Journal Article
. 2016 Apr; 5:e15.
doi: 10.1017/jns.2016.4.

The effect of algal polysaccharides laminarin and fucoidan on colonic pathology, cytokine gene expression and Enterobacteriaceae in a dextran sodium sulfate-challenged porcine model

C J O'Shea 1 J V O'Doherty 1 J J Callanan 2 D Doyle 1 K Thornton 2 T Sweeney 2 
  • PMID: 27110358
  •     42 References
  •     10 citations


The algal polysaccharides laminarin (LAM) and fucoidan (FUC) have potent anti-inflammatory activities in the gastrointestinal tract. Our objective was to examine the impact of prior consumption of LAM and/or FUC on pathology and inflammation following a dextran sodium sulfate (DSS) challenge in pigs. Pigs (n 7/group) were assigned to one of five experimental groups for 56 d. From 49-55 d, distilled water or DSS was administered intragastrically. The experimental groups were: (1) basal diet + distilled water (control); (2) basal diet + DSS (DSS); (3) basal diet + FUC + DSS (FUC + DSS); (4) basal diet + LAM + DSS (LAM + DSS); and (5) basal diet + LAM + FUC + DSS (LAMFUC + DSS). The DSS group had decreased body-weight gain (P < 0·05) and serum xylose (P < 0·05), and increased proximal colon pathology score (P < 0·05), diarrhoeal score (P < 0·001) and colonic Enterobacteriaceae (P < 0·05) relative to the control group. The FUC + DSS (P < 0·01), LAM + DSS (P < 0·05) and LAMFUC + DSS (P < 0·05) groups had improved diarrhoeal score, and the LAMFUC + DSS (P < 0·05) group had improved body weight relative to the DSS group. The FUC + DSS group (P < 0·001), LAM + DSS group (P < 0·05) and LAMFUC + DSS group (P < 0·001) had lower IL-6 mRNA abundance relative to the DSS group. The LAM + DSS group had reduced Enterobacteriaceae in proximal colon digesta relative to the DSS group (P < 0·05). In conclusion, FUC or a combination of FUC and LAM improved body-weight loss, diarrhoeal scores and clinical variables associated with a DSS challenge in pigs, in tandem with a reduction in colonic IL-6 mRNA abundance.

Keywords: Cytokines; DSS, dextran sodium sulphate; Dextran sodium sulfate; Enterobacteriaceae; FUC, fucoidan; Fucoidan; LAM, laminarin; LAMFUC, laminarin+ fucoidan; Laminarin; Pigs; UC, ulcerative colitis; Ulcerative colitis.

Innate mechanisms of epithelial host defense: spotlight on intestine.
G Hecht.
Am J Physiol, 1999 Sep 14; 277(3). PMID: 10484321
Gram-negative bacteria account for main differences between faecal microbiota from patients with ulcerative colitis and healthy controls.
L K Vigsnæs, J Brynskov, +2 authors, T R Licht.
Benef Microbes, 2012 Sep 13; 3(4). PMID: 22968374
Proinflammatory cytokines in the pathogenesis of inflammatory bowel diseases.
Warren Strober, Ivan J Fuss.
Gastroenterology, 2011 May 03; 140(6). PMID: 21530742    Free PMC article.
Highly Cited. Review.
Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines.
L A Dieleman, M J Palmen, +4 authors, E P Van Rees.
Clin Exp Immunol, 1998 Dec 09; 114(3). PMID: 9844047    Free PMC article.
Highly Cited.
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.
Jo Vandesompele, Katleen De Preter, +4 authors, Frank Speleman.
Genome Biol, 2002 Aug 20; 3(7). PMID: 12184808    Free PMC article.
Highly Cited.
Epidemiology and natural history of inflammatory bowel diseases.
Jacques Cosnes, Corinne Gower-Rousseau, Philippe Seksik, Antoine Cortot.
Gastroenterology, 2011 May 03; 140(6). PMID: 21530745
Highly Cited.
Effects of supplementing dietary laminarin and fucoidan on intestinal morphology and the immune gene expression in the weaned pig.
A M Walsh, T Sweeney, +2 authors, J V O'Doherty.
J Anim Sci, 2013 Feb 13; 90 Suppl 4. PMID: 23365357
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.
P Reilly, J V O'Doherty, +3 authors, T Sweeney.
Animal, 2008 Oct 01; 2(10). PMID: 22443904
Inflammatory bowel disease: the role of environmental factors.
Silvio Danese, Miquel Sans, Claudio Fiocchi.
Autoimmun Rev, 2004 Aug 04; 3(5). PMID: 15288007
Effects of dietary supplementation with Laminaria hyperborea, Laminaria digitata, and Saccharomyces cerevisiae on the IL-17 pathway in the porcine colon.
M T Ryan, C J O'Shea, +2 authors, T Sweeney.
J Anim Sci, 2013 Feb 13; 90 Suppl 4. PMID: 23365350
Effect of the interaction of seaweed extracts containing laminarin and fucoidan with zinc oxide on the growth performance, digestibility and faecal characteristics of growing piglets.
C J O'Shea, P McAlpine, +2 authors, J V O'Doherty.
Br J Nutr, 2013 Oct 18; 111(5). PMID: 24131869
Nonstarch polysaccharides modulate bacterial microbiota, pathways for butyrate production, and abundance of pathogenic Escherichia coli in the pig gastrointestinal tract.
Barbara U Metzler-Zebeli, Seema Hooda, +4 authors, Michael G Gänzle.
Appl Environ Microbiol, 2010 Apr 13; 76(11). PMID: 20382813    Free PMC article.
Longitudinal analyses of gut mucosal microbiotas in ulcerative colitis in relation to patient age and disease severity and duration.
Alemu Fite, Sandra Macfarlane, +4 authors, George T Macfarlane.
J Clin Microbiol, 2012 Dec 28; 51(3). PMID: 23269735    Free PMC article.
Ulcerative colitis.
Silvio Danese, Claudio Fiocchi.
N Engl J Med, 2011 Nov 04; 365(18). PMID: 22047562
Highly Cited. Review.
European evidence-based Consensus on the diagnosis and management of ulcerative colitis: Definitions and diagnosis.
E F Stange, S P L Travis, +14 authors, European Crohn's and Colitis Organisation (ECCO).
J Crohns Colitis, 2008 Mar 01; 2(1). PMID: 21172194
Highly Cited.
Performance of weanling piglets offered low-, medium- or high-lactose diets supplemented with a seaweed extract from Laminaria spp.
D A Gahan, M B Lynch, +2 authors, J V O'Doherty.
Animal, 2009 Jan 01; 3(1). PMID: 22444169
IL-6 promotes immune responses in human ulcerative colitis and induces a skin-homing phenotype in the dendritic cells and Tcells they stimulate.
David Bernardo, Sara Vallejo-Díez, +12 authors, Stella C Knight.
Eur J Immunol, 2012 Apr 28; 42(5). PMID: 22539302
Effect of purified β-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.
T Sweeney, C B Collins, +3 authors, J V O'Doherty.
Br J Nutr, 2012 Feb 09; 108(7). PMID: 22313684
Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae.
Claudia Lupp, Marilyn L Robertson, +4 authors, B Brett Finlay.
Cell Host Microbe, 2007 Nov 17; 2(2). PMID: 18005726
Highly Cited.
Chloride secretion by the intestinal epithelium: molecular basis and regulatory aspects.
K E Barrett, S J Keely.
Annu Rev Physiol, 2000 Jun 09; 62. PMID: 10845102
Highly Cited. Review.
The hydroxylase inhibitor dimethyloxalylglycine is protective in a murine model of colitis.
Eoin P Cummins, Fergal Seeballuck, +4 authors, Cormac T Taylor.
Gastroenterology, 2008 Jan 02; 134(1). PMID: 18166353
Highly Cited.
Fucoidan derived from Cladosiphon okamuranus Tokida ameliorates murine chronic colitis through the down-regulation of interleukin-6 production on colonic epithelial cells.
S Matsumoto, M Nagaoka, +3 authors, S Ueyama.
Clin Exp Immunol, 2004 May 19; 136(3). PMID: 15147344    Free PMC article.
Inflammatory bowel disease: epidemiology, pathogenesis, and therapeutic opportunities.
Stephen B Hanauer.
Inflamm Bowel Dis, 2005 Dec 27; 12 Suppl 1. PMID: 16378007
Highly Cited. Review.
Distinct cytokine patterns identified from multiplex profiles of murine DSS and TNBS-induced colitis.
Philip Alex, Nicholas C Zachos, +5 authors, Xuhang Li.
Inflamm Bowel Dis, 2008 Oct 24; 15(3). PMID: 18942757    Free PMC article.
Highly Cited.
Extracts of brown seaweeds can attenuate the bacterial lipopolysaccharide-induced pro-inflammatory response in the porcine colon ex vivo.
B Bahar, J V O'Doherty, M Hayes, T Sweeney.
J Anim Sci, 2013 Feb 13; 90 Suppl 4. PMID: 23365280
Cytokines in inflammatory bowel disease.
G Rogler, T Andus.
World J Surg, 1998 Apr 02; 22(4). PMID: 9523521
Highly Cited. Review.
Effects of different starch sources on Bacillus spp. in intestinal tract and expression of intestinal development related genes of weanling piglets.
Guo-Quan Han, Zhen-Tian Xiang, +6 authors, Zhi-Qing Huang.
Mol Biol Rep, 2011 Jun 11; 39(2). PMID: 21660473    Free PMC article.
Ileitis in ulcerative colitis: is it a backwash?
Ayman S Abdelrazeq, Timothy R Wilson, +2 authors, Stephen H Leveson.
Dis Colon Rectum, 2005 Sep 22; 48(11). PMID: 16175321
Comparative assessment of D-xylose absorption between small intestine and large intestine.
H Yuasa, C Kuno, J Watanabe.
J Pharm Pharmacol, 1997 Jan 01; 49(1). PMID: 9120765
Altered bone metabolism in inflammatory bowel disease.
S C Bischoff, A Herrmann, +3 authors, G Brabant.
Am J Gastroenterol, 1997 Jul 01; 92(7). PMID: 9219790
Effects of dietary seaweed extract supplementation in sows and post-weaned pigs on performance, intestinal morphology, intestinal microflora and immune status.
S G Leonard, T Sweeney, +2 authors, J V O'Doherty.
Br J Nutr, 2011 Jul 09; 106(5). PMID: 21736851
Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis.
Wendy S Garrett, Carey A Gallini, +10 authors, Laurie H Glimcher.
Cell Host Microbe, 2010 Sep 14; 8(3). PMID: 20833380    Free PMC article.
Highly Cited.
The commensal microbiota and enteropathogens in the pathogenesis of inflammatory bowel diseases.
Benoit Chassaing, Arlette Darfeuille-Michaud.
Gastroenterology, 2011 May 03; 140(6). PMID: 21530738
Highly Cited.
The serum D-xylose test as a useful tool to identify malabsorption in rats with antigen specific gut inflammatory reaction.
Danielle Mota Fontes Antunes, Janilda Pacheco da Costa, +5 authors, Gilberto Perez Cardoso.
Int J Exp Pathol, 2009 Apr 02; 90(2). PMID: 19335552    Free PMC article.
Sulfated fucans, fresh perspectives: structures, functions, and biological properties of sulfated fucans and an overview of enzymes active toward this class of polysaccharide.
Olivier Berteau, Barbara Mulloy.
Glycobiology, 2003 Mar 11; 13(6). PMID: 12626402
Dextran sodium sulfate (DSS) induces colitis in mice by forming nano-lipocomplexes with medium-chain-length fatty acids in the colon.
Hamed Laroui, Sarah A Ingersoll, +7 authors, Didier Merlin.
PLoS One, 2012 Mar 20; 7(3). PMID: 22427817    Free PMC article.
Highly Cited.
Predictors of quality of life in ulcerative colitis: the importance of symptoms and illness representations.
Seong Won Han, Elaine McColl, +3 authors, Mark Richard Welfare.
Inflamm Bowel Dis, 2005 Jan 28; 11(1). PMID: 15674110
Inhibition of selectin function and leukocyte rolling protects against dextran sodium sulfate-induced murine colitis.
X W Zhang, Q Liu, H Thorlacius.
Scand J Gastroenterol, 2001 Apr 18; 36(3). PMID: 11305514
Effect of seaweed-derived laminarin and fucoidan and zinc oxide on gut morphology, nutrient transporters, nutrient digestibility, growth performance and selected microbial populations in weaned pigs.
G Heim, A M Walsh, +4 authors, J V O'Doherty.
Br J Nutr, 2014 Feb 08; 111(9). PMID: 24502994
Characterisation of acute murine dextran sodium sulphate colitis: cytokine profile and dose dependency.
B Egger, M Bajaj-Elliott, +3 authors, M W Büchler.
Digestion, 2000 Nov 09; 62(4). PMID: 11070407
Highly Cited.
qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data.
Jan Hellemans, Geert Mortier, +2 authors, Jo Vandesompele.
Genome Biol, 2007 Feb 13; 8(2). PMID: 17291332    Free PMC article.
Highly Cited.
Effect of dietary laminarin and fucoidan on selected microbiota, intestinal morphology and immune status of the newly weaned pig.
A M Walsh, T Sweeney, +2 authors, J V O'Doherty.
Br J Nutr, 2013 Mar 28; 110(9). PMID: 23531383
Effects of Non-Starch Polysaccharides on Inflammatory Bowel Disease.
Ying Nie, Qinlu Lin, Feijun Luo.
Int J Mol Sci, 2017 Jun 28; 18(7). PMID: 28654020    Free PMC article.
Current understanding of microbiota- and dietary-therapies for treating inflammatory bowel disease.
Taekil Eom, Yong Sung Kim, +2 authors, Tatsuya Unno.
J Microbiol, 2018 Mar 02; 56(3). PMID: 29492876
Impact of Dietary Supplementation of Lactic Acid Bacteria Fermented Rapeseed with or without Macroalgae on Performance and Health of Piglets Following Omission of Medicinal Zinc from Weaner Diets.
Gizaw D Satessa, Paulina Tamez-Hidalgo, +6 authors, Mette O Nielsen.
Animals (Basel), 2020 Jan 19; 10(1). PMID: 31952154    Free PMC article.
Fucose Ameliorates Tryptophan Metabolism and Behavioral Abnormalities in a Mouse Model of Chronic Colitis.
Mariya A Borisova, Olga A Snytnikova, +5 authors, Elena N Kozhevnikova.
Nutrients, 2020 Feb 15; 12(2). PMID: 32053891    Free PMC article.
Improvement of Psoriasis by Alteration of the Gut Environment by Oral Administration of Fucoidan from Cladosiphon Okamuranus.
Masanobu Takahashi, Kento Takahashi, +7 authors, Hiroko Hoshi.
Mar Drugs, 2020 Mar 14; 18(3). PMID: 32164223    Free PMC article.
Effects of Increasing Doses of Lactobacillus Pre-Fermented Rapeseed Product with or without Inclusion of Macroalgae Product on Weaner Piglet Performance and Intestinal Development.
Gizaw Dabessa Satessa, Paulina Tamez-Hidalgo, +3 authors, Mette Olaf Nielsen.
Animals (Basel), 2020 Apr 02; 10(4). PMID: 32230825    Free PMC article.
The Effects of the Marine-Derived Polysaccharides Laminarin and Chitosan on Aspects of Colonic Health in Pigs Challenged with Dextran Sodium Sulphate.
Ruth Rattigan, John V O'Doherty, +9 authors, Torres Sweeney.
Mar Drugs, 2020 May 21; 18(5). PMID: 32429425    Free PMC article.
Extracts and Marine Algae Polysaccharides in Therapy and Prevention of Inflammatory Diseases of the Intestine.
Natalya N Besednova, Tatyana S Zaporozhets, +4 authors, Svetlana P Ermakova.
Mar Drugs, 2020 Jun 04; 18(6). PMID: 32486405    Free PMC article.
Dietary Red Meat Adversely Affects Disease Severity in a Pig Model of DSS-Induced Colitis Despite Reduction in Colonic Pro-Inflammatory Gene Expression.
Tina S Nielsen, Marlene Fredborg, +4 authors, Stig Purup.
Nutrients, 2020 Jun 13; 12(6). PMID: 32526985    Free PMC article.
Feeding Marine Polysaccharides to Alleviate the Negative Effects Associated with Weaning in Pigs.
John V O'Doherty, Brigkita Venardou, Ruth Rattigan, Torres Sweeney.
Animals (Basel), 2021 Sep 29; 11(9). PMID: 34573610    Free PMC article.