Abstract
We studied the anti-inflammatory properties of probiotic strains and blueberry in a colitis model. The disease activity index (DAI) was significantly lower on days 9 and 10 in all groups compared to the colitis control. Myeloperoxidase (MPO) and bacterial translocation to the liver and to the mesenteric lymph nodes (MLN) decreased significantly in all groups compared to colitis control. Cecal Enterobacteriaceae count decreased significantly in blueberry with and without probiotics compared to the other groups. Lactobacillus plantarum reisolated from the cecal content in the presence of blueberry, contrary to Lactobacillus fermentum. Colonic MDA decreased significantly in all groups, except the L. fermentum group, compared to the colitis control. The cecal concentration of acetic, propionic, and butyricbutyric acid was significantly higher in the L. plantarum group, while the L. fermentum group yielded the highest concentration of lactic acid compared with all other groups. Lactobacillus plantarum DSM 15313, Lactobacillus fermentum 35D, and blueberry alone and in combination improve the DAI, reduce bacterial translocation, and reduce inflammation.
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Grisham MB, Granger DN (1988) Neutrophil-mediated mucosal injury. Role of reactive oxygen metabolites. Dig Dis Sci 33:6S–15S
Babbs CF (1992) Oxygen radicals in ulcerative colitis. Free Radic Biol Med 13:169–181
Suematsu M, Suzuki M, Kitahora T, Miura S, Suzuki K, Hibi T et al (1987) Increased respiratory burst of leukocytes in inflammatory bowel diseases—the analysis of free radical generation by using chemiluminescence probe. J Clin Lab Immunol 24:125–128
Banks C, Bateman A, Payne R, Johnson P, Sheron N (2003) Chemokine expression in IBD. Mucosal chemokine expression is unselectively increased in both ulcerative colitis and Crohn’s disease. J Pathol 199:28–35
Kimura I, Nagahama S, Kawasaki M, Kataoka M, Sato M (1996) Study on the experimental ulcerative colitis (UC) model induced by dextran sulfate sodium (DSS) in rats (3). Folia Pharmacol Jpn 108:259–266
Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y, Nakaya R (1990) A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98:694–702
Kwon KH, Murakami A, Tanaka T, Ohigashi H (2005) Dietary rutin, but not its aglycone quercetin, ameliorates dextran sulfate sodium-induced experimental colitis in mice: attenuation of pro-inflammatory gene expression. Biochem Pharmacol 69(3):395–406
Hocman G (1989) Prevention of cancer: vegetables and plants. Comp Biochem Physiol B 93(2):201–212
Prior RL, Cao G, Martin A, Sofic E, McEwen JJ, O’Brien C et al (1998) Antioxidant capacity as influenced by total phenolic and anthocyanin content, maturity and variety of Vaccinium species. J Agric Food Chem 46:2686–2693
Kalt W, McDonald JE, Ricker RD, Lu X (1999) Anthocyanin content and profile within and among blueberry species. Can J Plant Sci 79:617–623
Galli RL, Shukitt-Hale B, Youdim KA, Joseph JA (2002) Fruit polyphenolics and brain aging: Nutritional interventions targeting age-related neuronal and behavioral deficits. Ann N Y Acad Sci 959:128–132
Sweeney MI, Kalt W, MacKinnon SL, Ashby J, Gottschall-Pass KT (2002) Feeding rats diets enriched in lowbush blueberries for six weeks decreases ischemia-induced brain damage. Nutr Neurosci 5:427–431
Youdim KA, McDonald J, Kalt W, Joseph JA (2002) Potential role of dietary flavonoids in reducing microvascular endothelium vulnerability to oxidative and inflammatory insults. J Nutr Biochem 13:282–288
Wang J, Mazza G (2002) Effects of anthocyanins and other phenolic compounds on the production of tumor necrosis factor α in LPS/IFN-γ-activated RAW 264.7 macrophages. J Agric Food Chem 50:4183–4189
Tsuda T, Horio F, Osawa T (1998) Dietary cyanidin 3-O-beta-d-glucoside increases ex vivo oxidation resistance of serum in rats. Lipids 33:583–588
Mazza G, Kay CD, Cottrell T, Holub BJ (2002) Absorption of anthocyanins from blueberries and serum antioxidant status in human subjects. J Agric Food Chem 50:7731–7737
Macfarlane GT, Cummings JH (2002) Probiotics, infection and immunity. Curr Opin Infect Dis 15:501–506
Mazza G, Fukumoto L, Delaquis P, Girard B, Ewert B (1999) Anthocyanins, phenolics, and color of Cabernet Franc, Merlot, and Pinot Noir wines from British Columbia. J Agric Food Chem 47:4009–4017
Talcott ST, Lee JH (2002) Ellagic acid and flavonoid antioxidant content of muscadine wine and juice. J Agric Food Chem 50:3186–3192
Martin LJ, Matar C (2005) Increase of antioxidant capacity of the lowbush blueberry (Vaccinium angustifolium) during fermentation by a novel bacterium from the fruit microflora. J Sci Food Agric 85:1477–1484
Johansson ML, Molin G, Jeppsson B, Nobaek S, Ahrne S, Bengmark S (1993) Administration of different Lactobacillus strains in fermented oatmeal soup: in vivo colonization of human intestinal mucosa and effect on the indigenous flora. Appl Environ Microbiol 59(1):15–20
Murthy SN, Cooper HS, Shim H, Shah RS, Ibrahim SA, Sedergran DI (1993) Treatment of dextran sulfate sodium-induced murine colitis by intracolonic cyclosporin. Dig Dis Sci 38(9):1722–1734
Cooper HS, Murthy SN, Shah RS, Sedergran DI (1993) Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest 69(2):238–249
Murthy S, Murthy NS, Coppola D, Wood DL (1997) The efficacy of BAY y 1015 in dextran sulfate model of mouse colitis. Inflamm Res 46:224–233
Quednau M, Ahrné S, Peterson AC, Molin G (1998) Identification of clinically important species of Enterococcus within 1 day with randomly amplified polymorphic DNA (RAPD). Curr Microbiol 36:332–336
Krawisz JE, Sharon P, Stenson WF (1984) Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models. Gastroenterology 87:1344–1350
Richardson AJ, Calder AG, Stewart CS, Smith A (1989) Simultaneous determination of volatile and non-volatile acidic fermentation products of anaerobes by capillary gas chromatography. Lett Appl Microbiol 9:5–8
Jensen MT, Cox RP, Jensen BB (1995) Microbial production of skatole in the hind gut of pigs given different diets and its relation to skatole deposition in back fat. Anim Sci 61:293–304
Fiocchi C (2005) Inflammatory bowel disease pathogenesis: therapeutic implications. Chin J Dig Dis 6(1):6–9
Schmidt C, Stallmach A (2005) Etiology and pathogenesis of inflammatory bowel disease. Minerva Gastroenterol Dietol 51(2):127–145
Faist E, Kim C (1998) Therapeutic immunomodulatory approaches for the control of systemic inflammatory response syndrome and the prevention of sepsis. New Horiz 6(Suppl 2):S97–S102
Araki Y, Andoh A, Fujiyama Y (2003) The free radical scavenger edaravone suppresses experimental dextran sulphate sodium-induced colitis in rats. Int J Mol Med 12(1):125–129
Peake J, Suzuki K (2004) Neutrophil activation, antioxidant supplements and exercise-induced oxidative stress. Exerc Immunol Rev 10:129–141
Dryden GW Jr, Deaciuc I, Arteel G, McClain CJ (2005) Clinical implications of oxidative stress and antioxidant therapy. Curr Gastroenterol Rep 7(4):308–316
Forrest CM, Gould SR, Darlington LG, Stone TW (2003) Levels of purine, kynurenine and lipid peroxidation products in patients with inflammatory bowel disease. Adv Exp Med Biol 527:395–400
Kruidenier L, Kuiper I, Lamers CB, Verspaget HW (2003) Intestinal oxidative damage in inflammatory bowel disease: semi-quantification, localization, and association with mucosal antioxidants. J Pathol 201(1):28–36
Kaizu M, Sasaki M, Nakajama H, Suzuki Y (1993) Effect of antioxidative lactic acid bacteria on rats fed a diet deficient in vitamin E. J Dairy Sci 76:2493–2499
Peuhkuri K, Lähteenmäki T, Sievi E, Saxelin M, Vapaatalo H, Korpela R (1996) Antioxidative properties of Lactobacillus GG measured as prostacyclin and nitric oxide production in endothelial cell culture. Nutr Today 31:53S–54S
Kullisaar T, Zilmer M, Mikelsaar M, Vihalemm T, Annuk H, Kairane C, Kilk A (2002) Two antioxidative lactobacilli strains as promising probiotics. Int J Food Microbiol 72:215–224
Hung J, Cooper D, Turner MS, Walsh T, Giffard PM (2003) Cystine uptake prevents production of hydrogen peroxide by Lactobacillus fermentum BR11. FEMS Microbiol Lett 227:93–99
Lin MY, Chang FY (2000) Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Dig Dis Sci 45:1617–1622
Oxman T, Shapira M, Diver A, Klein R, Avazov N, Rabinowitz B (2000) A new method of long-term preventive cardioprotection using Lactobacillus. Am J Physiol 278:H1717–H1724
Loguercio C, D’Argenio G, Delle Cave M, Cosenza V, Della Valle N, Mazzacca G, Del Vecchio Blanco C (2003) Glutathione supplementation improves oxidative damage in experimental colitis. Dig Liver Dis 35(9):635–641
Bibiloni R, Fedorak RN, Tannock GW, Madsen KL, Gionchetti P, Campieri M, De Simone C, Sartor RB (2005) VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol 100(7):1539–1546
Caradonna L, Amati L, Magrone T, Pellegrino NM, Jirillo E, Caccavo D (2000) Enteric bacteria, lipopolysaccharides and related cytokines in inflammatory bowel disease: biological and clinical significance. J Endotoxin Res 6(3):205–214
Ambrose NS, Johnson M, Burdon DW et al (1984) Incidence of pathogenic bacteria from mesenteric lymph nodes and ileal serosa during Crohn’s disease surgery. Br J Surg 71:623–625
Wiest R, Rath HC (2003) Gastrointestinal disorders of the critically ill. Bacterial translocation in the gut. Best Pract Res Clin Gastroenterol 17(3):397–425
MacFie J, Reddy BS, Gatt M, Jain PK, Sowdi R, Mitchell CJ (2006) Bacterial translocation studied in 927 patients over 13 years. Br J Surg 93:87–93
Schmidt BM, Howell AB, McEniry B, Knight CT, Seigler D, Erdman JW Jr, Lila MA (2004) Effective separation of potent antiproliferation and antiadhesion components from wild blueberry (Vaccinium angustifolium Ait.) fruits. J Agric Food Chem 52(21):6433–6442
Ishikawa H, Akedo I, Umesaki Y, Tanaka R, Imaoka A, Otani T (2003) Randomized controlled trial of the effect of bifidobacteria-fermented milk on ulcerative colitis. J Am Coll Nutr 22(1):56–63
Fooks LJ, Gibson GR (2002) Probiotics as modulators of the gut flora. Br J Nutr 88(Suppl 1):S39–S49
Ichikawa H, Shineha R, Satomi S, Sakata T (2002) Gastric or rectal instillation of short-chain fatty acids stimulates epithelial cell proliferation of small and large intestine in rats. Dig Dis Sci 47(5):1141–1146
Acknowledgments
This work was carried out with financial support from VINNOVA, Swedish Governmental Agency for Innovation Systems. It is also supported by grant no. K2000-72X-11616-04C from the Swedish Medical Research Council, Dir. A. Påhlsson’s Foundation, Ruth and Richard Julin’s Foundation, Malmö University Hospital, Lundgren’s Foundation, Gunnar Nilsson’s Foundation, and Apotekaren Hedberg’s Fond.
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Osman, N., Adawi, D., Ahrné, S. et al. Probiotics and Blueberry Attenuate the Severity of Dextran Sulfate Sodium (DSS)-Induced Colitis. Dig Dis Sci 53, 2464–2473 (2008). https://doi.org/10.1007/s10620-007-0174-x
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DOI: https://doi.org/10.1007/s10620-007-0174-x