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Dietary Supplementation with Soluble Plantain Non-Starch Polysaccharides Inhibits Intestinal Invasion of Salmonella Typhimurium in the Chicken

Soluble fibres (non-starch polysaccharides, NSP) from edible plants but particularly plantain banana (Musa spp.), have been shown in vitro and ex vivo to prevent various enteric pathogens from adhering to, or translocating across, the human intestinal epithelium, a property that we have termed contr...

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Autores principales: Parsons, Bryony N., Wigley, Paul, Simpson, Hannah L., Williams, Jonathan M., Humphrey, Suzie, Salisbury, Anne-Marie, Watson, Alastair J. M., Fry, Stephen C., O'Brien, David, Roberts, Carol L., O'Kennedy, Niamh, Keita, Åsa V., Söderholm, Johan D., Rhodes, Jonathan M., Campbell, Barry J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3911995/
https://www.ncbi.nlm.nih.gov/pubmed/24498347
http://dx.doi.org/10.1371/journal.pone.0087658
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author Parsons, Bryony N.
Wigley, Paul
Simpson, Hannah L.
Williams, Jonathan M.
Humphrey, Suzie
Salisbury, Anne-Marie
Watson, Alastair J. M.
Fry, Stephen C.
O'Brien, David
Roberts, Carol L.
O'Kennedy, Niamh
Keita, Åsa V.
Söderholm, Johan D.
Rhodes, Jonathan M.
Campbell, Barry J.
author_facet Parsons, Bryony N.
Wigley, Paul
Simpson, Hannah L.
Williams, Jonathan M.
Humphrey, Suzie
Salisbury, Anne-Marie
Watson, Alastair J. M.
Fry, Stephen C.
O'Brien, David
Roberts, Carol L.
O'Kennedy, Niamh
Keita, Åsa V.
Söderholm, Johan D.
Rhodes, Jonathan M.
Campbell, Barry J.
author_sort Parsons, Bryony N.
collection PubMed
description Soluble fibres (non-starch polysaccharides, NSP) from edible plants but particularly plantain banana (Musa spp.), have been shown in vitro and ex vivo to prevent various enteric pathogens from adhering to, or translocating across, the human intestinal epithelium, a property that we have termed contrabiotic. Here we report that dietary plantain fibre prevents invasion of the chicken intestinal mucosa by Salmonella. In vivo experiments were performed with chicks fed from hatch on a pellet diet containing soluble plantain NSP (0 to 200 mg/d) and orally infected with S.Typhimurium 4/74 at 8 d of age. Birds were sacrificed 3, 6 and 10 d post-infection. Bacteria were enumerated from liver, spleen and caecal contents. In vitro studies were performed using chicken caecal crypts and porcine intestinal epithelial cells infected with Salmonella enterica serovars following pre-treatment separately with soluble plantain NSP and acidic or neutral polysaccharide fractions of plantain NSP, each compared with saline vehicle. Bacterial adherence and invasion were assessed by gentamicin protection assay. In vivo dietary supplementation with plantain NSP 50 mg/d reduced invasion by S.Typhimurium, as reflected by viable bacterial counts from splenic tissue, by 98.9% (95% CI, 98.1–99.7; P<0.0001). In vitro studies confirmed that plantain NSP (5–10 mg/ml) inhibited adhesion of S.Typhimurium 4/74 to a porcine epithelial cell-line (73% mean inhibition (95% CI, 64–81); P<0.001) and to primary chick caecal crypts (82% mean inhibition (95% CI, 75–90); P<0.001). Adherence inhibition was shown to be mediated via an effect on the epithelial cells and Ussing chamber experiments with ex-vivo human ileal mucosa showed that this effect was associated with increased short circuit current but no change in electrical resistance. The inhibitory activity of plantain NSP lay mainly within the acidic/pectic (homogalacturonan-rich) component. Supplementation of chick feed with plantain NSP was well tolerated and shows promise as a simple approach for reducing invasive salmonellosis.
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spelling pubmed-39119952014-02-04 Dietary Supplementation with Soluble Plantain Non-Starch Polysaccharides Inhibits Intestinal Invasion of Salmonella Typhimurium in the Chicken Parsons, Bryony N. Wigley, Paul Simpson, Hannah L. Williams, Jonathan M. Humphrey, Suzie Salisbury, Anne-Marie Watson, Alastair J. M. Fry, Stephen C. O'Brien, David Roberts, Carol L. O'Kennedy, Niamh Keita, Åsa V. Söderholm, Johan D. Rhodes, Jonathan M. Campbell, Barry J. PLoS One Research Article Soluble fibres (non-starch polysaccharides, NSP) from edible plants but particularly plantain banana (Musa spp.), have been shown in vitro and ex vivo to prevent various enteric pathogens from adhering to, or translocating across, the human intestinal epithelium, a property that we have termed contrabiotic. Here we report that dietary plantain fibre prevents invasion of the chicken intestinal mucosa by Salmonella. In vivo experiments were performed with chicks fed from hatch on a pellet diet containing soluble plantain NSP (0 to 200 mg/d) and orally infected with S.Typhimurium 4/74 at 8 d of age. Birds were sacrificed 3, 6 and 10 d post-infection. Bacteria were enumerated from liver, spleen and caecal contents. In vitro studies were performed using chicken caecal crypts and porcine intestinal epithelial cells infected with Salmonella enterica serovars following pre-treatment separately with soluble plantain NSP and acidic or neutral polysaccharide fractions of plantain NSP, each compared with saline vehicle. Bacterial adherence and invasion were assessed by gentamicin protection assay. In vivo dietary supplementation with plantain NSP 50 mg/d reduced invasion by S.Typhimurium, as reflected by viable bacterial counts from splenic tissue, by 98.9% (95% CI, 98.1–99.7; P<0.0001). In vitro studies confirmed that plantain NSP (5–10 mg/ml) inhibited adhesion of S.Typhimurium 4/74 to a porcine epithelial cell-line (73% mean inhibition (95% CI, 64–81); P<0.001) and to primary chick caecal crypts (82% mean inhibition (95% CI, 75–90); P<0.001). Adherence inhibition was shown to be mediated via an effect on the epithelial cells and Ussing chamber experiments with ex-vivo human ileal mucosa showed that this effect was associated with increased short circuit current but no change in electrical resistance. The inhibitory activity of plantain NSP lay mainly within the acidic/pectic (homogalacturonan-rich) component. Supplementation of chick feed with plantain NSP was well tolerated and shows promise as a simple approach for reducing invasive salmonellosis. Public Library of Science 2014-02-03 /pmc/articles/PMC3911995/ /pubmed/24498347 http://dx.doi.org/10.1371/journal.pone.0087658 Text en © 2014 Parsons et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Parsons, Bryony N.
Wigley, Paul
Simpson, Hannah L.
Williams, Jonathan M.
Humphrey, Suzie
Salisbury, Anne-Marie
Watson, Alastair J. M.
Fry, Stephen C.
O'Brien, David
Roberts, Carol L.
O'Kennedy, Niamh
Keita, Åsa V.
Söderholm, Johan D.
Rhodes, Jonathan M.
Campbell, Barry J.
Dietary Supplementation with Soluble Plantain Non-Starch Polysaccharides Inhibits Intestinal Invasion of Salmonella Typhimurium in the Chicken
title Dietary Supplementation with Soluble Plantain Non-Starch Polysaccharides Inhibits Intestinal Invasion of Salmonella Typhimurium in the Chicken
title_full Dietary Supplementation with Soluble Plantain Non-Starch Polysaccharides Inhibits Intestinal Invasion of Salmonella Typhimurium in the Chicken
title_fullStr Dietary Supplementation with Soluble Plantain Non-Starch Polysaccharides Inhibits Intestinal Invasion of Salmonella Typhimurium in the Chicken
title_full_unstemmed Dietary Supplementation with Soluble Plantain Non-Starch Polysaccharides Inhibits Intestinal Invasion of Salmonella Typhimurium in the Chicken
title_short Dietary Supplementation with Soluble Plantain Non-Starch Polysaccharides Inhibits Intestinal Invasion of Salmonella Typhimurium in the Chicken
title_sort dietary supplementation with soluble plantain non-starch polysaccharides inhibits intestinal invasion of salmonella typhimurium in the chicken
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3911995/
https://www.ncbi.nlm.nih.gov/pubmed/24498347
http://dx.doi.org/10.1371/journal.pone.0087658
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