No Worm Is an Island; The Influence of Commensal Gut Microbiota on Cyathostomin Infections

Abstract

The importance of the gut microbiome for host health has been the subject of intense research over the last decade. In particular, there is overwhelming evidence for the influence of resident microbiota on gut mucosal and systemic immunity; with significant implications for the outcome of gastrointestinal (GI) infections, such as parasitic helminths. The horse is a species that relies heavily on its gut microbiota for GI and overall health, and disturbances in this complex ecosystem are often associated with life-threatening disease. In turn, nearly all horses harbour parasitic helminths from a young age, the most prevalent of which are the small strongyles, or cyathostomins. Research describing the relationship between gut microbiota and cyathostomin infection is in its infancy, however, to date there is evidence of meaningful interactions between these two groups of organisms which not only influence the outcome of cyathostomin infection but have long term consequences for equine host health. Here, we describe these interactions alongside supportive evidence from other species and suggest novel theories and avenues for research which have the potential to revolutionize our approach to cyathostomin prevention and control in the future.

Species interactions, stability, and resilience of the gut microbiota - Helminth assemblage in horses

“…However, the microbial interacting network remained less stable for six weeks after treatment because of changes in interaction strength and population dynamics, evoking a likely effect of successive larvae emergence into the gut lumen after post-adulticide treatment. 31 As such, these observations expand past studies focused on the consequences of parasite infection 6 , 17 , 39 , 92 or anthelmintic treatment on the host gut microbiota composition. 5 , 18 , 19 , 21 , 22 , 37 , 44 , 93 , 94 , 95 The ecosystem instability following anthelmintic treatment and parasite removal is compatible with the “Anna Karenina principle”, where uneasy communities vary more strongly than non-challenged communities, 96 and environmental changes can more easily tip the balance, especially in aged hosts experiencing recurrent infections and regularly subjected to prophylactic anthelmintic treatments.…”

“…Still, these patterns of gut microbial shifts do not reflect the ecosystem dynamics and the qualitative nature of the interactions between species. 28 , 29 , 30 , 31 , 32 , 33 , 34 The characterization of the interactions between microbial and parasite species in helminth-infected hosts is largely unknown. Evidence for direct interactions between helminth and gut microbial species mainly bear on the reciprocal feedback between Lactobacillaceae and Heligmosomoides polygyrus 3 or Trichuris muris in mice, 35 as well as the need for gut microbiota attachment to T. muris egg caps for triggering worm hatching.…”

Pathophysiology of exertional heat illness in the Thoroughbred racehorse: Broadening perspective to include an exercise‐induced gastrointestinal syndrome in which endotoxaemia and systemic inflammation may contribute to the condition

“…There is evidence that probiotics, glutamine and Vitamin C may be useful in that setting (Shing et al, 2014). So too, in horses there has been recent interest in the role of the GIT as it affects overall health (Garber et al, 2020;Stewart et al, 2017), undergoes alterations in relation to intense physical exercise (Plancade et al, 2019), changes its microbiota associated with microbial drug administration (Costa et al, 2015), interacts with its parasitic population (Walsh et al, 2020) and modifies some behavioural traits in equine athletes (Mach et al, 2020). Lindinger (2019) has published an extensive review of nutritional approaches to maintaining healthy intestinal barrier function, to which the reader is referred.…”

Molecular Species Determination of Cyathostomins from Horses in Ireland

“…Horses may tolerate light cyathostomin infection without the development of overt clinical signs (Love et al ., 1999; Morariu et al ., 2016; Murphy and Love, 1997; Walshe et al ., 2021). However, high burdens can lead to ill-thrift and poor performance (Murphy and Love, 1997) and in some cases a specific clinical presentation of acute larval cyathostominosis (ALC), which develops in response to synchronous emergence of larvae from the mucosa and involves severe local and systemic inflammation, with high morbidity and potential mortality (Hodgkinson et al ., 2003; Love et al ., 1999; Walshe et al ., 2020). The emergence of encysted cyathostomin larvae is believed to be affected by many factors, including negative inhibition from an established adult worm population, removed following anthelmintic treatment (Steinbach et al ., 2006; Walshe et al ., 2019; Walshe et al ., 2021).…”