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

Annals of Occupational and Environmental Medicine

Carrie A Cizauskas⁶  Wendy C Turner²  Bettina Wagner⁴  Martina Küsters¹  Russell E Vance⁵  Wayne M Getz³ 

[1] Ministry of Environment and Tourism, Windhoek, Namibia

[2] Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Oslo, Norway

[3] School of Mathematical Sciences, University of KwaZulu-Natal, Durban, South Africa

[4] Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA

[5] Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA, USA

[6] Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA

关键词: Seasonality;    Disease ecology;    Coinfections immunological trade-offs;    Microparasites;    Host-parasite interactions;    Endoparasites;    Ecological immunology;    Bacteria;   

Others  :  1084637
DOI  :  10.1186/s12898-014-0027-3

 received in 2014-07-21, accepted in 2014-10-03,  发布年份 2014

【 摘 要 】

Background

Most 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.

Results

We 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.

Conclusions

This 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.

【 授权许可】

   
2014 Cizauskas et al.; licensee BioMed Central Ltd.

【 图 表 】

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