Health; Peter Marra, Smithsonian Migratory Bird Center; Peter Daszak, Wildlife Trust; Laura D. Kramer, Wadsworth Center, New York State Department of Health, and SUNY Albany; “Vector feeding patterns and the transmission of multi-host pathogens” Colleen T. Webb, Colorado State University; “Modeling vector biology to decipher mechanisms of plague maintenance in wild hosts” Mike Levy, Fogarty International Center, National Institutes of Health; Dylan Small, Wharton School, University of Pennsylvania; Daril A. Vilhena, University of Pennsylvania; F. Ellis McKenzie, RAPIDD Program, Fogarty International Center, National Institutes of Health; Juan G. Cornejo del Carpio, Direccion Regional del Minsterio de Salud, Arequipa, Peru; Eleazar Cordova-Benzaquen, Universidad Nacional San Agustin; Robert H. Gilman, Johns Hopkins School of Public Health; Caryn Bern, Centers Symposium 17, “How does having a vector matter? Perspectives on vector biology and disease ecology for prediction and control of emerging diseases,” was organized by Juliet R. C. Pulliam (RAPIDD Program, NIH), F. Ellis McKenzie (RAPIDD Program, NIH), and Andrew P. Dobson (Princeton University), and was held during the 2009 ESA Annual Meeting in Albuquerque, New Mexico, on 6 August. for Disease Control and Prevention; Joshua B. Plotkin, University of Pennsylvania; “Inferring epicenters of vector-borne epidemics from vector biology, with an example of Chagas disease in Peru” Matthew B. Thomas, Pennsylvania State University; Krijn P. Paaijmans, Pennsylvania State University; Simon Blanford, Pennsylvania State University; Andrew F. Read, Pennsylvania State University; “Effects of climate on key entomological parameters determining R0” (CANCELLED) Heather Ferguson, University of Glasgow; “Semifield systems for the study of vector ecology” The theme of this year's ESA meeting was “ecological knowledge and a global sustainable society.” Wildlife, domestic animal, and human health are all essential concerns for building a global sustainable society, and vector-borne pathogens are of particular interest because they provide one of the clearest examples of how environment influences disease patterns, and therefore, how ecological understanding can contribute to public health policy. The goal of this symposium was to emphasize important generalities, differences, and gaps in knowledge across host–vector–pathogen systems, and to highlight avenues for reconciling models and data to produce quantitative frameworks for vector-borne disease control. David Smith began the symposium with an introduction to the history of the field, focusing on the development of mathematical approaches to malaria control. He then described specific entomological influences on malaria dynamics, emphasizing that proper incorporation of vector biology into model formulations is essential for understanding observed relationships between vector density, human density, and malaria prevalence (Dietz and Thomas 1974, Thomson et al. 1994, Hay et al. 2005, Le Menach et al. 2007). Key points included the link between vectorial capacity and mosquito larval biology, rather than human population density. He also discussed the potential of heterogeneous biting to explain observed nonlinearities between entomological inoculation rates and force of infection for malaria in endemic settings (Woolhouse et al. 1997, Smith et al. 2005). Dr. Smith finished by giving an overview of when explicit consideration of vector biology is necessary for understanding dynamics of vector-borne diseases. He concluded that summary measures such as vectorial capacity suffice when questions are focused on large spatial scales (such as for regional planning), when research is focused on host immunity, or when investigating the impact of host-based interventions (such as use of antimalarial drugs). On the other hand, questions focused on transmission, vector-based interventions, design of surveillance systems, or finer-scale assessment of infection risk require that the dynamic nature of vector biology be considered explicitly. The next two talks focused on the role of interactions between vector biology and host community composition in shaping the dynamics of multihost pathogens. Rick Ostfeld began his talk on Lyme disease by emphasizing that factors limiting vector abundance depend crucially on vector biology and vary across vector taxa. He then described the processes by which host community composition gets translated into the density of Borrelia burgdorferi infected nymphs, the primary predictor of human risk for Lyme disease. Using a combination of field and laboratory data, he showed that host species differ in their rates of exposure to larval ticks, proportions of larval ticks encountered that feed successfully, proportions of fed larvae infected by feeding on an infected host (reservoir competence), and proportions of larvae fed that survive the winter to become questing nymphs the following year (Logiudice et al. 2008, Keesing et al. 2009). By considering these factors and taking into account estimates of host densities, Dr. Ostfeld showed that mice, followed by chipmunks and grey squirrels, produce the most infected nymphs at his study site, whereas veeries, catbirds, and opossums contribute relatively few infected nymphs (<10 nymphs/ha); however, because grey squirrels kill or fail to infect the vast majority of larval ticks they encounter, the presence of grey squirrels in the host community actually reduces overall risk. In this sense, grey squirrels are similar to opossums, in that their removal from the host community would be expected to increase the total density of infected nymphs by ~30%. This observation emphasizes that the density of infected ticks can increase even when the total abundance of all hosts is reduced, an observation that contradicts models based on purely density-dependent processes. Removal of mice and chipmunks, on the other hand, would be expected to result in decreased risk, reducing the density of infected nymphs by 75% and 15%, respectively (Keesing et al. 2009). Because opossums and grey squirrels disappear from fragmented landscapes before chipmunks do, and because white-footed mice are the last species to disappear as biodiversity is lost, realistic sequences of species loss result in strongly increasing Lyme disease risk. Dr. Kilpatrick continued the focus on multihost pathogen systems, with an emphasis on vector feeding behavior and the role of host communities in determining infection dynamics of West Nile virus. In particular, he focused on the question of what drives the decline in transmission at the end of the West Nile season each year. To approach this question, he used detailed field data from the Washington, D.C., metropolitan area on host abundance patterns and mosquito abundance and feeding patterns, combined with laboratory data on host competence and vector infectivity, to parameterize a series of transmission models. The models examined incorporated different combinations of three factors that could lead to the decline in transmission at the end of the West Nile season: a build-up of host immunity, and two elements of seasonal patterns in contact between hosts and vectors: changes in mosquito abundance and changes in mosquito feeding patterns from competent to incompetent hosts (Kilpatrick et al. 2006, 2007). Dr. Kilpatrick used these models to examine the effective reproductive number (Re) for infectious mosquitoes throughout the season, and compared observed patterns between models. Based on this analysis, he concluded that the rank importance of the three factors in driving the seasonal decline in West Nile virus prevalence in mosquito populations was: (1) herd immunity among avian hosts, (2) feeding patterns of vectors, and (3) vector abundance. However, the relative importance of these factors could vary depending on the local details of the transmission cycle. The next two talks moved from description and interpretation of community infection dynamics in multihost pathogen systems to discussion of quantitative methodologies for inference regarding infection dynamics. Colleen Webb used dynamical models to address a classical hypothesis regarding the mechanism of plague transmission. By analyzing model sensitivity to three potential transmission mechanisms (classical “blocked” flea transmission, direct transmission between animals, and direct contact with another infectious source), she illustrated that the classical mechanism thought to drive plague transmission, blockage of an infected flea's digestive tract, which causes regurgitation of infectious bacteria when the flea attempts to feed, is insufficient to explain observed plague dynamics in prairie dogs. She illustrated that observed levels and timing of extinction seen in plague-infected prairie dog towns require the existence of a short-term infectious reservoir, such as early-phase (pre-blockage) flea transmission or fomite transmission via contaminated soil or infectious carcasses; however, classical “blocked” flea transmission may play an important role in the early stage of epizootic transmission within a prairie dog town (Webb et al. 2006). Mike Levy's talk focused on methods to illuminate the spatial and temporal origins of vector-borne epidemics. He described a detailed vector-based surveillance protocol used in Arequipa, Peru for the detection of Trypanosoma cruzi, which causes Chagas disease (American trypanosomiasis) (Levy et al. 2006, 2007). He then illustrated how the data collected on vector distribution and infection could be combined with human population and infection data to fit and compare transmission models. Using a technique he calls “epicenter regression,” Dr. Levy showed that Chagas disease is most likely to have been introduced into the study area relatively recently, in a series of microepidemics focused around four or more epicenters. He estimates that nearly half of human infections with T. cruzi in the study area occurred within the five years prior to the initiation of spraying campaigns in 2004, which has important implications for treatment guidelines. Unfortunately, the next talk on the agenda was cancelled. Matt Thomas would have talked about his work combining theory and data to explore the effects of temperature fluctuations on vector-borne disease invasion. His absence left a substantial gap in our program, as temperature is a primary driver of vector population dynamics, and is of particular interest for understanding the potential effects of climate change on pathogen biology; however, a paper describing this work was recently published and the citation was provided to symposium attendees (Paaijmans et al. 2009). In the final talk, Heather Ferguson discussed approaches to data collection for the study of vector dynamics and control. She described the construction of a semi-field system (SFS) for the study of Anopheles dynamics near the Ifakara Health Institute in Tanzania (Ferguson et al. 2008). The SFS provides a self-contained environment for experimental study of vector biology and infection-free vector–host interactions by providing habitat for all stages of the mosquito life-cycle. Studies conducted in the SFS so far have focused on evaluation and comparison of mosquito traps and repellants (Okumu et al. 2009), studies of vector fitness and behavior, and assessment of evolutionary dynamics over multiple mosquito generations. In addition to providing basic insights, all of these studies can be used to parameterize models of mosquito population dynamics and transmission, which can in turn be used to evaluate potential malaria intervention strategies in a variety of settings. In addition to providing an excellent overview of the use of semi-field systems for data collection on vector dynamics, Dr. Ferguson also emphasized several practical aspects of conducting vector studies in malaria endemic locations. First among these is the importance of community engagement. Informing the local population about the work that's being done and how malaria vectors are being handled so that they don't endanger the community is essential to the success of such projects. In addition, SFS construction and use in endemic areas provides an excellent resource for training local scientists who are able to conduct important experiments under the supervision of established leaders in the field. The capacity-building activities Dr. Ferguson described provide an excellent model that could be used in other studies conducted in resource-poor settings. further characterization of and analysis of the importance of heterogeneity, particularly regarding vector feeding patterns, better understanding of the role of density dependence in vector life cycles, validation of predictions regarding expected changes in disease risk following changes in host community structure (such as species introduction or removal), improved understanding of the link between entomological measures of risk (such as mosquito prevalence), and epidemiological measures of risk (such as incidence) further characterization of the role of vector transport in pathogen maintenance and spread, and characterization and implications of the relationship between feeding patterns and the density and diversity of available hosts. Dr. Pulliam is supported in part by the Research and Policy in Infectious Disease Dynamics (RAPIDD) Program of the Science and Technology Directorate, Department of Homeland Security, and Fogarty International Center, National Institutes of Health.