Abstract

BackgroundIn the animal production sector, enteritis is responsible for serious economic losses, and intestinal parasitism is a major stress factor leading to malnutrition and lowered performance and animal production efficiency. The effect of enteric parasites on the gut function of teleost fish, which represent the most ancient bony vertebrates, is far from being understood. The intestinal myxozoan parasite Enteromyxum leei dwells between gut epithelial cells and causes severe enteritis in gilthead sea bream (Sparus aurata), anorexia, cachexia, growth impairment, reduced marketability and increased mortality.MethodsThis study aimed to outline the gut failure in this fish-parasite model using a multifaceted approach and to find and validate non-lethal serum markers of gut barrier dysfunction. Intestinal integrity was studied in parasitized and non-parasitized fish by immunohistochemistry with specific markers for cellular adhesion (E-cadherin) and tight junctions (Tjp1 and Cldn3) and by functional studies of permeability (oral administration of FITC-dextran) and electrophysiology (Ussing chambers). Serum samples from parasitized and non-parasitized fish were analyzed using non-targeted metabolomics and some significantly altered metabolites were selected to be validated using commercial kits.ResultsThe immunodetection of Tjp1 and Cldn3 was significantly lower in the intestine of parasitized fish, while no strong differences were found in E-cadherin. Parasitized fish showed a significant increase in paracellular uptake measured by FITC-dextran detection in serum. Electrophysiology showed a decrease in transepithelial resistance in infected animals, which showed a diarrheic profile. Serum metabolomics revealed 3702 ions, from which the differential expression of 20 identified compounds significantly separated control from infected groups in multivariate analyses. Of these compounds, serum inosine (decreased) and creatine (increased) were identified as relevant and validated with commercial kits.ConclusionsThe results demonstrate the disruption of tight junctions and the loss of gut barrier function, a metabolomic profile of absorption dysfunction and anorexia, which further outline the pathophysiological effects of E. leei.

Highlights

  • In the animal production sector, enteritis is responsible for serious economic losses, and intestinal parasitism is a major stress factor leading to malnutrition and lowered performance and animal production efficiency

  • Enteritis is responsible for serious economic losses, intestinal parasitism being a major stress factor leading to malnutrition and lowered performance and production efficiency of livestock and poultry [2]

  • The intestinal myxozoan parasite Enteromyxum leei dwells between gut epithelial cells and causes severe desquamative enteritis in gilthead sea bream (Sparus aurata) (Teleostei), producing anorexia, cachexia, growth impairment, reduced marketability and increased mortality

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Summary

Introduction

In the animal production sector, enteritis is responsible for serious economic losses, and intestinal parasitism is a major stress factor leading to malnutrition and lowered performance and animal production efficiency. Enteritis is responsible for serious economic losses, intestinal parasitism being a major stress factor leading to malnutrition and lowered performance and production efficiency of livestock and poultry [2]. An imbalance in the intestinal barrier structure can flare up into an uncontrollable immune reaction in the intestinal microenvironment or allow the unrestrained growth of microbiota, which leads to various diseases. This loss increases the translocation of bacterial antigens and stimulates inflammation in the intestine [5, 6]

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