Dietary supplementation with soluble plantain non-starch polysaccharides inhibits intestinal invasion of Salmonella typhimurium in the chicken

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 Soderholm, Jonathan M Rhodes, Barry J Campbell

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Abstract

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 SalmonellaIn 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 withSalmonella 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 vivodietary 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 ofS.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.

Original languageEnglish
Article numbere87658
Number of pages11
JournalPloS ONE
Volume9
Issue number2
DOIs
Publication statusPublished - 3 Feb 2014

Keywords

  • cell-wall
  • Escherichia-coli
  • epithelial-cells
  • Crohns-disease
  • in-vitro
  • enterica
  • infection
  • broiler
  • colonization
  • serotype

Cite this

Parsons, B. N., Wigley, P., Simpson, H. L., Williams, J. M., Humphrey, S., Salisbury, A-M., ... Campbell, B. J. (2014). Dietary supplementation with soluble plantain non-starch polysaccharides inhibits intestinal invasion of Salmonella typhimurium in the chicken. PloS ONE, 9(2), [e87658]. https://doi.org/10.1371/journal.pone.0087658

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, Asa V; Soderholm, Johan D; Rhodes, Jonathan M; Campbell, Barry J.

In: PloS ONE, Vol. 9, No. 2, e87658, 03.02.2014.

Research output: Contribution to journalArticle

Parsons, BN, Wigley, P, Simpson, HL, Williams, JM, Humphrey, S, Salisbury, A-M, Watson, AJM, Fry, SC, O'Brien, D, Roberts, CL, O'Kennedy, N, Keita, AV, Soderholm, JD, Rhodes, JM & Campbell, BJ 2014, 'Dietary supplementation with soluble plantain non-starch polysaccharides inhibits intestinal invasion of Salmonella typhimurium in the chicken', PloS ONE, vol. 9, no. 2, e87658. https://doi.org/10.1371/journal.pone.0087658
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, Asa V ; Soderholm, 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. In: PloS ONE. 2014 ; Vol. 9, No. 2.
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abstract = "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 withSalmonella 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 vivodietary 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 ofS.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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AU - Parsons, Bryony N

AU - Wigley, Paul

AU - Simpson, Hannah L

AU - Williams, Jonathan M

AU - Humphrey, Suzie

AU - Salisbury, Anne-Marie

AU - Watson, Alastair J M

AU - Fry, Stephen C

AU - O'Brien, David

AU - Roberts, Carol L

AU - O'Kennedy, Niamh

AU - Keita, Asa V

AU - Soderholm, Johan D

AU - Rhodes, Jonathan M

AU - Campbell, Barry J

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N2 - 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 withSalmonella 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 vivodietary 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 ofS.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.

AB - 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 withSalmonella 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 vivodietary 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 ofS.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.

KW - cell-wall

KW - Escherichia-coli

KW - epithelial-cells

KW - Crohns-disease

KW - in-vitro

KW - enterica

KW - infection

KW - broiler

KW - colonization

KW - serotype

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DO - 10.1371/journal.pone.0087658

M3 - Article

VL - 9

JO - PloS ONE

JF - PloS ONE

SN - 1932-6203

IS - 2

M1 - e87658

ER -