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Review
. 2024 Mar 26;15(1):2577.
doi: 10.1038/s41467-024-46151-9.

Ecological countermeasures to prevent pathogen spillover and subsequent pandemics

Raina K Plowright  1 , Aliyu N Ahmed  2 , Tim Coulson  3 , Thomas W Crowther  4 , Imran Ejotre  5 , Christina L Faust  6 , Winifred F Frick  7   8 , Peter J Hudson  9 , Tigga Kingston  10 , P O Nameer  11 , M Teague O'Mara  7 , Alison J Peel  12 , Hugh Possingham  13 , Orly Razgour  14 , DeeAnn M Reeder  15 , Manuel Ruiz-Aravena  16   12   17 , Nancy B Simmons  18 , Prashanth N Srinivas  19 , Gary M Tabor  20 , Iroro Tanshi  21   22   23 , Ian G Thompson  24 , Abi T Vanak  25   26 , Neil M Vora  27 , Charley E Willison  16 , Annika T H Keeley  20
Affiliations
Review

Ecological countermeasures to prevent pathogen spillover and subsequent pandemics

Raina K Plowright et al. Nat Commun. .

Abstract

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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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Primary pandemic prevention, secondary pandemic prevention, and pandemic response.
Primary pandemic prevention is the set of actions taken to reduce the risk of pathogen spillover from animals to humans, focusing on processes upstream of the spillover event (left panel). By contrast, secondary pandemic prevention (middle panel) focuses on limiting the spread of an outbreak to prevent its escalation into an epidemic or a pandemic. Pandemic response (right panel) involves actions taken to address a pandemic once one is underway. Although not illustrated here, pandemic preparedness involves developing capabilities to respond to a pandemic if one were to occur, and can be implemented concurrently with primary and secondary pandemic prevention. The nature of interventions varies across these phases: Primary pandemic prevention emphasizes ecological and behavioral interventions, but also encompasses biosafety practices in virological research, whereas secondary pandemic prevention and response prioritize epidemiological and biomedical interventions. Definitions: an outbreak is “an increase, often sudden, in the number of cases of a disease in a particular area”; an epidemic is an outbreak extending over a wider geographic area; and a pandemic is “an epidemic occurring worldwide, or over a very wide area, crossing international boundaries and usually affecting a large number of people”.
Fig. 2
Fig. 2. Land use-induced spillover and ecological countermeasures.
Historic (left panel): Historically, reservoir hosts and large human populations (and their domestic animals) were more separated, viruses circulated at low levels with seasonal fluctuations in prevalence, and the holes in the barriers to spillover were small and did not align. Land use-induced spillover (middle panel): Land-use change increases the risk of spillover by driving two phenotypic changes in reservoir hosts: changes in behavior that alter how they use space, and changes in reservoir host energy and stress levels (allostatic load) that influence viral infection and shedding. Land-use change can also lead to emergent human behaviors that increase exposure to pathogens. Land-use change generally increases the overlap of reservoir, human, and bridging hosts; increases the probability that reservoir hosts are shedding pathogens; and increases the probability that humans are exposed to those pathogens. In sum, these changes increase the size and alignment of the holes in the barrier to spillover. Ecological countermeasures (right panel): Ecological countermeasures can address all three issues. Retaining natural resources reduces the overlap of humans and domestic recipient hosts in space and time, reduces the probability of allostatic overload and reduces the likelihood of emergent human behaviors that facilitate exposure.
Fig. 3
Fig. 3. Allostatic overload as a key driver of pathogen spillover.
Bats have evolved mechanisms to meet their exceptionally high energy needs under prevailing environmental conditions. A Baseline levels of energy (green) are required for basic daily activities – to fuel cells, to move around, to find food and water, and to maintain the immune system. At any given time, a certain amount of food - or energy - is available (blue+purple+green), which varies seasonally. Bats optimize their energy intake and energy expenditure, timing expensive activities like migration and reproduction (purple) to periods in which more food is available. Under normal conditions, an energetic buffer (blue) exists providing energetic wiggle room for years with poor food availability. B Perturbations in the environment, whether natural (e.g., fire in some instances) or man-made (e.g., downstream effects of global climate change, habitat destruction, etc.) increase the amount of energy needed for survival and reproduction. For example, animals may be required to travel greater distances to locate food and resting sites. Such increased exertion diminishes the energetic buffer that enables them to withstand periods of resource scarcity. C At its worst, these perturbations result in a reversal of fortune; less energy is available than the bat needs. In these conditions, or with disturbance or harassment, animals experience allostatic overload (red). This leads to suppression of immune function, and increased susceptibility to viral infection and shedding. Figure adapted, in part, from concepts in.
Fig. 4
Fig. 4. Proposed ecological countermeasures over different spatial scales and land-use intensity gradients.
We propose a tiered approach that considers the land-use context surrounding the habitats of reservoir hosts. Because the next pandemic is most likely to be triggered by a pathogen that is currently limited in its exposure to human populations, the highest priority should be to preserve intact ecosystems and enhance their resilience through restoration and increasing connectivity. In regions where humans and reservoir hosts share landscapes, we prioritize the safeguarding of critical areas needed for reservoir hosts’ feeding, resting, and social aggregation. Simultaneously, we aim to protect human communities and livestock most at risk of exposure to zoonotic pathogens.
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