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Abstract
Polyphenols are a class of bioactive plant secondary metabolites that are thought to have beneficial effects on gut health, such as modulation of mucosal immune and inflammatory responses and regulation of parasite burdens. Here, we examined the interactions between a polyphenol-rich diet supplement and infection with the enteric nematode Ascaris suum in pigs. Pigs were fed either a basal diet or the same diet supplemented with grape pomace (GP), an industrial by-product rich in polyphenols such as oligomeric proanthocyanidins. Half of the animals in each group were then inoculated with A. suum for 14 days to assess parasite establishment, acquisition of local and systemic immune responses and effects on the gut microbiome. Despite in vitro anthelmintic activity of GP-extracts, numbers of parasite larvae in the intestine were not altered by GP-supplementation. However, the bioactive diet significantly increased numbers of eosinophils induced by A. suum infection in the duodenum, jejunum and ileum, and modulated gene expression in the jejunal mucosa of infected pigs. Both GP-supplementation and A. suum infection induced significant and apparently similar changes in the composition of the prokaryotic gut microbiota, and both also decreased concentrations of isobutyric and isovaleric acid (branched-chain short chain fatty acids) in the colon. Our results demonstrate that while a polyphenol-enriched diet in pigs may not directly influence A. suum establishment, it significantly modulates the subsequent host response to helminth infection. Our results suggest an influence of diet on immune function which may potentially be exploited to enhance immunity to helminths.
Highlights
The effect of diet on gastrointestinal health and immune function in animals is an area of intense interest, in part due to the need to increase health and production without recourse to synthetic antibiotics and anti-parasitic drugs
Anthelmintic activity of grape pomace against Ascaris suum in vitro and in vivo We have previously observed that purified PAC molecules have direct anthelmintic effects in vitro against A. suum larvae in a polymerisation-dependent manner [6]
Consistent with our previous studies using PAC-rich extracts from a range of plants [6], acetone-water extracts prepared from grape pomace (GP) showed dose-dependent in vitro anthelmintic activity against A. suum L3
Summary
The effect of diet on gastrointestinal health and immune function in animals is an area of intense interest, in part due to the need to increase health and production without recourse to synthetic antibiotics and anti-parasitic drugs. More than a billion people are estimated to be infected with soil-transmitted helminths such as Ascaris lumbricoides, Trichuris trichiura and hookworms, and helminths are present in virtually all livestock production systems of economic importance, causing reduced growth rates and feed conversion ratios in both ruminants and monogastric animals such as pigs and horses [1, 2]. Antimicrobial effects of polyphenols are well-known; PAC- or ellagitannin-containing diets have been shown to effectively reduce helminth infection in sheep, goats, and cattle [9,10,11], and PAC-rich supplements have shown promise in controlling gut pathogens in pigs such as Escherichia coli [12, 13]
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