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Substantial global attention is focused on how to reduce the risk of future pandemics. Reducing this risk requires investment in prevention, preparedness, and response. Although preparedness and response have received significant focus, prevention, especially the prevention of zoonotic spillover, remains largely absent from global conversations. This oversight is due in part to the lack of a clear definition of prevention and lack of guidance on how to achieve it. To address this gap, we elucidate the mechanisms linking environmental change and zoonotic spillover using spillover of viruses from bats as a case study. We identify ecological interventions that can disrupt these spillover mechanisms and propose policy frameworks for their implementation. Recognizing that pandemics originate in ecological systems, we advocate for integrating ecological approaches alongside biomedical approaches in a comprehensive and balanced pandemic prevention strategy.
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Pandemias , Virus , Animales , Zoonosis/epidemiología , EcosistemaRESUMEN
Introduction: Bats are important providers of ecosystem services such as pollination, seed dispersal, and insect control but also act as natural reservoirs for virulent zoonotic viruses. Bats host multiple viruses that cause life-threatening pathology in other animals and humans but, themselves, experience limited pathological disease from infection. Despite bats' importance as reservoirs for several zoonotic viruses, we know little about the broader viral diversity that they host. Bat virus surveillance efforts are challenged by difficulties of field capture and the limited scope of targeted PCR- or ELISA-based molecular and serological detection. Additionally, virus shedding is often transient, thus also limiting insights gained from nucleic acid testing of field specimens. Phage ImmunoPrecipitation Sequencing (PhIP-Seq), a broad serological tool used previously to comprehensively profile viral exposure history in humans, offers an exciting prospect for viral surveillance efforts in wildlife, including bats. Methods: Here, for the first time, we apply PhIP-Seq technology to bat serum, using a viral peptide library originally designed to simultaneously assay exposures to the entire human virome. Results: Using VirScan, we identified past exposures to 57 viral genera-including betacoronaviruses, henipaviruses, lyssaviruses, and filoviruses-in semi-captive Pteropus alecto and to nine viral genera in captive Eonycteris spelaea. Consistent with results from humans, we find that both total peptide hits (the number of enriched viral peptides in our library) and the corresponding number of inferred past virus exposures in bat hosts were correlated with poor bat body condition scores and increased with age. High and low body condition scores were associated with either seropositive or seronegative status for different viruses, though in general, virus-specific age-seroprevalence curves defied assumptions of lifelong immunizing infection, suggesting that many bat viruses may circulate via complex transmission dynamics. Discussion: Overall, our work emphasizes the utility of applying biomedical tools, like PhIP-Seq, first developed for humans to viral surveillance efforts in wildlife, while highlighting opportunities for taxon-specific improvements.
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Quirópteros , Reservorios de Enfermedades , Animales , Humanos , Ecosistema , Estudios Seroepidemiológicos , ZoonosisRESUMEN
Co-infection is an underappreciated phenomenon in contemporary disease ecology despite its ubiquity and importance in nature. Viruses, and other co-infecting agents, can interact in ways that shape host and agent communities, influence infection dynamics, and drive evolutionary selective pressures. Bats are host to many viruses of zoonotic potential and have drawn increasing attention in their role as wildlife reservoirs for human spillover. However, the role of co-infection in driving viral transmission dynamics within bats is unknown. Here, we systematically review peer-reviewed literature reporting viral co-infections in bats. We show that viral co-infection is common in bats but is often only reported as an incidental finding. Biases identified in our study database related to virus and host species were pre-existing in virus studies of bats generally. Studies largely speculated on the role co-infection plays in viral recombination and few investigated potential drivers or impacts of co-infection. Our results demonstrate that current knowledge of co-infection in bats is an ad hoc by-product of viral discovery efforts, and that future targeted co-infection studies will improve our understanding of the role it plays. Adding to the broader context of co-infection studies in other wildlife species, we anticipate our review will inform future co-infection study design and reporting in bats. Consideration of detection strategy, including potential viral targets, and appropriate analysis methodology will provide more robust results and facilitate further investigation of the role of viral co-infection in bat reservoirs.
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Quirópteros , Coinfección , Virosis , Animales , Animales Salvajes , Evolución Biológica , Coinfección/veterinaria , Virosis/veterinariaRESUMEN
During recent decades, pathogens that originated in bats have become an increasing public health concern. A major challenge is to identify how those pathogens spill over into human populations to generate a pandemic threat1. Many correlational studies associate spillover with changes in land use or other anthropogenic stressors2,3, although the mechanisms underlying the observed correlations have not been identified4. One limitation is the lack of spatially and temporally explicit data on multiple spillovers, and on the connections among spillovers, reservoir host ecology and behaviour and viral dynamics. We present 25 years of data on land-use change, bat behaviour and spillover of Hendra virus from Pteropodid bats to horses in subtropical Australia. These data show that bats are responding to environmental change by persistently adopting behaviours that were previously transient responses to nutritional stress. Interactions between land-use change and climate now lead to persistent bat residency in agricultural areas, where periodic food shortages drive clusters of spillovers. Pulses of winter flowering of trees in remnant forests appeared to prevent spillover. We developed integrative Bayesian network models based on these phenomena that accurately predicted the presence or absence of clusters of spillovers in each of the 25 years. Our long-term study identifies the mechanistic connections between habitat loss, climate and increased spillover risk. It provides a framework for examining causes of bat virus spillover and for developing ecological countermeasures to prevent pandemics.
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Quirópteros , Ecología , Ecosistema , Virus Hendra , Caballos , Animales , Humanos , Australia , Teorema de Bayes , Quirópteros/virología , Clima , Caballos/virología , Salud Pública , Virus Hendra/aislamiento & purificación , Recursos Naturales , Agricultura , Bosques , Abastecimiento de Alimentos , Pandemias/prevención & control , Pandemias/veterinariaRESUMEN
The ecological conditions experienced by wildlife reservoirs affect infection dynamics and thus the distribution of pathogen excreted into the environment. This spatial and temporal distribution of shed pathogen has been hypothesised to shape risks of zoonotic spillover. However, few systems have data on both long-term ecological conditions and pathogen excretion to advance mechanistic understanding and test environmental drivers of spillover risk. We here analyse three years of Hendra virus data from nine Australian flying fox roosts with covariates derived from long-term studies of bat ecology. We show that the magnitude of winter pulses of viral excretion, previously considered idiosyncratic, are most pronounced after recent food shortages and in bat populations displaced to novel habitats. We further show that cumulative pathogen excretion over time is shaped by bat ecology and positively predicts spillover frequency. Our work emphasises the role of reservoir host ecology in shaping pathogen excretion and provides a new approach to estimate spillover risk.
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Quirópteros , Virus Hendra , Animales , Australia , Estaciones del AñoRESUMEN
BACKGROUND: Billions of people living in poverty are at risk of environmentally mediated infectious diseases-that is, pathogens with environmental reservoirs that affect disease persistence and control and where environmental control of pathogens can reduce human risk. The complex ecology of these diseases creates a global health problem not easily solved with medical treatment alone. METHODS: We quantified the current global disease burden caused by environmentally mediated infectious diseases and used a structural equation model to explore environmental and socioeconomic factors associated with the human burden of environmentally mediated pathogens across all countries. FINDINGS: We found that around 80% (455 of 560) of WHO-tracked pathogen species known to infect humans are environmentally mediated, causing about 40% (129â488 of 359â341 disability-adjusted life years) of contemporary infectious disease burden (global loss of 130 million years of healthy life annually). The majority of this environmentally mediated disease burden occurs in tropical countries, and the poorest countries carry the highest burdens across all latitudes. We found weak associations between disease burden and biodiversity or agricultural land use at the global scale. In contrast, the proportion of people with rural poor livelihoods in a country was a strong proximate indicator of environmentally mediated infectious disease burden. Political stability and wealth were associated with improved sanitation, better health care, and lower proportions of rural poverty, indirectly resulting in lower burdens of environmentally mediated infections. Rarely, environmentally mediated pathogens can evolve into global pandemics (eg, HIV, COVID-19) affecting even the wealthiest communities. INTERPRETATION: The high and uneven burden of environmentally mediated infections highlights the need for innovative social and ecological interventions to complement biomedical advances in the pursuit of global health and sustainability goals. FUNDING: Bill & Melinda Gates Foundation, National Institutes of Health, National Science Foundation, Alfred P. Sloan Foundation, National Institute for Mathematical and Biological Synthesis, Stanford University, and the US Defense Advanced Research Projects Agency.
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COVID-19 , Enfermedades Transmisibles , Carga Global de Enfermedades , Humanos , Enfermedades Transmisibles/epidemiología , Salud Global , Factores Socioeconómicos , Estados UnidosRESUMEN
In October 2021, the first contemporary detection of Hendra virus genotype 2 (HeV-g2) was made by veterinary priority disease investigation in a horse near Newcastle, New South Wales, Australia, as part of routine veterinary priority disease surveillance. This discovery followed an update of Hendra virus diagnostic assays following retrospective identification of this variant from 2015 via sentinel emerging infectious disease research, enabling timely detection of this case. The sole infected horse was euthanized in moribund condition. As the southernmost recognised HeV spill-over detection to date, it extends the southern limit of known cases by approximately 95 km. The event occurred near a large urban centre, characterised by equine populations of diverse type, husbandry, and purpose, with low HeV vaccination rates. Urgent multi-agency outbreak response involved risk assessment and monitoring of 11 exposed people and biosecurity management of at-risk animals. No human or additional animal cases were recognised. This One Health investigation highlights need for research on risk perception and strategic engagement to support owners confronted with the death of companion animals and potential human exposure to a high consequence virus. The location and timing of this spill-over event diverging from that established for prototype HeV (HeV-g1), highlight benefit in proactive One Health surveillance and research activities that improve understanding of dynamic transmission and spill-over risks of both HeV genotypic lineages and related but divergent emerging pathogens.
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As sustainable development practitioners have worked to "ensure healthy lives and promote well-being for all" and "conserve life on land and below water", what progress has been made with win-win interventions that reduce human infectious disease burdens while advancing conservation goals? Using a systematic literature review, we identified 46 proposed solutions, which we then investigated individually using targeted literature reviews. The proposed solutions addressed diverse conservation threats and human infectious diseases, and thus, the proposed interventions varied in scale, costs, and impacts. Some potential solutions had medium-quality to high-quality evidence for previous success in achieving proposed impacts in one or both sectors. However, there were notable evidence gaps within and among solutions, highlighting opportunities for further research and adaptive implementation. Stakeholders seeking win-win interventions can explore this Review and an online database to find and tailor a relevant solution or brainstorm new solutions.
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Control de Enfermedades Transmisibles , Desarrollo Sostenible , HumanosRESUMEN
The emergence of SARS-CoV-2 and the subsequent COVID-19 pandemic has resulted in significant global impact. However, COVID-19 is just one of several high-impact infectious diseases that emerged from wildlife and are linked to the human relationship with nature. The rate of emergence of new zoonoses (diseases of animal origin) is increasing, driven by human-induced environmental changes that threaten biodiversity on a global scale. This increase is directly linked to environmental drivers including biodiversity loss, climate change and unsustainable resource extraction. Australia is a biodiversity hotspot and is subject to sustained and significant environmental change, increasing the risk of it being a location for pandemic origin. Moreover, the global integration of markets means that consumption trends in Australia contributes to the risk of disease spill-over in our regional neighbours in Asia-Pacific, and beyond. Despite the clear causal link between anthropogenic pressures on the environment and increasing pandemic risks, Australia's response to the COVID-19 pandemic, like most of the world, has centred largely on public health strategies, with a clear focus on reactive management. Yet, the span of expertise and evidence relevant to the governance of pandemic risk management is much wider than public health and epidemiology. It involves animal/wildlife health, biosecurity, conservation sciences, social sciences, behavioural psychology, law, policy and economic analyses to name just a few.The authors are a team of multidisciplinary practitioners and researchers who have worked together to analyse, synthesise, and harmonise the links between pandemic risk management approaches and issues in different disciplines to provide a holistic overview of current practice, and conclude the need for reform in Australia. We discuss the adoption of a comprehensive and interdisciplinary 'One Health' approach to pandemic risk management in Australia. A key goal of the One Health approach is to be proactive in countering threats of emerging infectious diseases and zoonoses through a recognition of the interdependence between human, animal, and environmental health. Developing ways to implement a One Health approach to pandemic prevention would not only reduce the risk of future pandemics emerging in or entering Australia, but also provide a model for prevention strategies around the world.
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COVID-19 , Pandemias , Animales , Australia/epidemiología , COVID-19/epidemiología , COVID-19/prevención & control , Humanos , Pandemias/prevención & control , Gestión de Riesgos , SARS-CoV-2 , Zoonosis/epidemiología , Zoonosis/prevención & controlRESUMEN
Urban-living wildlife can be exposed to metal contaminants dispersed into the environment through industrial, residential, and agricultural applications. Metal exposure carries lethal and sublethal consequences for animals; in particular, heavy metals (e.g. arsenic, lead, mercury) can damage organs and act as carcinogens. Many bat species reside and forage in human-modified habitats and could be exposed to contaminants in air, water, and food. We quantified metal concentrations in fur samples from three flying fox species (Pteropus fruit bats) captured at eight sites in eastern Australia. For subsets of bats, we assessed ectoparasite burden, haemoparasite infection, and viral infection, and performed white blood cell differential counts. We examined relationships among metal concentrations, environmental predictors (season, land use surrounding capture site), and individual predictors (species, sex, age, body condition, parasitism, neutrophil:lymphocyte ratio). As expected, bats captured at sites with greater human impact had higher metal loads. At one site with seasonal sampling, bats had higher metal concentrations in winter than in summer, possibly owing to changes in food availability and foraging. Relationships between ectoparasites and metal concentrations were mixed, suggesting multiple causal mechanisms. There was no association between overall metal load and neutrophil:lymphocyte ratio, but mercury concentrations were positively correlated with this ratio, which is associated with stress in other vertebrate taxa. Comparison of our findings to those of previous flying fox studies revealed potentially harmful levels of several metals; in particular, endangered spectacled flying foxes (P. conspicillatus) exhibited high concentrations of cadmium and lead. Because some bats harbor pathogens transmissible to humans and animals, future research should explore interactions between metal exposure, immunity, and infection to assess consequences for bat and human health.
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Quirópteros , Mercurio , Animales , Australia , Metales , Estaciones del AñoRESUMEN
Due to their geographical isolation and small populations, insular bats may not be able to maintain acute immunizing viruses that rely on a large population for viral maintenance. Instead, endemic transmission may rely on viruses establishing persistent infections within hosts or inducing only short-lived neutralizing immunity. Therefore, studies on insular populations are valuable for developing broader understanding of viral maintenance in bats. The Christmas Island flying-fox (CIFF; Pteropus natalis) is endemic on Christmas Island, a remote Australian territory, and is an ideal model species to understand viral maintenance in small, geographically isolated bat populations. Serum or plasma (n = 190), oral swabs (n = 199), faeces (n = 31), urine (n = 32) and urine swabs (n = 25) were collected from 228 CIFFs. Samples were tested using multiplex serological and molecular assays, and attempts at virus isolation to determine the presence of paramyxoviruses, betacoronaviruses and Australian bat lyssavirus. Analysis of serological data provides evidence that the species is maintaining a pararubulavirus and a betacoronavirus. There was little serological evidence supporting the presence of active circulation of the other viruses assessed in the present study. No viral nucleic acid was detected and no viruses were isolated. Age-seropositivity results support the hypothesis that geographically isolated bat populations can maintain some paramyxoviruses and coronaviruses. Further studies are required to elucidate infection dynamics and characterize viruses in the CIFF. Lastly, apparent absence of some pathogens could have implications for the conservation of the CIFF if a novel disease were introduced into the population through human carriage or an invasive species. Adopting increased biosecurity protocols for ships porting on Christmas Island and for researchers and bat carers working with flying-foxes are recommended to decrease the risk of pathogen introduction and contribute to the health and conservation of the species.
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Quirópteros , Lyssavirus , Ácidos Nucleicos , Animales , Australia/epidemiología , Betacoronavirus , HumanosRESUMEN
The black flying fox (Pteropus alecto) is a natural reservoir for Hendra virus, a paramyxovirus that causes fatal infections in humans and horses in Australia. Increased excretion of Hendra virus by flying foxes has been hypothesized to be associated with physiological or energetic stress in the reservoir hosts. The objective of this study was to explore the leukocyte profiles of wild-caught P. alecto, with a focus on describing the morphology of each cell type to facilitate identification for clinical purposes and future virus spillover research. To this end, we have created an atlas of images displaying the commonly observed morphological variations across each cell type. We provide quantitative and morphological information regarding the leukocyte profiles in bats captured at two roost sites located in Redcliffe and Toowoomba, Queensland, Australia, over the course of two years. We examined the morphology of leukocytes, platelets, and erythrocytes of P. alecto using cytochemical staining and characterization of blood films through light microscopy. Leukocyte profiles were broadly consistent with previous studies of P. alecto and other Pteropus species. A small proportion of individual samples presented evidence of hemoparasitic infection or leukocyte morphological traits that are relevant for future research on bat health, including unique large granular lymphocytes. Considering hematology is done by visual inspection of blood smears, examples of the varied cell morphologies are included as a visual guide. To the best of our knowledge, this study provides the first qualitative assessment of P. alecto leukocytes, as well as the first set of published hematology reference images for this species.
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Quirópteros , Leucocitos , Animales , Quirópteros/inmunología , Virus Hendra , QueenslandRESUMEN
A novel Hendra virus variant, genotype 2, was recently discovered in a horse that died after acute illness and in Pteropus flying fox tissues in Australia. We detected the variant in flying fox urine, the pathway relevant for spillover, supporting an expanded geographic range of Hendra virus risk to horses and humans.
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Quirópteros , Virus Hendra , Infecciones por Henipavirus , Animales , Australia/epidemiología , Virus Hendra/genética , Infecciones por Henipavirus/epidemiología , Infecciones por Henipavirus/veterinaria , CaballosRESUMEN
We identified and isolated a novel Hendra virus (HeV) variant not detected by routine testing from a horse in Queensland, Australia, that died from acute illness with signs consistent with HeV infection. Using whole-genome sequencing and phylogenetic analysis, we determined the variant had ≈83% nt identity with prototypic HeV. In silico and in vitro comparisons of the receptor-binding protein with prototypic HeV support that the human monoclonal antibody m102.4 used for postexposure prophylaxis and current equine vaccine will be effective against this variant. An updated quantitative PCR developed for routine surveillance resulted in subsequent case detection. Genetic sequence consistency with virus detected in grey-headed flying foxes suggests the variant circulates at least among this species. Studies are needed to determine infection kinetics, pathogenicity, reservoir-species associations, viral-host coevolution, and spillover dynamics for this virus. Surveillance and biosecurity practices should be updated to acknowledge HeV spillover risk across all regions frequented by flying foxes.
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Quirópteros , Virus Hendra , Infecciones por Henipavirus , Enfermedades de los Caballos , Animales , Australia/epidemiología , Virus Hendra/genética , Infecciones por Henipavirus/epidemiología , Infecciones por Henipavirus/veterinaria , Enfermedades de los Caballos/epidemiología , Caballos , Filogenia , Vigilancia de GuardiaRESUMEN
In the past two decades, three coronaviruses with ancestral origins in bats have emerged and caused widespread outbreaks in humans, including severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Since the first SARS epidemic in 2002-2003, the appreciation of bats as key hosts of zoonotic coronaviruses has advanced rapidly. More than 4,000 coronavirus sequences from 14 bat families have been identified, yet the true diversity of bat coronaviruses is probably much greater. Given that bats are the likely evolutionary source for several human coronaviruses, including strains that cause mild upper respiratory tract disease, their role in historic and future pandemics requires ongoing investigation. We review and integrate information on bat-coronavirus interactions at the molecular, tissue, host and population levels. We identify critical gaps in knowledge of bat coronaviruses, which relate to spillover and pandemic risk, including the pathways to zoonotic spillover, the infection dynamics within bat reservoir hosts, the role of prior adaptation in intermediate hosts for zoonotic transmission and the viral genotypes or traits that predict zoonotic capacity and pandemic potential. Filling these knowledge gaps may help prevent the next pandemic.