Dietary flaxseed intake exacerbates acute colonic mucosal injury and inflammation induced by dextran sodium sulfate

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 306, Issue 12, 2014, Pages

  Zarepoor, Leila ^a,b   Lu, Jenifer T ^a,b   Zhang, Claire ^a,b   Wu, Wenqing ^a   Lepp, Dion ^a   Robinson, Lindsay ^b   Wanasundara, Janitha ^c   Cui, Steve ^a   Villeneuve, Sébastien ^a   Fofana, Bourlaye ^a   Tsao, Rong ^a   Wood, Geoffrey A ^b   Power, Krista A ^a,b  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b UNIVERSITY OF GUELPH   (Canada)

^c SASKATOON RESEARCH CENTRE   (Canada)

Author keywords

Experimental colitis; Flaxseed; Lignans; n 3 polyunsaturated fatty acids; Shortchain fatty acids

Indexed keywords

BIOLOGICAL MARKER; CHOLESTEROL; DEXTRAN SULFATE; DRINKING WATER; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIGNAN; MYELOPEROXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATF1 GENE; BACTERIAL TRANSLOCATION; BCL2A1A GENE; BIRC3 GENE; BODY WEIGHT; CCL5 GENE; CHOLESTEROL LIVER LEVEL; COLON INJURY; COLON MUCOSA; COLON MUCOSA INJURY; CONTROLLED STUDY; CYTOKINE RESPONSE; DIETARY FIBER; DIETARY INTAKE; DISEASE ACTIVITY; DISEASE EXACERBATION; EGFR GENE; ENDOTOXEMIA; EXPERIMENTAL COLITIS; FLUID INTAKE; FOOD COMPOSITION; GENE; GENE EXPRESSION; HISTOPATHOLOGY; INTESTINE MUCOSA PERMEABILITY; LINSEED; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NFKB1 GENE; NONHUMAN; PATHOGEN LOAD; PRIORITY JOURNAL; RELB GENE; SIGNAL TRANSDUCTION;

EXPERIMENTAL COLITIS; FLAXSEED; LIGNANS; N-3 POLYUNSATURATED FATTY ACIDS; SHORT-CHAIN FATTY ACIDS;

ACUTE DISEASE; ANIMALS; COLITIS; COLON; DEXTRAN SULFATE; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; FATTY ACIDS, OMEGA-3; FLAX; INTESTINAL MUCOSA; MALE; MICE; MICE, INBRED C57BL;

EID: 84902664373     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00253.2013     Document Type: Article

References (105)

1. Adolphe JL, Whiting SJ, Juurlink BH, Thorpe LU, Alcorn J. Health effects with consumption of the flax lignan secoisolariciresinol diglucoside. Br J Nutr 103: 929-938, 2010.
2. Araki Y, Mukaisyo K, Sugihara H, Fujiyama Y, Hattori T. Increased apoptosis and decreased proliferation of colonic epithelium in dextran sulfate sodium-induced colitis in mice. Oncol Rep 24: 869-874, 2010.
3. Aufreiter S, Kim JH, O'Connor DL. Dietary oligosaccharides increase colonic weight and the amount but not concentration of bacterially synthesized folate in the colon of piglets. J Nutr 141: 366-372, 2011.
4. Barros KV, Xavier RA, Abreu GG, Martinez CA, Ribeiro ML, Gambero A, Carvalho PO, Nascimento CM, Silveira VL. Soybean and fish oil mixture increases IL-10, protects against DNA damage and decreases colonic inflammation in rats with dextran sulfate sodium (DSS) colitis. Lipids Health Dis 9: 68, 2010.
5. Bassett CM, Rodriguez-Leyva D, Pierce GN. Experimental and clinical research findings on the cardiovascular benefits of consuming flaxseed. Appl Physiol Nutr Metab 34: 965-974, 2009.
6. Bommareddy A, Arasada BL, Mathees DP, Dwivedi C. Chemopreventive effects of dietary flaxseed on colon tumor development. Nutr Cancer 54: 216-222, 2006.
7. Bommareddy A, Zhang X, Schrader D, Kaushik RS, Zeman D, Matthees DP, Dwivedi C. Effects of dietary flaxseed on intestinal tumorigenesis in Apc(Min) mouse. Nutr Cancer 61: 276-283, 2009.
8. Bommareddy A, Zhang XY, Kaushik RS, Dwivedi C. Effects of components present in flaxseed on human colon adenocarcinoma Caco-2 cells: possible mechanisms of flaxseed on colon cancer development in animals. Drug Discoveries Ther 4: 184-189, 2010.
9. Breton J, Le Clere K, Daniel C, Sauty M, Nakab L, Chassat T, Dewulf J, Penet S, Carnoy C, Thomas P, Pot B, Nesslany F, Foligne B. Chronic ingestion of cadmium and lead alters the bioavailability of essential and heavy metals, gene expression pathways and genotoxicity in mouse intestine. Arch Toxicol 87: 1787-1795, 2013.
10. Brinkman BM, Becker A, Ayiseh RB, Hildebrand F, Raes J, Huys G, Vandenabeele P. Gut microbiota affects sensitivity to acute DSSinduced colitis independently of host genotype. Inflamm Bowel Dis 19: 2560-2567, 2013.
11. Butzner JD, Parmar R, Bell CJ, Dalal V. Butyrate enema therapy stimulates mucosal repair in experimental colitis in the rat. Gut 38: 568-573, 1996.
12. Cardoso Carraro JC, De Souza Dantas MI, Espeschit AC, Martino HS, Ribeiro SM. Flaxseed and human health: reviewing benefits and adverse effects. Food Rev Int 28: 203-230, 2011.
13. Chapkin RS, Hong MY, Fan YY, Davidson LA, Sanders LM, Henderson CE, Barhoumi R, Burghardt RC, Turner ND, Lupton JR. Dietary n-3 PUFA alter colonocyte mitochondrial membrane composition and function. Lipids 37: 193-199, 2002.
14. Chen J, Saggar JK, Corey P, Thompson LU. Flaxseed and pure secoisolariciresinol diglucoside, but not flaxseed hull, reduce human breast tumor growth (MCF-7) in athymic mice. J Nutr 139: 2061-2066, 2009.
15. Chen J, Saggar JK, Corey P, Thompson LU. Flaxseed cotyledon fraction reduces tumour growth and sensitises tamoxifen treatment of human breast cancer xenograft (MCF-7) in athymic mice. Br J Nutr 105: 339-347, 2011.
16. Christofidou-Solomidou M, Tyagi S, Pietrofesa R, Dukes F, Arguiri E, Turowski J, Grieshaber PA, Solomides CC, Cengel KA. Radioprotective role in lung of the flaxseed lignan complex enriched in the phenolic secoisolariciresinol diglucoside (SDG). Radiat Res 178: 568-580, 2012.
17. Christofidou-Solomidou M, Tyagi S, Pietrofesa R, Dukes F, Arguiri E, Turowski J, Grieshaber PA, Solomides CC, Cengel KA. Radioprotective role in lung of the flaxseed lignan complex enriched in the phenolic secoisolariciresinol diglucoside (SDG). Radiat Res 178: 568-580, 2012.
18. Clavel T, Henderson G, Alpert CA, Philippe C, Rigottier-Gois L, Dore J, Blaut M. Intestinal bacterial communities that produce active estrogen-like compounds enterodiol and enterolactone in humans. Appl Environ Microbiol 71: 6077-6085, 2005.
19. Cotterchio M, Boucher BA, Manno M, Gallinger S, Okey A, Harper P. Dietary phytoestrogen intake is associated with reduced colorectal cancer risk. J Nutr 136: 3046-3053, 2006.
20. Danbara N, Yuri T, Tsujita-Kyutoku M, Tsukamoto R, Uehara N, Tsubura A. Enterolactone induces apoptosis and inhibits growth of Colo 201 human colon cancer cells both in vitro and in vivo. Anticancer Res 25: 2269-2276, 2005.
21. Di Sabatino A, Morera R, Ciccocioppo R, Cazzola P, Gotti S, Tinozzi FP, Tinozzi S, Corazza GR. Oral butyrate for mildly to moderately active Crohn's disease. Aliment Pharmacol Ther 22: 789-794, 2005.
22. Dichi I, Frenhane P, Dichi JB, Correa CR, Angeleli AY, Bicudo MH, Rodrigues MA, Victoria CR, Burini RC. Comparison of ω-3 fatty acids and sulfasalazine in ulcerative colitis. Nutrition 16: 87-90, 2000.
23. Dignass A, Lindsay JO, Sturm A, Windsor A, Colombel JF, Allez M, D'Haens G, D'Hoore A, Mantzaris G, Novacek G, Oresland T, Reinisch W, Sans M, Stange E, Vermeire S, Travis S, Van Assche G. Second European evidence-based consensus on the diagnosis and management of ulcerative colitis. 2. Current management. J Crohns Colitis 6: 991-1030, 2012.
24. Dube PE, Yan F, Punit S, Girish N, McElroy SJ, Washington MK, Polk DB. Epidermal growth factor receptor inhibits colitis-associated cancer in mice. J Clin Invest 122: 2780-2792, 2012.
25. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric method for determination of sugars and related substances. Anal Chem 28: 350-356, 1956.
26. During A, Debouche C, Raas T, Larondelle Y. Among plant lignans, pinoresinol has the strongest antiinflammatory properties in human intestinal Caco-2 cells. J Nutr 142: 1798-1805, 2012.
27. Dwivedi C, Natarajan K, Matthees DP. Chemopreventive effects of dietary flaxseed oil on colon tumor development. Nutr Cancer 51: 52-58, 2005.
28. Fan YY, Ran Q, Toyokuni S, Okazaki Y, Callaway ES, Lupton JR, Chapkin RS. Dietary fish oil promotes colonic apoptosis and mitochondrial proton leak in oxidatively stressed mice. Cancer Prev Res (Phila) 4: 1267-1274, 2011.
29. Fedorak RN. Understanding why probiotic therapies can be effective in treating IBD. J Clin Gastroenterol 42 Suppl 3: S111-S115, 2008.
30. Fisk ID, Gray DA. Soybean (Glycine max) oil bodies and their associated phytochemicals. J Food Sci 76: C1349-C1354, 2011.
31. Fodje AM, Chang PR, Leterme P. In vitro bile acid binding and short-chain fatty acid profile of flax fiber and ethanol co-products. J Med Food 12: 1065-1073, 2009.
32. Gabele E, Dostert K, Hofmann C, Wiest R, Scholmerich J, Hellerbrand C, Obermeier F. DSS induced colitis increases portal LPS levels and enhances hepatic inflammation and fibrogenesis in experimental NASH. J Hepatol 55: 1391-1399, 2011.
33. Geier MS, Butler RN, Howarth GS. Inflammatory bowel disease: current insights into pathogenesis and new therapeutic options; probiotics, prebiotics and synbiotics. Int J Food Microbiol 115: 1-11, 2007.
34. Glew RH, Hernandez M, Pastuszyn A, Ernst J, Djomdi N, Vander-Jagt J. The amino acid, mineral and fatty acid content of three species of human plant foods in Cameroun. Food 4: 1-6, 2010.
35. Guarner F, Malagelada JR. Role of bacteria in experimental colitis. Best Pract Res Clin Gastroenterol 17: 793-804, 2003.
36. Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ. The role of butyrate on colonic function. Aliment Pharmacol Ther 27: 104-119, 2008.
37. Hanai H, Iida T, Takeuchi K, Watanabe F, Maruyama Y, Andoh A, Tsujikawa T, Fujiyama Y, Mitsuyama K, Sata M, Yamada M, Iwaoka Y, Kanke K, Hiraishi H, Hirayama K, Arai H, Yoshii S, Uchijima M, Nagata T, Koide Y. Curcumin maintenance therapy for ulcerative colitis: randomized, multicenter, double-blind, placebo-controlled trial. Clin Gastroenterol Hepatol 4: 1502-1506, 2006.
38. Hanauer SB. Evolving concepts in treatment and disease modification in ulcerative colitis. Aliment Pharmacol Ther 27 Suppl 1: 15-21, 2008.
39. Hassan A, Ibrahim A, Mbodji K, Coeffier M, Ziegler F, Bounoure F, Chardigny JM, Skiba M, Savoye G, Dechelotte P, Marion-Letellier R. An α-linolenic acid-rich formula reduces oxidative stress and inflammation by regulating NF-κB in rats with TNBS-induced colitis. J Nutr 140: 1714-1721, 2010.
40. Herchi W, Arraez-Roman D, Trabelsi H, Bouali I, Boukhchina S, Kallel H, Segura-Carretero A, Fernandez-Gutierrez A. Phenolic compounds in flaxseed: a review of their properties and analytical methods. An overview of the last decade. J Oleo Sci 63: 7-14, 2014.
41. Hookman P, Barkin JS. Clostridium difficile associated infection, diarrhea and colitis. World J Gastroenterol 15: 1554-1580, 2009.
42. Houvras Y, Benezra M, Zhang H, Manfredi JJ, Weber BL, Licht JD. BRCA1 physically and functionally interacts with ATF1. J Biol Chem 275: 36230-36237, 2000.
43. Ilan Y. Leaky gut and the liver: a role for bacterial translocation in nonalcoholic steatohepatitis. World J Gastroenterol 18: 2609-2618, 2012.
44. Iwamoto M, Koji T, Makiyama K, Kobayashi N, Nakane PK. Apoptosis of crypt epithelial cells in ulcerative colitis. J Pathol 180: 152-159, 1996.
45. Jenab M, Thompson LU. The influence of flaxseed and lignans on colon carcinogenesis and β-glucuronidase activity. Carcinogenesis 17: 1343-1348, 1996.
46. Jia Q, Ivanov I, Zlatev ZZ, Alaniz RC, Weeks BR, Callaway ES, Goldsby JS, Davidson LA, Fan YY, Zhou L, Lupton JR, McMurray DN, Chapkin RS. Dietary fish oil and curcumin combine to modulate colonic cytokinetics and gene expression in dextran sodium sulphatetreated mice. Br J Nutr 106: 519-529, 2011.
47. Jiang Q, Jiang Z, Hall YJ, Jang Y, Snyder PW, Bain C, Huang J, Jannasch A, Cooper B, Wang Y, Moreland M. γ-Tocopherol attenuates moderate but not severe colitis and suppresses moderate colitispromoted colon tumorigenesis in mice. Free Radic Biol Med 65C: 1069-1077, 2013.
48. John S, Luben R, Shrestha SS, Welch A, Khaw KT, Hart AR. Dietary n-3 polyunsaturated fatty acids and the aetiology of ulcerative colitis: a UK prospective cohort study. Eur J Gastroenterol Hepatol 22: 602-606, 2010.
49. Joo YE, Karrasch T, Muhlbauer M, Allard B, Narula A, Herfarth HH, Jobin C. Tomato lycopene extract prevents lipopolysaccharideinduced NF-κB signaling but worsens dextran sulfate sodium-induced colitis in NF-κBEGFP mice. PLos One 4: e4562, 2009.
50. Joza N, Kroemer G, Penninger JM. Genetic analysis of the mammalian cell death machinery. Trends Genet 18: 142-149, 2002.
51. Karlsson A, Jagervall A, Pettersson M, Andersson AK, Gillberg PG, Melgar S. Dextran sulphate sodium induces acute colitis and alters hepatic function in hamsters. Int Immunopharmacol 8: 20-27, 2008.
52. Koboziev I, Reinoso Webb C, Furr KL, Grisham MB. Role of the enteric microbiota in intestinal homeostasis and inflammation. Free Radic Biol Med 68C: 122-133, 2014.
53. 2+ loading and apoptosis in colonocytes. Cancer 117: 5294-5303, 2011.
54. Kuijsten A, Arts IC, van't Veer P, Hollman PC. The relative bioavailability of enterolignans in humans is enhanced by milling and crushing of flaxseed. J Nutr 135: 2812-2816, 2005.
55. Lee JC, Krochak R, Blouin A, Kanterakis S, Chatterjee S, Arguiri E, Vachani A, Solomides CC, Cengel KA, Christofidou-Solomidou M. Dietary flaxseed prevents radiation-induced oxidative lung damage, inflammation and fibrosis in a mouse model of thoracic radiation injury. Cancer Biol Ther 8: 47-53, 2009.
56. Leonel AJ, Alvarez-Leite JI. Butyrate: implications for intestinal function. Curr Opin Clin Nutr Metab Care 15: 474-479, 2012.
57. Lin B, Gong J, Wang Q, Cui S, Yu H, Huang B. In-vitro assessment of the effects of dietary fibers on microbial fermentation and communities from large intestinal digesta of pigs. Food Hydrocolloids 25: 180-188, 2011.
58. Low D, Nguyen DD, Mizoguchi E. Animal models of ulcerative colitis and their application in drug research. Drug Design Dev Ther 7: 1341-1357, 2013.
59. Mangerich A, Knutson CG, Parry NM, Muthupalani S, Ye W, Prestwich E, Cui L, McFaline JL, Mobley M, Ge Z, Taghizadeh K, Wishnok JS, Wogan GN, Fox JG, Tannenbaum SR, Dedon PC. Infection-induced colitis in mice causes dynamic and tissue-specific changes in stress response and DNA damage leading to colon cancer. Proc Natl Acad Sci USA 109: E1820-E1829, 2012.
60. Marsh JW, Curry SR. Therapeutic approaches for Clostridium difficile infections. Current Protocols Microbiol 30: 1-9, 2013.
61. Melgar S, Bjursell M, Gerdin AK, Svensson L, Michaelsson E, Bohlooly YM. Mice with experimental colitis show an altered metabolism with decreased metabolic rate. Am J Physiol Gastrointest Liver Physiol 292: G165-G172, 2007.
62. Mopper K, Schultz CA, Chevolot L, Germain C, Revuelta R, Dawson R. Determination of sugars in unconcentrated seawater and other natural waters by liquid chromatography and pulsed amperometric detection. Environ Sci Technol 26: 133-138, 1992.
63. Morimoto M, Watanabe T, Yamori M, Takebe M, Wakatsuki Y. Isoflavones regulate innate immunity and inhibit experimental colitis. J Gastroenterol Hepatol 24: 1123-1129, 2009.
64. Nadkarni MA, Martin FE, Jacques NA, Hunter N. Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148: 257-266, 2002.
65. Naito Y, Takagi T, Katada K, Uchiyama K, Kuroda M, Kokura S, Ichikawa H, Watabe J, Yoshida N, Okanoue T, Yoshikawa T. Partially hydrolyzed guar gum down-regulates colonic inflammatory response in dextran sulfate sodium-induced colitis in mice. J Nutr Biochem 17: 402-409, 2006.
66. Ng Y, Barhoumi R, Tjalkens RB, Fan YY, Kolar S, Wang N, Lupton JR, Chapkin RS. The role of docosahexaenoic acid in mediating mitochondrial membrane lipid oxidation and apoptosis in colonocytes. Carcinogenesis 26: 1914-1921, 2005.
67. Oikarinen SI, Pajari AM, Salminen I, Heinonen SM, Adlercreutz H, Mutanen M. Effects of a flaxseed mixture and plant oils rich in α-linolenic acid on the adenoma formation in multiple intestinal neoplasia (Min) mice. Br J Nutr 94: 510-518, 2005.
68. Oomah BD. Processing of flaxseed fiber, oil, protein, and lignan. In: Flaxseed in Human Nutrition, edited by Thompson LU. Urbana, IL: Am. Oil Chemists' Soc., 2003.
69. Park MY, Ji GE, Sung MK. Dietary kaempferol suppresses inflammation of dextran sulfate sodium-induced colitis in mice. Dig Dis Sci 57: 355-363, 2012.
70. Pellizzon MA, Billheimer JT, Bloedon LT, Szapary PO, Rader DJ. Flaxseed reduces plasma cholesterol levels in hypercholesterolemic mouse models. J Am Coll Nutr 26: 66-75, 2007.
71. Pietrofesa R, Turowski J, Tyagi S, Dukes F, Arguiri E, Busch TM, Gallagher-Colombo SM, Solomides CC, Cengel KA, Christofidou-Solomidou M. Radiation mitigating properties of the lignan component in flaxseed. BMC Cancer 13: 179, 2013.
72. Podolsky DK. Inflammatory bowel disease. N Engl J Med 347: 417-429, 2002.
73. Power KA, Chen JM, Saarinen NM, Thompson LU. Changes in biomarkers of estrogen receptor and growth factor signaling pathways in MCF-7 tumors after short-and long-term treatment with soy and flaxseed. J Steroid Biochem Mol Biol 112: 13-19, 2008.
74. Qu H, Madl RL, Takemoto DJ, Baybutt RC, Wang W. Lignans are involved in the antitumor activity of wheat bran in colon cancer SW480 cells. J Nutr 135: 598-602, 2005.
75. Rath HC, Ikeda JS, Linde HJ, Scholmerich J, Wilson KH, Sartor RB. Varying cecal bacterial loads influences colitis and gastritis in HLA-B27 transgenic rats. Gastroenterology 116: 310-319, 1999.
76. Ravnefjord A, Pettersson M, Rehnstrom E, Martinez V. Acute colonic ischaemia in rats results in long-term structural changes without alterations of colonic sensitivity. Int J Exp Pathol 89: 476-489, 2008.
77. Roberfroid M, Gibson GR, Hoyles L, McCartney AL, Rastall R, Rowland I, Wolvers D, Watzl B, Szajewska H, Stahl B, Guarner F, Respondek F, Whelan K, Coxam V, Davicco MJ, Leotoing L, Wittrant Y, Delzenne NM, Cani PD, Neyrinck AM, Meheust A. Prebiotic effects: metabolic and health benefits. Br J Nutr 104 Suppl 2: S1-S63, 2010.
78. Roediger WE. Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 21: 793-798, 1980.
79. Rogler G. Inflammatory bowel disease cancer risk, detection and surveillance. Dig Dis 30 Suppl 2: 48-54, 2012.
80. Roscic-Mrkic B, Fischer M, Leemann C, Manrique A, Gordon CJ, Moore JP, Proudfoot AE, Trkola A. RANTES (CCL5) uses the proteoglycan CD44 as an auxiliary receptor to mediate cellular activation signals and HIV-1 enhancement. Blood 102: 1169-1177, 2003.
81. Russell WR, Hoyles L, Flint HJ, Dumas ME. Colonic bacterial metabolites and human health. Curr Opin Microbiol 16: 246-254, 2013.
82. Scheppach W, Sommer H, Kirchner T, Paganelli GM, Bartram P, Christl S, Richter F, Dusel G, Kasper H. Effect of butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology 103: 51-56, 1992.
83. Segain JP, Raingeard de la Bletiere D, Bourreille A, Leray V, Gervois N, Rosales C, Ferrier L, Bonnet C, Blottiere HM, Galmiche JP. Butyrate inhibits inflammatory responses through NFκB inhibition: implications for Crohn's disease. Gut 47: 397-403, 2000.
84. Serraino M, Thompson LU. Flaxseed supplementation and early markers of colon carcinogenesis. Cancer Lett 63: 159-165, 1992.
85. Shahidi F, Wanasundara PK. Cyanogenic glycosides of flaxseeds. In: Antinutrients and Phytochemicals in Food. Washington, DC: Am. Chem. Soc., 1997, p. 171-185.
86. Singh P, Mogra P, Sankhla V, Deora K. Protective effects of curcumin on cadmium chloride induced colon toxicity in Swiss albino mice. J Cell Mol Biol 9: 31-36, 2011.
87. Steinhart AH, Hiruki T, Brzezinski A, Baker JP. Treatment of left-sided ulcerative colitis with butyrate enemas: a controlled trial. Aliment Pharmacol Ther 10: 729-736, 1996.
88. Sugawara T, Miyazawa T. Beneficial effect of dietary wheat glycolipids on cecum short-chain fatty acid and secondary bile acid profiles in mice. J Nutr Sci Vitaminol (Tokyo) 47: 299-305, 2001.
89. Tedelind S, Westberg F, Kjerrulf M, Vidal A. Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: a study with relevance to inflammatory bowel disease. World J Gastroenterol 13: 2826-2832, 2007.
90. Thorsen AJ. Noninfectious colitides: collagenous colitis, lymphocytic colitis, diversion colitis, and chemically induced colitis. Clin Colon Rectal Surg 20: 47-57, 2007.
91. Turk HF, Monk JM, Fan YY, Callaway ES, Weeks B, Chapkin RS. Inhibitory effects of ω-3 fatty acids on injury-induced epidermal growth factor receptor transactivation contribute to delayed wound healing. Am J Physiol Cell Physiol 304: C905-C917, 2013.
92. Turner D, Shah PS, Steinhart AH, Zlotkin S, Griffiths AM. Maintenance of remission in inflammatory bowel disease using ω-3 fatty acids (fish oil): a systematic review and meta-analyses. Inflamm Bowel Dis 17: 336-345, 2011.
93. Tyagi A, Kumar U, Reddy S, Santosh VS, Mohammed SB, Ehtesham NZ, Ibrahim A. Attenuation of colonic inflammation by partial replacement of dietary linoleic acid with α-linolenic acid in a rat model of inflammatory bowel disease. Br J Nutr 108: 1612-1622, 2012.
94. Uko V, Thangada S, Radhakrishnan K. Liver disorders in inflammatory bowel disease. Gastroenterol Res Pract 2012: 642923, 2012.
95. Veereman-Wauters G, Staelens S, Van de Broek H, Plaskie K, Wesling F, Roger LC, McCartney AL, Assam P. Physiological and bifidogenic effects of prebiotic supplements in infant formulae. J Pediatr Gastroenterol Nutr 52: 763-771, 2011.
96. Vernia P, Annese V, Bresci G, d'Albasio G, D'Inca R, Giaccari S, Ingrosso M, Mansi C, Riegler G, Valpiani D, Caprilli R. Topical butyrate improves efficacy of 5-ASA in refractory distal ulcerative colitis: results of a multicentre trial. Eur J Clin Invest 33: 244-248, 2003.
97. Vetuschi A, Latella G, Sferra R, Caprilli R, Gaudio E. Increased proliferation and apoptosis of colonic epithelial cells in dextran sulfate sodium-induced colitis in rats. Dig Dis Sci 47: 1447-1457, 2002.
98. Vieira EL, Leonel AJ, Sad AP, Beltrao NR, Costa TF, Ferreira TM, Gomes-Santos AC, Faria AM, Peluzio MC, Cara DC, Alvarez-Leite JI. Oral administration of sodium butyrate attenuates inflammation and mucosal lesion in experimental acute ulcerative colitis. J Nutr Biochem 23: 430-436, 2012.
99. Wallace KL, Zheng LB, Kanazawa Y, Shih DQ. Immunopathology of inflammatory bowel disease. World J Gastroenterol 20: 6-21, 2014.
100. Werner AB, de Vries E, Tait SW, Bontjer I, Borst J. Bcl-2 family member Bfl-1/A1 sequesters truncated Bid to inhibit is collaboration with pro-apoptotic Bak or Bax. J Biol Chem 277: 22781-22788, 2002.
101. Woodworth HL, McCaskey SJ, Duriancik DM, Clinthorne JF, Langohr IM, Gardner EM, Fenton JI. Dietary fish oil alters T lymphocyte cell populations and exacerbates disease in a mouse model of inflammatory colitis. Cancer Res 70: 7960-7969, 2010.
102. Yates CM, Calder PC, Ed Rainger G. Pharmacology and therapeutics of ω-3 polyunsaturated fatty acids in chronic inflammatory disease. Pharmacol Ther 141: 272-282, 2014.
103. Zanetti M, Castiglioni P, Schoenberger S, Gerloni M. The role of relB in regulating the adaptive immune response. Ann NY Acad Sci 987: 249-257, 2003.
104. Zhang C, Monk JM, Lu JT, Zarepoor L, Wu W, Liu R, Pauls KP, Wood GA, Robinson L, Tsao R, Power KA. Cooked navy and black bean diets improve biomarkers of colon health and reduce inflammation during colitis. Br J Nutr 111: 1549-1563, 2014.
105. Zhang YZ, Li YY. Inflammatory bowel disease: pathogenesis. World J Gastroenterol 20: 91-99, 2014.