Sampling to elucidate the dynamics of infections in reservoir hosts

Plowright, Raina K.; Becker, Daniel J.; McCallum, Hamish; Manlove, Kezia R.

doi:10.1098/rstb.2018.0336

Cited by 77 publications

(92 citation statements)

References 84 publications

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“…Quantifying spatial dependence can also assist with sampling designs, which often involve trade‐offs between spatial and temporal replication (Plowright, Becker, McCallum, & Manlove, ). Researchers may first decide to intensively sample over space but at a fixed time.…”

Section: Spatial Statistical Methods For Ecoimmunologymentioning

confidence: 99%

“…Similarly, large-scale studies that identify urbanization as a key determinant of immunity (e.g. could be followed by field experiments to further differentiate the roles of improved food availability from other ecological factors such as infection or population size (Pedersen & Greives, 2008).…”

Section: Methodological Recommendationsmentioning

confidence: 99%

“…Although incorporating seasonality into macroimmunology may not always be feasible given trade‐offs between spatial and temporal sampling, we also implore researchers to consider time when standardizing efforts over space. Spatial patterns can be obscured, or artificially produced, if sites are sampled at different months or years or use different protocols (Plowright et al, ). For ecoimmunology, factors such as the time between capture and sampling and time between sample collection and assays can also introduce additional noise (Becker, Czirják, Rynda‐Apple, & Plowright, ; Zylberberg, ).…”

Section: Future Directions For Macroimmunologymentioning

confidence: 99%

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Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence

Becker

Albery

Kessler

et al. 2020

Journal of Animal Ecology

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101

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The prevalence and intensity of parasites in wild hosts varies across space and is a key determinant of infection risk in humans, domestic animals and threatened wildlife. Because the immune system serves as the primary barrier to infection, replication and transmission following exposure, we here consider the environmental drivers of immunity. Spatial variation in parasite pressure, abiotic and biotic conditions, and anthropogenic factors can all shape immunity across spatial scales. Identifying the most important spatial drivers of immunity could help pre‐empt infectious disease risks, especially in the context of how large‐scale factors such as urbanization affect defence by changing environmental conditions. We provide a synthesis of how to apply macroecological approaches to the study of ecoimmunology (i.e. macroimmunology). We first review spatial factors that could generate spatial variation in defence, highlighting the need for large‐scale studies that can differentiate competing environmental predictors of immunity and detailing contexts where this approach might be favoured over small‐scale experimental studies. We next conduct a systematic review of the literature to assess the frequency of spatial studies and to classify them according to taxa, immune measures, spatial replication and extent, and statistical methods. We review 210 ecoimmunology studies sampling multiple host populations. We show that whereas spatial approaches are relatively common, spatial replication is generally low and unlikely to provide sufficient environmental variation or power to differentiate competing spatial hypotheses. We also highlight statistical biases in macroimmunology, in that few studies characterize and account for spatial dependence statistically, potentially affecting inferences for the relationships between environmental conditions and immune defence. We use these findings to describe tools from geostatistics and spatial modelling that can improve inference about the associations between environmental and immunological variation. In particular, we emphasize exploratory tools that can guide spatial sampling and highlight the need for greater use of mixed‐effects models that account for spatial variability while also allowing researchers to account for both individual‐ and habitat‐level covariates. We finally discuss future research priorities for macroimmunology, including focusing on latitudinal gradients, range expansions and urbanization as being especially amenable to large‐scale spatial approaches. Methodologically, we highlight critical opportunities posed by assessing spatial variation in host tolerance, using metagenomics to quantify spatial variation in parasite pressure, coupling large‐scale field studies with small‐scale field experiments and longitudinal approaches, and applying statistical tools from macroecology and meta‐analysis to identify generalizable spatial patterns. Such work will facilitate scaling ecoimmunology from individual‐ to habitat‐level insights about the drivers of immu...

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Section: Spatial Statistical Methods For Ecoimmunologymentioning

confidence: 99%

Section: Methodological Recommendationsmentioning

confidence: 99%

Section: Future Directions For Macroimmunologymentioning

confidence: 99%

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Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence

Becker

Albery

Kessler

et al. 2020

Journal of Animal Ecology

Self Cite

101

122

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“…In the longer term, understanding of the spatial and temporal distribution of infection within vectors and reservoir hosts and their consequent roles in transmission is crucial to predicting spillover and establishing interventions that target non-human barriers [85]. Indeed, the complexity of zoonotic disease dynamics, combined with restrictions imposed by funding and resource availability, favours the focus of most interventions for neglected tropical zoonoses on human barriers to spillover.…”

Section: Discussionmentioning

confidence: 99%

Reviewing the Ecological Evidence-Base for Management of Emerging Tropical Zoonoses: Kyasanur Forest Disease in India as A Case Study

Burthe

Schäfer

Asaaga

et al. 2020

Preprint

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Background Zoonotic diseases disproportionately affect poor tropical communities. Transmission dynamics of zoonoses are complex, involving communities of vector and animal hosts, with human behaviour and ecosystem use altering exposure to infected vectors and hosts. This complexity means that efforts to manage and prevent human spillover are often hampered by a poor ecological evidence base and intervention strategies tend to focus on humans (e.g. vaccination, preventative drug treatment). However, integrating ecological and evolutionary understanding of multi-vector and host transmission, human and environmental factors into disease control policy is essential. Recent frameworks have been developed to guide appropriate design of “ecological interventions” which have the potential for being more long-term, effective and economical approaches to managing human disease.Results We extended new frameworks to identify the hierarchical series of barriers that need to be overcome by a vector-borne pathogen to facilitate human spillover, focusing on an emerging, tick-borne zoonotic pathogen in India, Kyasanur Forest Disease Virus (KFDV). Current management recommendations focus on human barriers, through personal protection and vaccination, as well as targeting vector control on cattle and at the sites of monkey deaths. Assessment of the validity of current management practices for KFD through literature review and interviews with disease managers found the efficacy of interventions difficult to quantify, due to poor empirical evidence and a lack of understanding of KFDV-vector-host ecology, particularly regarding the role of cattle in amplifying tick populations and the spatial scale of risk arising from ticks infected via monkeys, which are considered to be amplifying hosts for KFDV. The spraying of malathion around dead monkeys and the burning of vegetation to reduce tick abundance were particularly unfounded interventions. The need for community guidance and education in best practice for tick-prevention and improved vaccine efficacy and surveillance were also identified. We highlight 18 urgent research priorities and identify those which could refine current management strategies or facilitate ecological interventions targeting vectors and host barriers to spillover in the future. Conclusions We emphasise that inter-disciplinary One Health approaches involving collaboration across diverse disciplines including ecology, epidemiology, animal and public health, health systems and social sciences, and with meaningful involvement of local communities, are necessary to refine predictive models of spillover, develop new interventions and target vaccination strategies and surveillance more effectively. Applying such approaches to understand the complex ecological systems involved in zoonotic spillover, and refine and develop appropriate management interventions, including ecological interventions targeting non-human barriers, will ultimately lead to more sustainable and long-term reductions in human cases of neglected zoonoses in the future.

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“…Understanding the interplay between these factors is a crucial first step toward reducing human incidence. Upstream factors include the level of environmental contamination (in turn governed by disease ecology in the animal host population [4]), and human exposures to contaminated & 2019 The Author(s) Published by the Royal Society. All rights reserved.…”

Section: Introductionmentioning

confidence: 99%

Mechanistic dose–response modelling of animal challenge data shows that intact skin is a crucial barrier to leptospiral infection

Gostic

Wunder

Bisht

et al. 2019

Phil. Trans. R. Soc. B

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Leptospirosis is a widespread and potentially life-threatening zoonotic disease caused by spirochaetes of the genus Leptospira . Humans become infected primarily via contact with environmental reservoirs contaminated by the urine of shedding mammalian hosts. Populations in high transmission settings, such as urban slums and subsistence farming communities, are exposed to low doses of Leptospira on a daily basis. Under these conditions, numerous factors determine whether infection occurs, including the route of exposure and inoculum dose. Skin wounds and abrasions are risk factors for leptospirosis, but it is not known whether broken skin is necessary for spillover, or if low-dose exposures to intact skin and mucous membranes can also cause infection. To establish a quantitative relationship between dose, route and probability of infection, we performed challenge experiments in hamsters and rats, developed mechanistic dose–response models representing the spatial dynamics of within-host infection and persistence, and fitted models to experimental data. Results show intact skin is a strong barrier against infection, and that broken skin is the predominant route by which low-dose environmental exposures cause infection. These results identify skin integrity as a bottleneck to spillover of Leptospira and underscore the importance of barrier interventions in the prevention of leptospirosis. This article is part of the theme issue ‘Dynamic and integrative approaches to understanding pathogen spillover’.

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Sampling to elucidate the dynamics of infections in reservoir hosts

Cited by 77 publications

References 84 publications

Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence

Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence

Reviewing the Ecological Evidence-Base for Management of Emerging Tropical Zoonoses: Kyasanur Forest Disease in India as A Case Study

Mechanistic dose–response modelling of animal challenge data shows that intact skin is a crucial barrier to leptospiral infection

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