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 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.
Gastroenterology, Institute of Translational Medicine, University of Liverpool, Liverpool, United Kingdom.
Bryony N
BN
Parsons
Infection Biology, Institute of Infection and Global Health, University of Liverpool, Leahurst, United Kingdom.
Paul
P
Wigley
Gastroenterology, Institute of Translational Medicine, University of Liverpool, Liverpool, United Kingdom.
Hannah L
HL
Simpson
Gastroenterology, Institute of Translational Medicine, University of Liverpool, Liverpool, United Kingdom.
Jonathan M
JM
Williams
Infection Biology, Institute of Infection and Global Health, University of Liverpool, Leahurst, United Kingdom.
Suzie
S
Humphrey
Infection Biology, Institute of Infection and Global Health, University of Liverpool, Leahurst, United Kingdom.
Anne-Marie
AM
Salisbury
Gastroenterology, Institute of Translational Medicine, University of Liverpool, Liverpool, United Kingdom ; Norwich Medical School, University of East Anglia, Norwich Research Park, Norwich, United Kingdom.
Alastair J M
AJ
Watson
The Edinburgh Cell Wall Group, Institute of Molecular Plant Sciences, University of Edinburgh, Edinburgh, United Kingdom.
Stephen C
SC
Fry
Provexis plc, c/o Rowett Institute of Nutrition and Health, Aberdeen, United Kingdom.
David
D
O'Brien
Gastroenterology, Institute of Translational Medicine, University of Liverpool, Liverpool, United Kingdom ; Provexis plc, c/o Rowett Institute of Nutrition and Health, Aberdeen, United Kingdom.
Carol L
CL
Roberts
Provexis plc, c/o Rowett Institute of Nutrition and Health, Aberdeen, United Kingdom.
Niamh
N
O'Kennedy
Clinical and Experimental Medicine, Division of Surgery, Faculty of Health Sciences, Linköping University, Linköping, Sweden.
Asa V
AV
Keita
Clinical and Experimental Medicine, Division of Surgery, Faculty of Health Sciences, Linköping University, Linköping, Sweden.
Johan D
JD
Söderholm
Gastroenterology, Institute of Translational Medicine, University of Liverpool, Liverpool, United Kingdom.
Jonathan M
JM
Rhodes
Gastroenterology, Institute of Translational Medicine, University of Liverpool, Liverpool, United Kingdom.
Barry J
BJ
Campbell
D000818:Animals; D001422:Bacterial Adhesion / Q000187:drug effects; D058491:Bacterial Load; D018938:Caco-2 Cells; D002432:Cecum / Q000187:drug effects / Q000382:microbiology; D002460:Cell Line; D002645:Chickens; D004043:Dietary Fiber / Q000008:administration & dosage*; D019587:Dietary Supplements; D020895:Enterocytes / Q000187:drug effects / Q000382:microbiology; D004847:Epithelial Cells / Q000187:drug effects / Q000382:microbiology; D006801:Humans; D007082:Ileum / Q000187:drug effects / Q000382:microbiology / Q000503:physiopathology; D007413:Intestinal Mucosa / Q000187:drug effects* / Q000382:microbiology / Q000503:physiopathology; D008099:Liver / Q000187:drug effects / Q000382:microbiology; D010368:Pectins / Q000494:pharmacology; D010943:Plantago / Q000737:chemistry*; D011134:Polysaccharides / Q000494:pharmacology; D011201:Poultry Diseases / Q000382:microbiology / Q000517:prevention & control*; D012477:Salmonella enteritidis / Q000187:drug effects / Q000502:physiology; D012486:Salmonella typhimurium / Q000187:drug effects*; D013154:Spleen / Q000187:drug effects / Q000382:microbiology; D013552:Swine
D004043:Dietary Fiber; D011134:Polysaccharides; D010368:Pectins; C003181:polygalacturonic acid