Gastrointestinal helminths may affect host susceptibility to anthrax through seasonal immune trade-offs

Abstract

BackgroundMost vertebrates experience coinfections, and many pathogen-pathogen interactions occur indirectly through the host immune system. These interactions are particularly strong in mixed micro-macroparasite infections because of immunomodulatory effects of helminth parasites. While these trade-offs have been examined extensively in laboratory animals, few studies have examined them in natural systems. Additionally, many wildlife pathogens fluctuate seasonally, at least partly due to seasonal host immune changes. We therefore examined seasonality of immune resource allocation, pathogen abundance and exposure, and interactions between infections and immunity in plains zebra (Equus quagga) in Etosha National Park (ENP), Namibia, a system with strongly seasonal patterns of gastrointestinal (GI) helminth infection intensity and concurrent anthrax outbreaks. Both pathogens are environmentally transmitted, and helminth seasonality is driven by environmental pressures on free living life stages. The reasons behind anthrax seasonality are currently not understood, though anthrax is less likely directly driven by environmental factors.ResultsWe measured a complex, interacting set of variables and found evidence that GI helminth infection intensities, eosinophil counts, IgE and IgGb antibody titers, and possibly IL-4 cytokine signaling were increased in wetter seasons, and that ectoparasite infestations and possibly IFN-γ cytokine signaling were increased in drier seasons. Monocyte counts and anti-anthrax antibody titers were negatively associated with wet season eosinophilia, and monocytes were negatively correlated with IgGb and IgE titers. Taken together, this supports the hypothesis that ENP wet seasons are characterized by immune resource allocation toward Th-2 type responses, while Th1-type immunity may prevail in drier seasons, and that hosts may experience Th1-Th2 trade-offs. We found evidence that this Th2-type resource allocation is likely driven by GI parasite infections, and that these trade-offs may render hosts less capable of concurrently mounting effective Th1-type immune responses against anthrax.ConclusionsThis study is one of the first to examine laboratory-demonstrated Th1-Th2 trade-offs in a natural system. It provides evidence that seasonally bound pathogens may affect, through immunology, transmission dynamics of pathogens that might otherwise not be seasonally distributed. It suggests that, by manipulating the internal host ecosystem, GI parasites may influence the external ecosystem by affecting the dynamics of another environmentally transmitted pathogen.Electronic supplementary materialThe online version of this article (doi:10.1186/s12898-014-0027-3) contains supplementary material, which is available to authorized users.

The global distribution of Bacillus anthracis and associated anthrax risk to humans, livestock and wildlife

“…Across countries and continents, anthrax dynamics are often seasonal, although this may range from predictable annual outbreaks to sporadic, high-mortality epizootics 12,23,[28][29][30][31] . The timing and intensity of seasonality are far from consistent across space, even on the same continent 1,5 , and the underlying drivers are a complex product of local climate and soil conditions, herbivore community structure and seasonal movement dynamics, and co-morbidity with other pathogens 23,[32][33][34] . Several recently advanced spatiotemporal modelling methods can capture and infer complex seasonal drivers of zoonotic spillover 35,36 , but in application to anthrax, these models would be most appropriate at spatial scales where these drivers are consistent across the landscape 37 .…”

Using movement data to estimate contact rates in a simulated environmentally-transmitted disease system

“…For example, zebra in Etosha National Park in Namibia experience peaks in infection during the warm wet season (March-April), whereas elephants are more likely to be infected during the dry months of October-November [35]. A definitive explanation for these peaks remains elusive, but a number of alternatives have been proposed, including nutritional stress, heterogeneous soil ingestion rates [33], and complex coinfection dynamics [39,40].…”

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

“…A similar key problem is that anthrax infections exist in an ecosystem of pathogens, and the within‐host role that co‐infection plays in anthrax immunology is complicated at best. Field studies in Etosha have shown apparent trade‐offs in zebra between helper T cell class 1 (Th‐1) and 2 (Th‐2) type immune responses, where Th‐2 responses seem to peak in the wet season in response to gastrointestinal helminths (Cizauskas et al ., ). These immune responses appear to make zebra and springbok more tolerant of helminth infections when they peak during the wet season, decreasing host resistance to anthrax infection and thereby potentially contributing to the overall seasonality of anthrax outbreaks (Cizauskas et al ., ).…”