Kristine L. Metzger, Katie Hampson, Sarah Cleaveland, Karen Stamey, Craig Packer, Tiziana Lembo, Harriet Auty, Paul R. Bessell, Christine Mentzel, Patricia P. Wilkins, Robert D. Fyumagwa, Richard Hoare, Keith Roberts, Titus Mlengeya, Eblate Ernest, Jo E. B. Halliday, and Cari A. Beesley
Anthrax is endemic throughout Africa, causing considerable livestock and wildlife losses and severe, sometimes fatal, infection in humans. Predicting the risk of infection is therefore important for public health, wildlife conservation and livestock economies. However, because of the intermittent and variable nature of anthrax outbreaks, associated environmental and climatic conditions, and diversity of species affected, the ecology of this multihost pathogen is poorly understood. We explored records of anthrax from the Serengeti ecosystem in north-west Tanzania where the disease has been documented in humans, domestic animals and a range of wildlife. Using spatial and temporal case-detection and seroprevalence data from wild and domestic animals, we investigated spatial, environmental, climatic and species-specific associations in exposure and disease. Anthrax was detected annually in numerous species, but large outbreaks were spatially localized, mostly affecting a few focal herbivores. Soil alkalinity and cumulative weather extremes were identified as useful spatial and temporal predictors of exposure and infection risk, and for triggering the onset of large outbreaks. Interacting ecological and behavioural factors, specifically functional groups and spatiotemporal overlap, helped to explain the variable patterns of infection and exposure among species. Synthesis and applications. Our results shed light on ecological drivers of anthrax infection and suggest that soil alkalinity and prolonged droughts or rains are useful predictors of disease occurrence that could guide risk-based surveillance. These insights should inform strategies for managing anthrax including prophylactic livestock vaccination, timing of public health warnings and antibiotic provision in high-risk areas. However, this research highlights the need for greater surveillance (environmental, serological and case-detection-orientated) to determine the mechanisms underlying anthrax dynamics. Keywords: Bacillus anthracis, disease ecology, exposure, infectious disease, multihost, serology, surveillance, susceptibility, zoonosis Introduction Bacillus anthracis (Cohn), the causative agent of anthrax, is a multihost pathogen affecting human, livestock and wildlife populations. The disease has a world-wide distribution, but has declined in many developed countries because of the implementation of livestock vaccination programmes and sanitary measures. However, anthrax is still endemic in Africa, with severe outbreaks causing significant losses in domestic and wild animal populations (Prins & Weyerhaeuser 1987; Shiferaw et al. 2002; Siamudaala 2006; Clegg et al. 2007; Wafula, Patrick & Charles 2008). Non-fatal cutaneous anthrax acquired through contact with infected carcasses or animal products accounts for >95% of all reported human cases globally (World Health Organization 2008). More severe forms, particularly gastrointestinal anthrax because of handling and consumption of inadequately cooked products from infected animals, may also exert a substantial burden that is both underreported and under-diagnosed (Sirisanthana & Brown 2002). Predicting the risk of infection is therefore important from the perspectives of public health, wildlife conservation and livestock economies. Despite the infamous reputation of anthrax, the ecology and transmission of the disease under natural conditions are not well understood (Hugh-Jones & de Vos 2002). The difficulty lies in the intermittent and variable nature of outbreaks, with considerable variation in the species affected, and associated environmental and climatic conditions (Table 1). Table 1 Anthrax outbreaks in Eastern and Southern Africa for which details were available. Predominant species are emboldened, followed by species in which > 5 cases were documented The life cycle of B. anthracis comprises a multiplication phase in the mammalian host and a persistence phase of spores in the soil. Transmission to herbivores largely occurs indirectly, so risk factors are usually associated with exposure to spores, rather than direct animal-to-animal transmission. Survival mechanisms of the pathogen outside the host remain unclear. Bacillus anthracis has been shown to be associated with plant roots (Saile & Koehler 2006), and this is suggested to be an adaptation that increases the likelihood of infecting ungulate hosts (Raymond et al. 2010). Certain environmental factors affect long-term spore survival and thus increase the risk of anthrax (Blackburn et al. 2007). For example, the endemicity of B. anthracis in some areas has been associated with calcium-rich and neutral-to-alkaline soils (van Ness 1971; Dragon et al. 2005; Hugh-Jones & Blackburn 2009), although strain differences exist in soil chemistry preferences (Smith et al. 2000). Strain differences, in fact, may also govern spread in anthrax epidemics (Blackburn et al. 2007; Garofolo et al. 2010). Seasonal incidence patterns suggest climatic factors (precipitation and ambient temperature) play an important role in triggering outbreaks, although these are not consistent between locations (Table 1), and therefore underlying mechanisms are debated. In some African ecosystems, outbreaks have been reported late in the dry season (Prins & Weyerhaeuser 1987; Turnbull et al. 1991; Lindeque & Turnbull 1994; de Vos & Bryden 1996; Shiferaw et al. 2002; Clegg et al. 2007; Muoria et al. 2007), leading to suggestions that transmission may be facilitated by close grazing, nutritional stress and congregation at water holes (Hugh-Jones & de Vos 2002). Elsewhere, outbreaks have been associated with heavy rains (Lindeque & Turnbull 1994; Mlengeya et al. 1998; Wafula, Patrick & Charles 2008; Bellan 2010), which are hypothesized to unearth spores and amplify vector populations (Durrheim et al. 2009; Hugh-Jones & Blackburn 2009; Lewerin et al. 2010). Experimental spore germination and vegetative growth in the rhizosphere provide a mechanism by which bursts of rainfall could spark epidemics (Saile & Koehler 2006). This would parsimoniously explain anthrax occurrences during dry summers in North America and Australia that have been preceded by rains and when animals are often in good body condition (Turner et al. 1999; Hugh-Jones & de Vos 2002; Parkinson, Rajic & Jenson 2003; Hugh-Jones & Blackburn 2009; Epp, Waldner & Argue 2010). Although anthrax infects a wide range of species, outbreaks are typically associated with just a few (Table 1), for example impala Aepyceros melampus, kudu Tragelaphus strepsiceros, buffalo Syncerus caffer and zebra Equus spp. (Prins & Weyerhaeuser 1987; Mlengeya et al. 1998; Clegg et al. 2007; Muoria et al. 2007; Wafula, Patrick & Charles 2008). Even within a single ecosystem, different species may be affected at different times (Lindeque & Turnbull 1994). Reasons for this remain unclear, but could be attributed to host-specific differences in susceptibility and exposure as a result of behavioural and ecological traits as well as differences in pathogen strains. The overall ecological and genetic factors that contribute to environmental persistence of anthrax, and the underlying conditions that initiate outbreaks and underlie patterns of circulation are poorly known. In the Serengeti ecosystem, anthrax has been reported in a variety of species, with sporadic outbreaks occurring in relatively localized endemic foci and mostly affecting a few focal species (Lembo et al. 2011). The ecosystem covers a large area (over 20 000 km2, Sinclair et al. 2008) encompassing a variety of habitats and environmental gradients, which may influence anthrax occurrence. Here, we draw on data gathered opportunistically including serology indicative of exposure and case reports from human, domestic and wild animal populations in the greater Serengeti ecosystem, to explore ecological factors affecting infection patterns in a range of species. Combined, the investigation into environmental and climatic predictors of anthrax and their associations with species-specific patterns of exposure and mortality provides a holistic picture of ecological drivers of anthrax dynamics and identifies priorities for further research in anthrax endemic ecosystems.