Lindsay P. Campbell

Climate Change Influences on Global Distributions of Dengue and Chikungunya Virus Vectors

Numerous recent studies have illuminated global distributions of human cases of dengue and other mosquito-transmitted diseases, yet the potential distributions of key vector species have not been incorporated integrally into those mapping efforts. Projections onto future conditions to illuminate potential distributional shifts in coming decades are similarly lacking, at least outside Europe. This study examined the global potential distributions of Aedes aegypti and Aedes albopictus in relation to climatic variation worldwide to develop ecological niche models that, in turn, allowed anticipation of possible changes in distributional patterns into the future. Results indicated complex global rearrangements of potential distributional areas, which—given the impressive dispersal abilities of these two species—are likely to translate into actual distributional shifts. This exercise also signalled a crucial priority: digitization and sharing of existing distributional data so that models of this sort can be developed more rigorously, as present availability of such data is fragmentary and woefully incomplete.

Detection of Mycobacterium ulcerans in the Environment Predicts Prevalence of Buruli Ulcer in Benin

Background Mycobacterium ulcerans is the causative agent of Buruli ulcer (BU). In West Africa there is an association between BU and residence in low-lying rural villages where aquatic sources are plentiful. Infection occurs through unknown environmental exposure; human-to-human infection is rare. Molecular evidence for M. ulcerans in environmental samples is well documented, but the association of M. ulcerans in the environment with Buruli ulcer has not been studied in West Africa in an area with accurate case data. Methodology/Principal Finding Environmental samples were collected from twenty-five villages in three communes of Benin. Sites sampled included 12 BU endemic villages within the Ouheme and Couffo River drainages and 13 villages near the Mono River and along the coast or ridge where BU has never been identified. Triplicate water filtrand samples from major water sources and samples from three dominant aquatic plant species were collected. Detection of M. ulcerans was based on quantitative polymerase chain reaction. Results show a significant association between M. ulcerans in environmental samples and Buruli ulcer cases in a village (p = 0.0001). A “dose response” was observed in that increasing numbers of M. ulceran- positive environmental samples were associated with increasing prevalence of BU cases (R2 = 0.586). Conclusions/Significance This study provides the first spatial data on the overlap of M. ulcerans in the environment and BU cases in Benin where case data are based on active surveillance. The study also provides the first evidence on M. ulcerans in well-defined non-endemic sites. Most environmental pathogens are more broadly distributed in the environment than in human populations. The congruence of M. ulcerans in the environment and human infection raises the possibility that humans play a role in the ecology of M. ulcerans. Methods developed could be useful for identifying new areas where humans may be at high risk for BU.

Climate and Landscape Factors Associated with Buruli Ulcer Incidence in Victoria, Australia

Background Buruli ulcer (BU), caused by Mycobacterium ulcerans (M. ulcerans), is a necrotizing skin disease found in more than 30 countries worldwide. BU incidence is highest in West Africa; however, cases have substantially increased in coastal regions of southern Australia over the past 30 years. Although the mode of transmission remains uncertain, the spatial pattern of BU emergence in recent years seems to suggest that there is an environmental niche for M. ulcerans and BU prevalence. Methodology/Principal Findings Network analysis was applied to BU cases in Victoria, Australia, from 1981–2008. Results revealed a non-random spatio-temporal pattern at the regional scale as well as a stable and efficient BU disease network, indicating that deterministic factors influence the occurrence of this disease. Monthly BU incidence reported by locality was analyzed with landscape and climate data using a multilevel Poisson regression approach. The results suggest the highest BU risk areas occur at low elevations with forested land cover, similar to previous studies of BU risk in West Africa. Additionally, climate conditions as far as 1.5 years in advance appear to impact disease incidence. Warmer and wetter conditions 18–19 months prior to case emergence, followed by a dry period approximately 5 months prior to case emergence seem to favor the occurrence of BU. Conclusions/Significance The BU network structure in Victoria, Australia, suggests external environmental factors favor M. ulcerans transmission and, therefore, BU incidence. A unique combination of environmental conditions, including land cover type, temperature and a wet-dry sequence, may produce habitat characteristics that support M. ulcerans transmission and BU prevalence. These findings imply that future BU research efforts on transmission mechanisms should focus on potential vectors/reservoirs found in those environmental niches. Further, this study is the first to quantitatively estimate environmental lag times associated with BU outbreaks, providing insights for future transmission investigations.

Leishmaniasis transmission: distribution and coarse-resolution ecology of two vectors and two parasites in Egypt

INTRODUCTION In past decades, leishmaniasis burden has been low across Egypt; however, changing environment and land use has placed several parts of the country at risk. As a consequence, leishmaniasis has become a particularly difficult health problem, both for local inhabitants and for multinational military personnel. METHODS To evaluate coarse-resolution aspects of the ecology of leishmaniasis transmission, collection records for sandflies and Leishmania species were obtained from diverse sources. To characterize environmental variation across the country, we used multitemporal Land Surface Temperature (LST) and Normalized Difference Vegetation Index (NDVI) data from the Moderate Resolution Imaging Spectroradiometer (MODIS) for 2005-2011. Ecological niche models were generated using MaxEnt, and results were analyzed using background similarity tests to assess whether associations among vectors and parasites (i.e., niche similarity) can be detected across broad geographic regions. RESULTS We found niche similarity only between one vector species and its corresponding parasite species (i.e., Phlebotomus papatasi with Leishmania major), suggesting that geographic ranges of zoonotic cutaneous leishmaniasis and its potential vector may overlap, but under distinct environmental associations. Other associations (e.g., P. sergenti with L. major) were not supported. Mapping suitable areas for each species suggested that northeastern Egypt is particularly at risk because both parasites have potential to circulate. CONCLUSIONS Ecological niche modeling approaches can be used as a first-pass assessment of vector-parasite interactions, offering useful insights into constraints on the geography of transmission patterns of leishmaniasis.

Spatial Analysis of Anthropogenic Landscape Disturbance and Buruli Ulcer Disease in Benin

Background Land use and land cover (LULC) change is one anthropogenic disturbance linked to infectious disease emergence. Current research has focused largely on wildlife and vector-borne zoonotic diseases, neglecting to investigate landscape disturbance and environmental bacterial infections. One example is Buruli ulcer (BU) disease, a necrotizing skin disease caused by the environmental pathogen Mycobacterium ulcerans (MU). Empirical and anecdotal observations have linked BU incidence to landscape disturbance, but potential relationships have not been quantified as they relate to land cover configurations. Methodology/Principal Findings A landscape ecological approach utilizing Bayesian hierarchical models with spatial random effects was used to test study hypotheses that land cover configurations indicative of anthropogenic disturbance were related to Buruli ulcer (BU) disease in southern Benin, and that a spatial structure existed for drivers of BU case distribution in the region. A final objective was to generate a continuous, risk map across the study region. Results suggested that villages surrounded by naturally shaped, or undisturbed rather than disturbed, wetland patches at a distance within 1200m were at a higher risk for BU, and study outcomes supported the hypothesis that a spatial structure exists for the drivers behind BU risk in the region. The risk surface corresponded to known BU endemicity in Benin and identified moderate risk areas within the boundary of Togo. Conclusions/Significance This study was a first attempt to link land cover configurations representative of anthropogenic disturbances to BU prevalence. Study results identified several significant variables, including the presence of natural wetland areas, warranting future investigations into these factors at additional spatial and temporal scales. A major contribution of this study included the incorporation of a spatial modeling component that predicted BU rates to new locations without strong knowledge of environmental factors contributing to disease distribution.

Automated identification of insect vectors of Chagas disease in Brazil and Mexico: the Virtual Vector Lab

Identification of arthropods important in disease transmission is a crucial, yet difficult, task that can demand considerable training and experience. An important case in point is that of the 150+ species of Triatominae, vectors of Trypanosoma cruzi, causative agent of Chagas disease across the Americas. We present a fully automated system that is able to identify triatomine bugs from Mexico and Brazil with an accuracy consistently above 80%, and with considerable potential for further improvement. The system processes digital photographs from a photo apparatus into landmarks, and uses ratios of measurements among those landmarks, as well as (in a preliminary exploration) two measurements that approximate aspects of coloration, as the basis for classification. This project has thus produced a working prototype that achieves reasonably robust correct identification rates, although many more developments can and will be added, and—more broadly—the project illustrates the value of multidisciplinary collaborations in resolving difficult and complex challenges.

Landscape and environmental influences on Mycobacterium ulcerans distribution among aquatic sites in Ghana

Buruli ulcer, caused by Mycobacterium ulcerans, is highly endemic in West Africa. While the mode of transmission is unknown, many studies associate Buruli ulcer with different types of water exposure. We present results from the largest study to date to test for M. ulcerans in aquatic sites and identify environmental attributes associated with its presence. Environmental samples from 98 aquatic sites in the Greater Accra, Ashanti, and Volta regions of Ghana were tested for the presence of M. ulcerans DNA by polymerase chain reaction. The proportion of aquatic sites positive for M. ulcerans varied by region: Ashanti 66% (N = 39), Greater Accra 34% (N = 29), and Volta 0% (N = 30). We explored the spatial distribution of M. ulcerans positive and negative water bodies and found no significant clusters. We also determined both highly localized water attributes and broad scale remotely sensed land cover and terrain environmental characteristics associated with M. ulcerans presence through logistic regression. Our results concur with published results regarding conditions suitable for M. ulcerans growth and associations with Buruli ulcer disease burden with regards to water characteristics and disturbed environments, but differ from others with regards to spatial associations and topographic effects such as elevation and wetness. While our results suggest M. ulcerans is an environmental organism existing in a specific ecological niche, they also reveal variation in the elements defining this niche across the sites considered. In addition, despite the causal association between Buruli ulcer and M. ulcerans, we observed no significant statistical association between case reports of Buruli ulcer and presence of M. ulcerans in nearby waterbodies.

Landscape Genetics of Aedes mcintoshi (Diptera: Culicidae), an Important Vector of Rift Valley Fever Virus in Northeastern Kenya

Abstract Rift Valley fever virus (RVFV) is a vector-borne, zoonotic disease that affects humans, wild ungulates, and domesticated livestock in Africa and the Arabian Peninsula. Rift Valley fever virus exhibits interepizootic and epizootic phases, the latter defined by widespread virus occurrence in domesticated livestock. Kenya appears to be particularly vulnerable to epizootics, with 11 outbreaks occurring between 1951 and 2007. The mosquito species Aedes mcintoshi (subgenus Neomelaniconion) is an important primary vector for RVFV in Kenya. Here, we investigate associations between genetic diversity and differentiation of one regional subclade of Ae. mcintoshi in Northeastern Kenya with environmental variables, using a multivariate statistical approach. Using CO1 (cytochrome oxidase subunit 1) sequence data deposited in GenBank, we found no evidence of isolation by distance contributing to genetic differentiation across the study area. However, we did find significant CO1 subpopulation structure and associations with recent mean precipitation values. In addition, variation in genetic diversity across our seven sample sites was associated with both precipitation and percentage clay in the soil. The large number of haplotypes found in this data set indicates that a great deal of diversity remains unsampled in this region. Additional sampling across a larger geographic area, combined with next-generation sequencing approaches that better characterize the genome, would provide a more robust assessment of genetic diversity and differentiation. Further understanding of the genetic structure of Ae. mcintoshi could provide useful information regarding the potential for RVFV to spread across East African landscapes.

Buruli ulcer disease: The unknown environmental and social ecology of a bacterial pathogen

Foreword Billie Lee Turner II Chapter 1: Human Health at the Nexus of Ecologies and Politics Kelley A. Crews and Brian King Section I: Health within Social and Ecological Systems Chapter 2: Positioning Health in a Socio-Ecological Systems Framework Kelley A. Crews Chapter 3: Capitals and Context: Bridging Health and Livelihoods in Smallholder Frontiers Leah K. VanWey, James R. Hull, and Gilvan Guedes Chapter 4: Change in Tropical Landscapes: Implications for Health and Livelihoods Kenneth R. Young Section II: Empirical Approaches to Injury and Infectious Disease Chapter 5: Buruli Ulcer Disease: The Unknown Environmental and Social Ecology of a Bacterial Pathogen Jiaguo Qi, Lindsay P. Campbell, Jenni van Ravensway, Andrew O. Finley, Richard W. Merritt, and M. Eric Benbow Chapter 6: The Ecology of Injuries in Matlab, Bangladesh Elisabeth D. Root and Michael Emch Chapter 7: Human Settlement, Environmental Change, and Frontier Malaria in the Brazilian Amazon Marcia C. Castro and Burton H. Singer Section III: Disease Histories, the State, and [Mis]Management Chapter 8: Vaccines, Fertility, and Power: The Political Ecology of Indigenous Health and Well-Being in Lowland Latin America Kendra McSweeney and Zoe Pearson Chapter 9: Tsetse and Trypanosomiasis: Eradication, Control, and Coexistence in Africa Paul F. McCord, Joseph P. Messina, & Carolyn A. Fahey Chapter 10: Geographies of HIV and Marginalization: A Case Study of HIV/AIDS Risk among Mayan Communities in Western Belize Cynthia Pope Chapter 11: The Mosquito State: How Technology, Capital and State Practice Mediate the Ecologies of Public Health Paul Robbins and Jacob C. Miller Section IV: Health Vulnerabilities Chapter 12: Exposure to Heat Stress in Urban Environments Olga Wilhelmi, Alex de Sherbinin, and Mary Hayden Chapter 13: Power, Race, and the Neglect of Science: The HIV Epidemics in Sub-Saharan Africa Eileen Stillwaggon and Larry Sawers Chapter 14: Disease as Shock, HIV/AIDS as Experience: Coupling Social and Ecological Responses in Sub-Saharan Africa Brian King Chapter 15: Futures for Ecologies and Politics of Health Brian King and Kelley A. Crews