Abstract

BackgroundThe roundworm Ascaris suum is one of the parasites with the greatest economic impact on pig farming. In this context, lower weight gain is hypothesized to be due to decreased nutrient absorption. This study aims at characterizing the effects of A. suum infection on intestinal nutrient transport processes and potential molecular mechanisms.MethodsThree groups of six piglets each were infected orally (10,000 embryonated A. suum eggs) in a single dose (“single infection”). Another three groups were infected orally (1000 embryonated eggs) for 10 consecutive days (“trickle infection”). Animals were necropsied 21, 35 and 49 days post-infection (dpi). Three groups served as respective controls. The Ussing chamber technique was applied for the functional characterization of small intestinal tissues [short-circuit currents (Isc) as induced by glucose, alanine and peptides; 3H-glucose net flux rates; tissue conductance (Gt)]. Transcription and expression levels of relevant cytokines and nutrient transporters were evaluated (qPCR/western blot).ResultsPeptide- and alanine-induced changes in Isc were significantly decreased in the jejunum and ileum of the trickle-infected group at 49 dpi and in the ileum of the single-infected group at 49 dpi. No significant differences regarding glucose transport were observed between the Ascaris-infected groups and the control group in Ussing chamber experiments. Transcription levels of the glucose and peptide transporters as well as of selected transcription factors (transcription of signal transducer and activator of transcription 6 [STAT6] and hypoxia-inducible factor 1-alpha [Hif-1α]) were significantly increased in response to both infection types after some periods. The transcription of interleukins 4 and 13 varied between decrease and increase regarding the respective time points, as did the protein expression of glucose transporters. The expression of the peptide transporter PepT1 was significantly decreased in the ileal single-infected group at 35 dpi. Hif-1α was significantly increased in the ileal tissue from the single-infected group at 21 dpi and in the trickle-infected group at 35 dpi. The expression levels of Na+/K+-ATPase and ASCT1 remained unaffected.ConclusionsIn contrast to the current hypothesis, these results indicate that the nutrient deprivation induced by A. suum cannot be explained by transcriptional or expression changes alone and requires further studies.Graphical abstract

Highlights

  • The roundworm Ascaris suum is one of the parasites with the greatest economic impact on pig farming

  • Full list of author information is available at the end of the article

  • Considering electrophysiological, transcriptional and expression data as well as weight gain and histomorphometric analysis, the infected pigs did not experience the comprehensive nutrient restriction that was expected based on previous studies [14, 15]

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Summary

Introduction

The roundworm Ascaris suum is one of the parasites with the greatest economic impact on pig farming. In this context, lower weight gain is hypothesized to be due to decreased nutrient absorption. Lower weight gain might be explained by a dysfunction of gastrointestinal nutrient absorption induced by alterations of the intestinal ion transport [12], as well as by reduced availability of glucose or cholesterol [13]. Chickens infected with Ascaridia galli showed significantly decreased electrogenic transport of glucose and alanine [15] These findings were associated with increased transcription of the Th2 cell-associated cytokines interleukin (IL)-4 and IL-13. IL-4 and IL-13, being upregulated during gastrointestinal nematode infections, activate signal transducer and activator of transcription 6 (STAT6), which in turn may lead to decreased sodium-linked glucose absorption [16, 17]

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