Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-10T06:02:47.636Z Has data issue: false hasContentIssue false
  • English
  • Français

Seaweed extracts and galacto-oligosaccharides improve intestinal health in pigs following Salmonella Typhimurium challenge

Published online by Cambridge University Press:  13 February 2017

M. A. Bouwhuis ,
M. J. McDonnell ,
T. Sweeney ,
A. Mukhopadhya ,
C. J. O’Shea  and
J. V. O’Doherty
M. A. Bouwhuis
Affiliation:
School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland
M. J. McDonnell
Affiliation:
School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland
T. Sweeney
Affiliation:
School of Veterinary Medicine, University College Dublin, Belfield, Dublin 4, Ireland
A. Mukhopadhya
Affiliation:
School of Veterinary Medicine, University College Dublin, Belfield, Dublin 4, Ireland
C. J. O’Shea
Affiliation:
School of Veterinary Medicine, University College Dublin, Belfield, Dublin 4, Ireland
J. V. O’Doherty*
Affiliation:
School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland
*
†E-mail: john.vodoherty@ucd.ie
Get access

Abstract

Pork and pork products are recognised as vehicles of Salmonella Typhimurium infection in humans. Seaweed-derived polysaccharides (SWE) and galacto-oligosaccharides (GOS) have shown to exhibit antimicrobial, prebiotic and immunomodulatory activity. The objective of this study was to assess the effects of dietary GOS and SWE supplementation on reducing S. Typhimurium numbers and intestinal inflammation in vivo. In total, 30 pigs (n=10/treatment, BW 30.9 kg) were randomly assigned to three dietary treatments: (1) basal diet; (2) basal diet+2.5 g GOS/kg diet; (3) basal diet+SWE (containing 180 mg laminarin/kg diet+340 mg fucoidan/kg diet). Following an 11-day dietary adaptation period, pigs were orally challenged with 108 colony-forming units/ml S. Typhimurium (day 0). Pigs remained on their diets for a further 17 days and were then sacrificed for sample collection. The SWE supplementation did not affect S. Typhimurium numbers on days 2 and 4 post-challenge but reduced S. Typhimurium numbers in faecal samples collected day 7 post-challenge (−0.80 log gene copy numbers (GCN)/g faeces) and in caecal and colonic digesta (−0.62 and −0.98 log GCN/g digesta, respectively; P<0.05) compared with the control treatment. Lactobacillus numbers were increased in caecal and colonic digesta after GOS supplementation (+0.70 and +0.35 log GCN/g digesta, respectively; P<0.05). In colonic tissue, both GOS and SWE supplementation resulted in reduced messenger RNA expression levels of interleukin (IL)-6, IL-22, tumour necrosis factor-α and regenerating islet-derived protein 3-γ (P<0.05). It can be concluded that dietary supplementation of SWE reduced faecal and intestinal S. Typhimurium numbers compared with the basal diet, whereas dietary GOS supplementation increased Lactobacillus numbers in caecal and colonic digesta but did not affect S. Typhimurium numbers. Supplementation of GOS and SWE reduced the gene expression of pro-inflammatory cytokines in colonic tissue of pigs after the experimental S. Typhimurium challenge.

Keywords

pigSalmonella Typhimuriumimmune responsegalacto-oligosaccharidesseaweed extract
Type
Research Article
Information
animal , Volume 11 , Issue 9 , September 2017 , pp. 1488 - 1496
Copyright
© The Animal Consortium 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a

Present address: School of Veterinary Science, University of Sydney, Camden, NSW 2570, Australia.

References

Behnsen, J, Jellbauer, S, Wong, C, Edwards, R, George, M, Ouyang, W and Raffatellu, M 2014. The cytokine IL-22 promotes pathogen colonization by suppressing related commensal bacteria. Immunity 40, 262–273.Google Scholar
Casewell, M, Friis, C, Marco, E, McMullin, P and Phillips, I 2003. The European ban on growth-promoting antibiotics and emerging consequences for human and animal health. Journal of Antimicrobial Chemotherapy 52, 159–161.Google Scholar
Casey, PG, Casey, GD, Gardiner, GE, Tangney, M, Stanton, C, Ross, RP, Hill, C and Fitzgerald, GF 2004. Isolation and characterization of anti-Salmonella lactic acid bacteria from the porcine gastrointestinal tract. Letters in Applied Microbiology 39, 431–438.CrossRefGoogle ScholarPubMed
Delroisse, JM, Boulvin, AL, Parmentier, I, Dauphin, RD, Vandenbol, M and Portetelle, D 2008. Quantification of Bifidobacterium spp. and Lactobacillus spp. in rat fecal samples by real-time PCR. Microbiological Research 163, 663–670.Google Scholar
Fachmann, MSR, Josefsen, MH, Hoorfar, J, Nielsen, MT and Löfström, C 2015. Cost‐effective optimization of real‐time PCR‐based detection of Campylobacter and Salmonella with inhibitor tolerant DNA polymerases. Journal of Applied Microbiology 119, 1391–1402.CrossRefGoogle ScholarPubMed
Gibson, GR and Roberfroid, MB 1995. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. The Journal of Nutrition 125, 1401–1412.CrossRefGoogle ScholarPubMed
Heim, G, Sweeney, T, O’Shea, CJ, Doyle, DN and O’Doherty, JV 2014. Effect of maternal supplementation with seaweed extracts on growth performance and aspects of gastrointestinal health of newly weaned piglets after challenge with enterotoxigenic Escherichia coli K88. British Journal of Nutrition 112, 1955–1965.CrossRefGoogle ScholarPubMed
Jiao, G, Yu, G, Zhang, J and Ewart, HS 2011. Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Marine Drugs 9, 196–223.Google Scholar
Knetter, SM, Bearson, SM, Huang, T-H, Kurkiewicz, D, Schroyen, M, Nettleton, D, Berman, D, Cohen, V, Lunney, JK, Ramer-Tait, AE, Wannemuehler, MJ and Tuggle, CK 2015. Salmonella enterica serovar typhimurium-infected pigs with different shedding levels exhibit distinct clinical, peripheral cytokine and transcriptomic immune response phenotypes. Innate Immunity 21, 227–241.Google Scholar
Lai, MA, Quarles, EK, López-Yglesias, AH, Zhao, X, Hajjar, AM and Smith, KD 2013. Innate immune detection of flagellin positively and negatively regulates Salmonella infection. PLoS ONE 8, e72047.Google Scholar
McCabe, EM, Burgess, CM, O’Regan, E, McGuinnes, S, Barry, T, Fanning, S and Duffy, G 2011. Development and evaluation of DNA and RNA real-time assays for food analysis using the hilA gene of Salmonella enterica subspecies enterica . Food Microbiology 28, 447–456.Google Scholar
McDonnell, P, Figat, S and O’Doherty, JV 2010. The effect of dietary laminarin and fucoidan in the diet of the weanling piglet on performance, selected faecal microbial populations and volatile fatty acid concentrations. Animal 4, 579–585.Google Scholar
Mukherjee, S and Hooper, LV 2015. Antimicrobial defense of the intestine. Immunity 42, 28–39.Google Scholar
O’Shea, CJ, Sweeney, T, Bahar, B, Ryan, MT, Thornton, K and O’Doherty, JV 2012. Indices of gastrointestinal fermentation and manure emissions of growing-finishing pigs as influenced through singular or combined consumption of Lactobacillus plantarum and inulin. Journal of Animal Science 90, 3848–3857.CrossRefGoogle ScholarPubMed
Penders, J, Vink, C, Driessen, C, London, N, Thijs, C and Stobberingh, EE 2005. Quantification of Bifidobacterium spp., Escherichia coli and Clostridium difficile in faecal samples of breast-fed and formula-fed infants by real-time PCR. FEMS Microbiology Letters 243, 141–147.Google Scholar
Prendergast, DM, Duggan, SJ, Gonzales-Barron, U, Fanning, S, Butler, F, Cormican, M and Duffy, G 2009. Prevalence, numbers and characteristics of Salmonella spp. on Irish retail pork. International Journal of Food Microbiology 131, 233–239.CrossRefGoogle ScholarPubMed
Price, KL, Totty, HR, Lee, HB, Utt, MD, Fitzner, GE, Yoon, I, Ponder, MA and Escobar, J 2010. Use of Saccharomyces cerevisiae fermentation product on growth performance and microbiota of weaned pigs during Salmonella infection. Journal of Animal Science 88, 3896–3908.CrossRefGoogle ScholarPubMed
Reilly, P, O’Doherty, JV, Pierce, KM, Callan, JJ, O’Sullivan, JT and Sweeney, T 2008. The effects of seaweed extract inclusion on gut morphology, selected intestinal microbiota, nutrient digestibility, volatile fatty acid concentrations and the immune status of the weaned pig. Animal 2, 1465–1473.Google Scholar
Rostagno, MH and Callaway, TR 2012. Pre-harvest risk factors for Salmonella enterica in pork production. Food Research International 45, 634–640.Google Scholar
Ryan, MT, Collins, CB, O’Doherty, JV and Sweeney, T 2010. Selection of stable reference genes for quantitative real-time PCR in porcine gastrointestinal tissues. Livestock Science 133, 42–44.Google Scholar
Sauvant, D, Perez, JM and Tran, G 2004. Table of composition and nutritional value of feed materials. Pigs, poultry, cattle, sheep, goats, rabbits, horses, fish. Wageningen Academic Publishers, The Netherlands.CrossRefGoogle Scholar
Searle, LE, Cooley, WA, Jones, G, Nunez, A, Crudgington, B, Weyer, U, Dugdale, AH, Tzortzis, G, Collins, JW, Woodward, MJ and La Ragione, RM 2010. Purified galactooligosaccharide, derived from a mixture produced by the enzymic activity of Bifidobacterium bifidum, reduces Salmonella enterica serovar typhimurium adhesion and invasion in vitro and in vivo. Journal of Medical Microbiology 59, 1428–1439.Google Scholar
Shibata, H, Iimuro, M, Uchiya, N, Kawamori, T, Nagaoka, M, Ueyama, S, Hashimoto, S, Yokokura, T, Sugimura, T and Wakabayashi, K 2003. Preventive effects of Cladosiphon fucoidan against Helicobacter pylori infection in Mongolian gerbils . Helicobacter 8, 59–65.Google Scholar
Smith, A, O’Doherty, J, Reilly, P, Ryan, M, Bahar, B and Sweeney, T 2011. The effects of laminarin derived from Laminaria digitata on measurements of gut health: selected bacterial populations, intestinal fermentation, mucin gene expression and cytokine gene expression in the pig. British Journal of Nutrition 105, 669–677.Google Scholar
Soler, L, Miller, I, Nöbauer, K, Carpentier, S and Niewold, T 2015. Identification of the major regenerative III protein (RegIII) in the porcine intestinal mucosa as RegIIIγ, not RegIIIα. Veterinary Immunology and Immunopathology 167, 51–56.CrossRefGoogle Scholar
Sweeney, T, Collins, CB, Reilly, P, Pierce, KM, Ryan, M and O’Doherty, JV 2012. Effect of purified beta-glucans derived from Laminaria digitata, Laminaria hyperborea and Saccharomyces cerevisiae on piglet performance, selected bacterial populations, volatile fatty acids and pro-inflammatory cytokines in the gastrointestinal tract of pigs. British Journal of Nutrition 108, 1226–1234.Google Scholar
Sweeney, T, Dillon, S, Fanning, J, Egan, J, O’Shea, CJ, Figat, S, Gutierrez, JJM, Mannion, C, Leonard, F and O’Doherty, JV 2011. Evaluation of seaweed-derived polysaccharides on indices of gastrointestinal fermentation and selected populations of microbiota in newly weaned pigs challenged with Salmonella typhimurium . Animal Feed Science and Technology 165, 85–94.Google Scholar
Tanabe, S and Hochi, S 2010. Oral administration of a galactooligosaccharide preparation inhibits development of atopic dermatitis-like skin lesions in NC/Nga mice. International Journal of Molecular Medicine 25, 331–336.Google Scholar
Usov, A, Smirnova, G and Klochkova, N 2001. Polysaccharides of algae: 55. Polysaccharide composition of several brown algae from Kamchatka. Russian Journal of Bioorganic Chemistry 27, 395–399.Google Scholar
Vandesompele, J, De Preter, K, Pattyn, F, Poppe, B, Van Roy, N, De Paepe, A and Speleman, F 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, Research0034.Google Scholar
Van Soest, PJ, Robertson, JB and Lewis, BA 1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.Google Scholar
Vetvicka, V, Vannucci, L and Sima, P 2014. The effects of β-glucan on pig growth and immunity. The Open Biochemistry Journal 8, 89–93.CrossRefGoogle ScholarPubMed
Vladimer, GI, Marty-Roix, R, Ghosh, S, Weng, D and Lien, E 2013. Inflammasomes and host defenses against bacterial infections. Current Opinion in Microbiology 16, 23–31.Google Scholar
Vulevic, J, Drakoularakou, A, Yaqoob, P, Tzortzis, G and Gibson, GR 2008. Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (B-GOS) in healthy elderly volunteers. The American Journal of Clinical Nutrition 88, 1438–1446.Google Scholar
Walsh, AM, Sweeney, T, O’Shea, CJ, Doyle, DN and O’Doherty, JV 2013. Effect of dietary laminarin and fucoidan on selected microbiota, intestinal morphology and immune status of the newly weaned pig. British Journal of Nutrition 110, 1630–1638.Google Scholar
Zheng, R, Yang, L, Zhou, X-l, Zhu, C, Shu, X-g, Wu, X, Li, H, Wang, L and Bo, J 2012. Effect of soybean oligosaccharides in immunity and TLR2-NF-κB signal pathway response for weaning pigs. Journal of Food, Agriculture & Environment 10, 273–279.Google Scholar