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: Bryony N Parsons, Paul Wigley, Hannah L Simpson, Jonathan M Williams, Suzie Humphrey, Anne-Marie Salisbury, Alastair J M Watson, Stephen C Fry, David O'Brien, Carol L Roberts, Niamh O'Kennedy, Asa V Keita, Johan D Söderholm, Jonathan M Rhodes, Barry J Campbell
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Publicado: Public Library of Science (PLoS) 2014
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spelling oai:doaj.org-article:c9650eb50de44dbd8d9db0a1f8f638632021-11-18T08:34:14ZDietary supplementation with soluble plantain non-starch polysaccharides inhibits intestinal invasion of Salmonella Typhimurium in the chicken.1932-620310.1371/journal.pone.0087658https://doaj.org/article/c9650eb50de44dbd8d9db0a1f8f638632014-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24498347/?tool=EBIhttps://doaj.org/toc/1932-6203Soluble 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.Bryony N ParsonsPaul WigleyHannah L SimpsonJonathan M WilliamsSuzie HumphreyAnne-Marie SalisburyAlastair J M WatsonStephen C FryDavid O'BrienCarol L RobertsNiamh O'KennedyAsa V KeitaJohan D SöderholmJonathan M RhodesBarry J CampbellPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 9, Iss 2, p e87658 (2014)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Bryony N Parsons
Paul Wigley
Hannah L Simpson
Jonathan M Williams
Suzie Humphrey
Anne-Marie Salisbury
Alastair J M Watson
Stephen C Fry
David O'Brien
Carol L Roberts
Niamh O'Kennedy
Asa V Keita
Johan D Söderholm
Jonathan M Rhodes
Barry J Campbell
Dietary supplementation with soluble plantain non-starch polysaccharides inhibits intestinal invasion of Salmonella Typhimurium in the chicken.
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.
format article
author Bryony N Parsons
Paul Wigley
Hannah L Simpson
Jonathan M Williams
Suzie Humphrey
Anne-Marie Salisbury
Alastair J M Watson
Stephen C Fry
David O'Brien
Carol L Roberts
Niamh O'Kennedy
Asa V Keita
Johan D Söderholm
Jonathan M Rhodes
Barry J Campbell
author_facet Bryony N Parsons
Paul Wigley
Hannah L Simpson
Jonathan M Williams
Suzie Humphrey
Anne-Marie Salisbury
Alastair J M Watson
Stephen C Fry
David O'Brien
Carol L Roberts
Niamh O'Kennedy
Asa V Keita
Johan D Söderholm
Jonathan M Rhodes
Barry J Campbell
author_sort Bryony N Parsons
title 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_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_sort dietary supplementation with soluble plantain non-starch polysaccharides inhibits intestinal invasion of salmonella typhimurium in the chicken.
publisher Public Library of Science (PLoS)
publishDate 2014
url https://doaj.org/article/c9650eb50de44dbd8d9db0a1f8f63863
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