Ecological and life history traits are associated with Ross River virus infection among sylvatic mammals in Australia
Background: Ross River virus (RRV) is Australia’s most important arbovirus given its annual burden of disease and the relatively large number of Australians at risk for infection. This mosquito-borne arbovirus is also a zoonosis, making its epidemiology and infection ecology complex and cryptic. Our grasp of enzootic, epizootic, and zoonotic RRV transmission dynamics is imprecise largely due to a poor understanding of the role of wild mammalian hosts in the RRV system.
Methods: The current study applied a piecewise structural equation model (PSEM) toward an interspecific comparison of sylvatic Australian mammals to characterize the ecological and life history profile of species with a history of RRV infection relative to those species with no such history among all wild mammalian species surveyed for RRV infection. The effects of species traits were assessed through multiple causal pathways within the PSEM framework.
Results: Sylvatic mammalian species with a history of RRV infection tended to express dietary specialization and smaller population density. These species were also characterized by a longer gestation length.
Conclusions: This study provides the first interspecific comparison of wild mammals for RRV infection and identifies some potential targets for future wildlife surveys into the infection ecology of this important arbovirus. An applied RRV macroecology may prove invaluable to the epidemiological modeling of RRV epidemics across diverse sylvatic landscapes, as well as to the development of human and animal health surveillance systems.
Michael G. Walsh BMC Ecology201919:2 https://doi.org/10.1186/s12898-019-0220-5.
Climatic influence on anthrax suitability in warming northern latitudes
Climate change is impacting ecosystem structure and function, with potentially drastic downstream effects on human and animal health. Emerging zoonotic diseases are expected to be particularly vulnerable to climate and biodiversity disturbance. Anthrax is an archetypal zoonosis that manifests its most significant burden on vulnerable pastoralist communities. The current study sought to investigate the influence of temperature increases on geographic anthrax suitability in the temperate, boreal, and arctic North, where observed climate impact has been rapid. This study also explored the influence of climate relative to more traditional factors, such as livestock distribution, ungulate biodiversity, and soil-water balance, in demarcating risk. Machine learning was used to model anthrax suitability in northern latitudes. The model identified climate, livestock density and wild ungulate species richness as the most influential features in predicting suitability. These findings highlight the significance of warming temperatures for anthrax ecology in northern latitudes, and suggest potential mitigating effects of interventions targeting megafauna biodiversity conservation in grassland ecosystems, and animal health promotion among small to midsize livestock herds. Michael G. Walsh, Allard W. de Smalen & Siobhan M. Mor. Scientific Reports volume 8, Article number: 9269 (2018). https://rdcu.be/Z8Vg
Interspecific network centrality, host range and early‐life development are associated with wildlife hosts of Rift Valley fever virus
Rift Valley fever virus (RVFV) is responsible for a substantive disease burden in pastoralist communities and the agricultural sector in the African continent and Arabian Peninsula. Enzootic, epizootic and zoonotic RVFV transmission dynamics remain ill‐defined, particularly due to a poor understanding of the role of mammalian hosts in the epidemiology and infection ecology of this arbovirus. Using a piecewise structural equation model, this study sought to identify associations between biological and ecological characteristics of mammalian species and documented RVFV infection to highlight species‐level traits that may influence wildlife host status. Interspecific network centrality, size of species home range and reproductive life‐history traits were all associated with being an RVFV host. The identification of these species‐level characteristics may help to provide ecological context for the role of wildlife amplification hosts in the epidemiology of spillover to livestock and humans and may also help to identify specific points of vulnerability at the wildlife–livestock interface. Walsh and Mor. Transboundary and Emerging Diseases. 2018 May 13. doi: 10.1111/tbed.12903
Hydrological features and the ecological niches of mammalian hosts delineate elevated risk for Ross River virus epidemics in anthropogenic landscapes in Australia
The current understanding of the landscape epidemiology of Ross River virus (RRV), Australia’s most common arthropod-borne pathogen, is fragmented due to gaps in surveillance programs and the relatively narrow focus of the research conducted to date. This leaves public health agencies with an incomplete understanding of the spectrum of infection risk across the diverse geography of the Australian continent. The current investigation sought to assess the risk of RRV epidemics based on abiotic and biotic landscape features in anthropogenic landscapes, with a particular focus on the influence of water and wildlife hosts.
Abiotic features, including hydrology, land cover and altitude, and biotic features, including the distribution of wild mammalian hosts, were interrogated using a Maxent model to discern the landscape suitability to RRV epidemics in anthropogenically impacted environments across Australia.
Water-soil balance, proximity to controlled water reservoirs, and the ecological niches of four species (Perameles nasuta, Wallabia bicolor, Pseudomys novaehollandiae and Trichosurus vulpecula) were important features identifying high risk landscapes suitable for the occurrence of RRV epidemics.
These results help to delineate human infection risk and thus provide an important perspective for geographically targeted vector, wildlife, and syndromic surveillance within and across the boundaries of local health authorities. Importantly, our analysis highlights the importance of the hydrology, and the potential role of mammalian host species in shaping RRV epidemic risk in peri-urban space. This study offers novel insight into wildlife hosts and RRV infection ecology and identifies those species that may be beneficial to future targeted field surveillance particularly in ecosystems undergoing rapid change. Walsh and Webb Parasites & Vectors (2018) 11:192. https://doi.org/10.1186/s13071-018-2776-x
The impact of human population pressure on flying fox niches and the potential consequences for Hendra virus spillover
Hendra virus (HeV) is an emerging pathogen of concern in Australia given its ability to spillover from its reservoir host, pteropid bats, to horses and further on to humans, and the severe clinical presentation typical in these latter incidental hosts. Specific human pressures over recent decades, such as expanding human populations, urbanization, and forest fragmentation, may have altered the ecological niche of Pteropus species acting as natural HeV reservoirs and may modulate spillover risk. This study explored the influence of inter-decadal net human local migration between 1970 and 2000 on changes in the habitat suitability to P. alecto and P. conspicillatus from 1980 to 2015 in eastern Australia. These ecological niches were modeled using boosted regression trees and subsequently fitted, along with additional landscape factors, to HeV spillovers to explore the spatial dependency of this zoonosis. The spatial model showed that the ecological niche of these two flying fox species, the human footprint, and proximity to woody savanna were each strongly associated with HeV spillover and together explained most of the spatial dependency exhibited by this zoonosis. These findings reinforce the potential for anthropogenic pressures to shape the landscape epidemiology of HeV spillover. Scientific Reports 7, Article number: 8226 (2017) doi:10.1038/s41598-017-08065-z
Wetlands, wild Bovidae species richness and sheep density delineate risk of Rift Valley fever outbreaks in the African continent and Arabian Peninsula
Rift Valley fever (RVF) is an emerging, vector-borne viral zoonosis that has significantly impacted public health, livestock health and production, and food security over the last three decades across large regions of the African continent and the Arabian Peninsula. The potential for expansion of RVF outbreaks within and beyond the range of previous occurrence is unknown. Despite many large national and international epidemics, the landscape epidemiology of RVF remains obscure, particularly with respect to the ecological roles of wildlife reservoirs and surface water features. The current investigation modeled RVF risk throughout Africa and the Arabian Peninsula as a function of a suite of biotic and abiotic landscape features using machine learning methods. Intermittent wetland, wild Bovidae species richness and sheep density were associated with increased landscape suitability to RVF outbreaks. These results suggest the role of wildlife hosts and distinct hydrogeographic landscapes in RVF virus circulation and subsequent outbreaks may be underestimated. These results await validation by studies employing a deeper, field-based interrogation of potential wildlife hosts within high risk taxa.
Walsh MG, Willem de Smalen A, Mor SM (2017) Wetlands, wild Bovidae species richness and sheep density delineate risk of Rift Valley fever outbreaks in the African continent and Arabian Peninsula. PLoS Negl Trop Dis 11(7): e0005756. https://doi.org/10.1371/journal.pntd.0005756
Global Seasonal Clustering of H5N1 Avian Influenza
Highly pathogenic avian influenza subtype H5N1 (H5N1) has contributed to substantial economic loss for backyard and large scale poultry farmers each year since 1997. While the distribution of domestic H5N1 outbreaks across Africa, Europe and Asia is extensive, those features of the landscape conferring greatest risk remain uncertain. Furthermore, the extent to which influential landscape features may vary by season has been inadequately described. The current investigation used World Organization for Animal Health surveillance data to 1) delineate areas at greatest risk for H5N1 epizootics among domestic poultry, 2) identify those abiotic and biotic features of the landscape associated with outbreak risk, and 3) examine patterns of epizootic clustering by season. Inhomogeneous point process models were used to predict the intensity of H5N1 outbreaks and describe the spatial dependencies between them. During October through March, decreasing precipitation, increasing isothermality, and the presence of H5N1 in wild birds were significantly associated with increased risk of domestic H5N1 epizootics. Conversely, increasing precipitation and decreasing isothermality were associated with increased risk during April through September. Increasing temperature during the coldest quarter, domestic poultry density, and proximity to surface water were associated with increased risk of domestic outbreaks throughout the year. Spatial dependencies between outbreaks appeared to vary seasonally, with substantial clustering at small and large scale identified during October through March even after accounting for inhomogeneity due to landscape factors. In contrast, during April to September, H5N1 outbreaks exhibited no clustering at small scale once accounting for landscape factors. This investigation has identified seasonal differences in risk and clustering patterns of H5N1 outbreaks in domestic poultry, and may suggest strategies in high risk areas with features amenable to intervention such as controlling domestic bird movement in areas of high poultry density or preventing contact between poultry and wild birds and/or surface water features.
Walsh, MG, Amstislavski P, Andrea Greene, Haseeb, MA. The landscape epidemiology of seasonal clustering of highly pathogenic avian influenza (H5N1) in domestic poultry in Africa, Europe and Asia. Transboundary and Emerging Diseases 2016 Jun 16. doi: 10.1111/tbed.12537. Epub ahead of print.
The Ecologic Niche of Plague in the Western US
Plague has been established in the western United States (US) since 1900 following the west coast introduction of commensal rodents infected with Yersinia pestis via early industrial shipping. Over the last century, plague ecology has transitioned through cycles of widespread human transmission, urban domestic transmission among commensal rodents, and ultimately settled into the predominantly sylvan foci that remain today where it is maintained alternatively by enzootic and epizootic transmission. While zoonotic transmission to humans is much less common in modern times, significant plague risk remains in parts of the western US. Moreover, risk to some threatened species that are part of the epizootic cycle can be quite substantive. This investigation attempted to predict the risk of plague across the western US by modeling the ecologic niche of plague in sylvan and domestic animals identified between 2000 and 2015. A Maxent machine learning algorithm was used to predict this niche based on climate, altitude, land cover, and the presence of an important enzootic species, Peromyscus maniculatus. This model demonstrated good predictive ability (AUC = 86%) and identified areas of high risk in central Colorado, north-central New Mexico, and southwestern and northeastern California. The presence of P. maniculatus, altitude, precipitation during the driest and wettest quarters, and distance to artificial surfaces, all contributed substantively to maximizing the gain function. These findings add to the known landscape epidemiology and infection ecology of plague in the western US and may suggest locations of particular risk to be targeted for wild and domestic animal intervention.
Walsh, MG and Haseeb, MA. Modeling the ecologic niche of plague in sylvan and domestic animal hosts to delineate sources of human exposure in the western United States. PeerJ. 2015 Dec 14;3:e1493. doi: 10.7717/peerj.1493.
Nipah Virus Spillover
Nipah virus (NiV) is a significant emerging zoonotic pathogen given its wide geographic distribution, and the severe morbidity and high mortality that accompanies infection. Moreover, the layered landscape epidemiology surrounding spillover from reservoir host species to humans is ill-defined. Identifying landscape features that contribute to NiV spillover would likely prove helpful in preventing emergence in human populations. Using an inhomogeneous Poisson model, this study investigated the role of vegetation cover, the human footprint (HFP), and reservoir Pteropus bat distribution to identify the spatial dependence of spillover and map risk across South and Southeast Asia. The spatial model identified HFP (RR = 1.08, 95% C.I. 1.05 – 1.11) and bat distribution (RR = 19.44, 95% C.I 1.92 – 196.7) as significant predictors of NiV risk, while vegetation cover was not significant after accounting for HFP and the presence of Pteropus bats. These findings further inform the landscape epidemiology of NiV and suggest specific conduits for spillover in the landscape. However, more detailed field studies will be required to validate these results.
Walsh, MG. Mapping the risk of Nipah virus spillover into human populations in South and Southeast Asia. Trans R Soc Trop Med Hyg. 2015 Sep;109(9):563-71. doi: 10.1093/trstmh/trv055.
Ebola Virus Disease
Ebola virus disease (EVD) is an emerging infectious disease of zoonotic origin that has been responsible for high mortality and significant social disruption in West and Central Africa. Zoonotic transmission of EVD requires contact between susceptible human hosts and the reservoir species for Ebolaviruses, which are believed to be fruit bats. Nevertheless, features of the landscape that may facilitate such points of contact have not yet been adequately identified. Nor have spatial dependencies between zoonotic EVD transmission and landscape structures been delineated. This investigation sought to describe the spatial relationship between zoonotic EVD transmission events, or spillovers, and population density and vegetation cover. An inhomogeneous Poisson process model was fitted to all precisely geolocated zoonotic transmissions of EVD in West and Central Africa. Population density was strongly associated with spillover; however, there was significant interaction between population density and green vegetation cover. In areas of very low population density, increasing vegetation cover was associated with a decrease in risk of zoonotic transmission, but as population density increased in a given area, increasing vegetation cover was associated with increased risk of zoonotic transmission. This study showed that the spatial dependencies of Ebolavirus spillover were associated with the distribution of population density and vegetation cover in the landscape, even after controlling for climate and altitude. While this is an observational study, and thus precludes direct causal inference, the findings do highlight areas that may be at risk for zoonotic EVD transmission based on the spatial configuration of important features of the landscape.
Walsh MG, Haseeb M. (2015) The landscape configuration of zoonotic transmission of Ebola virus disease in West and Central Africa: interaction between population density and vegetation cover. PeerJ 3:e735https://dx.doi.org/10.7717/peerj.735
Rats in New York City
Rats are ubiquitous in urban environments and, as established reservoirs for infectious pathogens, present a control priority for public health agencies. New York City (NYC) harbors one of the largest rat populations in the United States, but surprising little study has been undertaken to define rat ecology across varied features of this urban landscape. More importantly, factors that may contribute to increased encounters between rats and humans have rarely been explored. Using city-wide records of rat sightings reported to the NYC Department of Health and Mental Hygiene, this investigation sought to identify sociodemographic, housing, and physical landscape characteristics that are associated with increased rat sightings across NYC census tracts. A hierarchical Bayesian conditional autoregressive Poisson model was used to assess these associations while accounting for spatial heterogeneity in the variance. Closer proximity to both subway lines and recreational public spaces was associated with a higher concentration of rat sightings, as was a greater presence of older housing, vacant housing units, and low education among the population. Moreover, these aspects of the physical and social landscape accurately predicted rat sightings across the city. These findings have identified specific features of the NYC urban environment that may help to provide direct control targets for reducing human–rat encounters.
Walsh MG. (2014) Rat sightings in New York City are associated with neighborhood sociodemographics, housing characteristics, and proximity to open public space. PeerJ 2:e533 https://dx.doi.org/10.7717/peerj.533
Predicting toxocariasis in New York City
Toxocariasis is increasingly recognized as an important neglected infection of poverty (NIP) in developed countries, and may constitute the most important NIP in the United States (US) given its association with chronic sequelae such as asthma and poor cognitive development. Its potential public health burden notwithstanding, toxocariasis surveillance is minimal throughout the US and so the true burden of disease remains uncertain in many areas. The Third National Health and Nutrition Examination Survey conducted a representative serologic survey of toxocariasis to estimate the prevalence of infection in diverse US subpopulations across different regions of the country. Using the NHANES III surveillance data, the current study applied the predicted probabilities of toxocariasis to the sociodemographic composition of New York census tracts to estimate the local probability of infection across the city. The predicted probability of toxocariasis ranged from 6% among US-born Latino women with a university education to 57% among immigrant men with less than a high school education. The predicted probability of toxocariasis exhibited marked spatial variation across the city, with particularly high infection probabilities in large sections of Queens, and smaller, more concentrated areas of Brooklyn and northern Manhattan. This investigation is the first attempt at small-area estimation of the probability surface of toxocariasis in a major US city. While this study does not define toxocariasis risk directly, it does provide a much needed tool to aid the development of toxocariasis surveillance in New York City.
Walsh MG, Haseeb MA (2014) Small-Area Estimation of the Probability of Toxocariasis in New York City Based on Sociodemographic Neighborhood Composition. PLoS ONE 9(6): e99303. doi:10.1371/journal.pone.0099303
Forest Fragmentation and Babesiosis in New York State
Babesiosis is an emerging arthropod-borne infection that has been increasing in incidence for the last decade in the northeastern United States. Babesiosis may share features of its landscape epidemiology with other arthropod-borne infections transmitted by the same tick vectors in similar geographic spaces. This study examined 11 years of surveillance data in New York State to measure the relationship between forest fragmentation and the incidence of human babesiosis. Adjusted Poisson models showed that increasing edges of contact between forested land and developed land, as measured by their shared perimeters, was associated with a higher incidence of babesiosis cases (incident rate ratio [IRR]=1.015, 95% confidence interval [CI] 1.01-1.02; p<0.001), even after controlling for the total developed land area and forest density, and temperature and precipitation. Each 10-km increase in perimeter contact between forested land and developed land per county was associated with a 1.5% increase in babesiosis risk. Higher temperature was also strongly associated with increasing babesiosis risk (IRR=1.18, 95% CI 1.10-1.27; p<0.001), wherein each degree Celsius increase was associated with an 18% increase in babesiosis risk. While direct causal conclusions cannot be drawn from these data, these findings do identify a potentially important signal in the epidemiology of babesiosis and suggest that the underlying physical landscape may play a role in shaping points of contact between humans and tick vectors and the subsequent transmission of Babesia microti.
Walsh MG. The relevance of forest fragmentation on the incidence of human babesiosis: investigating the landscape epidemiology of an emerging tick-borne disease. Vector Borne Zoonotic Dis. 2013 Apr;13(4):250-5. doi: 10.1089/vbz.2012.1198.
Hydrogeography and Climate in the Landscape Epidemiology of West Nile Virus in New York State
The epidemiology and ecology of West Nile virus (WNV) have not yet been completely described. In particular, the specific roles of climate and water in the landscape in the occurrence of human WNV cases remain unknown. This study used Poisson regression to describe the relationships between WNV cases and temperature, precipitation, and the hydrogeography of the landscape in New York State from 2000 to 2010. Fully adjusted models showed that hydrogeographic area was significantly inversely associated with WNV cases (incidence rate ratio (IRR) = 0.99; 95% C.I. = 0.98–0.997, p = 0.04), such that each one square kilometer increase in hydrogeographic area was associated with a 1% decrease in WNV incidence. This association was independent of both temperature, which was also associated with WNV incidence (IRR = 2.06; 95% C.I. = 1.84–2.31, p<0.001), and precipitation, which was not (IRR = 1.0; 95% C.I. = 0.99–1.01, p = 0.16). While the results are only suggestive due to the county-level aggregated data, these findings do identify a potentially important surveillance signal in the landscape epidemiology of WNV infection.
Walsh MG (2012) The Role of Hydrogeography and Climate in the Landscape Epidemiology of West Nile Virus in New York State from 2000 to 2010. PLoS ONE 7(2): e30620. doi:10.1371/journal.pone.0030620