Lethal exposure: An integrated approach to pathogen transmission via environmental reservoirs

Abstract

To mitigate the effects of zoonotic diseases on human and animal populations, it is critical to understand what factors alter transmission dynamics. Here we assess the risk of exposure to lethal concentrations of the anthrax bacterium, Bacillus anthracis, for grazing animals in a natural system over time through different transmission mechanisms. We follow pathogen concentrations at anthrax carcass sites and waterholes for five years and estimate infection risk as a function of grass, soil or water intake, age of carcass sites, and the exposure required for a lethal infection. Grazing, not drinking, seems the dominant transmission route, and transmission is more probable from grazing at carcass sites 1-2 years of age. Unlike most studies of virulent pathogens that are conducted under controlled conditions for extrapolation to real situations, we evaluate exposure risk under field conditions to estimate the probability of a lethal dose, showing that not all reservoirs with detectable pathogens are significant transmission pathways.Understanding the ecological processes that drive zoonotic disease outbreaks is important in mitigating their effects on human and animal populations. One critical factor affecting infectious disease dynamics is spatio-temporal heterogeneity in transmission 1,2 . For directly transmitted pathogens, this heterogeneity can be described through peer to peer contact rates and the structure of social networks in host populations [3][4][5] . When pathogens are acquired from environmental reservoirs, the pathogen's distribution in the environment and the interaction between host behavior and reservoir becomes the crucial link in transmission. Despite the global burden of diseases with environmental reservoirs (like cholera, tularemia, polio, botulism, anthrax, bubonic plague, leptospirosis, enteropathogenic E. coli and others 6 ), microbial ecology in the field is currently understudied due to the difficulties of monitoring microbes in their natural environment. Though progress is being made in risk assessment studies, more data are needed on diseases currently posing threats to public health, livestock health, and wildlife health. Moreover, to calibrate the risk and thus an appropriate response to emerging diseases following environmental change or the release of bioweapons, we need to know their long-term behavior in natural systems.The distribution of infectious agents in the environment is typically aggregated due to pulsed releases from infected hosts, creating heterogeneity in the risk of exposure for future hosts. Public health scientists assess risk of infection by identifying disease agents, quantifying exposure, and characterizing dose-response relationships 7,8 .

Spores and soil from six sides: interdisciplinarity and the environmental biology of anthrax (Bacillus anthracis)

“…Transmission takes place through several pathways, the primary one for ungulates being ingestion of B. anthracis spores during feeding at carcass sites (Hugh‐Jones & De Vos, ; Hugh‐Jones & Blackburn, ; Turner et al , ). Other potential pathways include ingesting emesis and faeces deposited by necrophagous flies on vegetation after these flies have fed on hosts that have died of anthrax (Blackburn et al , ), inhaling anthrax spores that have become airborne [in nature occurring from dust‐bathing hosts, although recent evidence casts doubt on this (Barandongo, Mfune & Turner, )], waterborne transmission from waterholes and temporary ponds (Turner et al , ), cutaneous routes, which account for the majority of human clinical cases globally (Shadomy & Smith, ), and gastrointestinal infections from eating infected meat and blood directly (Bales et al , ; Hugh‐Jones & De Vos, ; Beatty et al , ; Hugh‐Jones & Blackburn, ). In some regions, anthrax outbreaks are a consistent and predictable feature of ecosystems and occur regularly on a seasonal cycle; in other settings, epizootics are infrequent or rare events, and can be responsible for mass die‐offs among wildlife and livestock (Lindeque & Turnbull, ; Hugh‐Jones & De Vos, ; Hoffmann et al , ).…”

“…Studies in Etosha have provided the tools to begin to develop models that cross these different scales, and thereby unravel the false 'lethal dose paradox', in which the experimentally determined lethal dose required to kill herbivores appears to be far higher than would be encountered in nature (Turner et al, 2016). Work that combines field experiments and modelling shows that, especially in the first 2 years after deposition, carcasses should provide ample infection risk for grazing herbivores, even when soil ingestion is minimal (Turner et al, 2016). Even though spore concentrations begin to decline rapidly after 2 years, they may still be sufficient to produce sporadic outbreaks, especially in drought years that intensify herbivore soil contact during grazing.…”

“…Even though spore concentrations begin to decline rapidly after 2 years, they may still be sufficient to produce sporadic outbreaks, especially in drought years that intensify herbivore soil contact during grazing. These small outbreaks may set off (and often precede) epidemic years, illustrating how the long tail of LIZ persistence could ultimately play an important role in long-term anthrax dynamics (Turner et al, 2016). Studies like this allow future work that considers the epidemiology of anthrax at large scales more explicitly, such as by using agent-based models to simulate the effects of host heterogeneity and landscape structure on outbreak dynamics, and measuring the relative utility of different host movement metrics as predictors of anthrax risk.…”

Zebra migration strategies and anthrax in Etosha National Park, Namibia

“…Rather, anthrax in herbivores in ENP is contracted by ingesting soil laden with infectious B. anthracis spores while grazing (Turner et al. ).…”

“…In ENP, the notion that animals are infected by inhalation of airborne spores was rejected (Turnbull et al 1998). Rather, anthrax in herbivores in ENP is contracted by ingesting soil laden with infectious B. anthracis spores while grazing (Turner et al 2016).…”