Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
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Effect of vegetable oils with different fatty acid composition on high-fat diet-induced obesity and colon inflammation

  • Thomas, Shalom Sara (Department of Food Science and Human Nutrition, Jeonbuk National University) ;
  • Cha, Youn-Soo (Department of Food Science and Human Nutrition, Jeonbuk National University) ;
  • Kim, Kyung-Ah (Department of Food and Nutrition, Chungnam National University)
  • Received : 2020.02.25
  • Accepted : 2020.05.04
  • Published : 2020.10.01
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Abstract

BACKGROUND/OBJECTIVES: Different fatty acids exert different health benefits. This study investigated the potential protective effects of perilla, olive, and safflower oils on high-fat diet-induced obesity and colon inflammation. MATERIALS/METHODS: Five-week old, C57BL/6J mice were assigned to 5 groups: low-fat diet (LFD), high-fat diet (HFD) and high-fat diet supplemented with-perilla oil (HPO), olive oil (HOO), and safflower oil (HSO). After 16 weeks of the experimental period, the mice were sacrificed, and blood and tissues were collected. The serum was analyzed for obesity- and inflammation-related biomarkers. Gene expression of the biomarkers in the liver, adipose tissue, and colon tissue was analyzed. Micro-computed tomography (CT) analysis was performed one week before sacrifice. RESULTS: Treatment with all the three oils significantly improved obesity-induced increases in body weight, liver weight, and epididymal fat weight as well as serum triglyceride and leptin levels. Treatment with perilla oil (PO) and safflower oil (SO) increased adiponectin levels. The micro-CT analysis revealed that PO and SO reduced abdominal fat volume considerably. The mRNA expression of lipogenic genes was reduced in all the three oilsupplemented groups and PO upregulated lipid oxidation in the liver. Supplementation of oils improved macroscopic score, increased colon length, and decreased serum endotoxin and proinflammatory cytokine levels in the colon. The abundance of Bifidobacteria was increased and that of Enterobacteriaceae was reduced in the PO-supplemented group. All three oils reduced proinflammatory cytokine levels, as indicated by the mRNA expression. In addition, PO increased the expression of tight junction proteins. CONCLUSIONS: Taken together, our data indicate that the three oils exert similar anti-obesity effects. Interestingly, compared with olive oil and SO, PO provides better protection against high-fat diet-induced colon inflammation, suggesting that PO consumption helps manage inflammation-related diseases and provides omega-3 fatty acids needed by the body.

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References

  1. Kinlen D, Cody D, O'Shea D. Complications of obesity. QJM 2018;111:437-43. https://doi.org/10.1093/qjmed/hcx152
  2. Jung UJ, Choi MS. Obesity and its metabolic complications: the role of adipokines and the relationship between obesity, inflammation, insulin resistance, dyslipidemia and nonalcoholic fatty liver disease. Int J Mol Sci 2014;15:6184-223. https://doi.org/10.3390/ijms15046184
  3. Hruby A, Manson JE, Qi L, Malik VS, Rimm EB, Sun Q, Willett WC, Hu FB. Determinants and consequences of obesity. Am J Public Health 2016;106:1656-62. https://doi.org/10.2105/AJPH.2016.303326
  4. Lumeng CN, Saltiel AR. Inflammatory links between obesity and metabolic disease. J Clin Invest 2011;121:2111-7. https://doi.org/10.1172/JCI57132
  5. Saltiel AR, Olefsky JM. Inflammatory mechanisms linking obesity and metabolic disease. J Clin Invest 2017;127:1-4. https://doi.org/10.1172/JCI92035
  6. Yook JS, Kim KA, Kim M, Cha YS. Black adzuki bean (Vigna angularis) attenuates high-fat diet-induced colon inflammation in mice. J Med Food 2017;20:367-75. https://doi.org/10.1089/jmf.2016.3821
  7. Orsavova J, Misurcova L, Ambrozova JV, Vicha R, Mlcek J. Fatty acids composition of vegetable oils and its contribution to dietary energy intake and dependence of cardiovascular mortality on dietary intake of fatty acids. Int J Mol Sci 2015;16:12871-90. https://doi.org/10.3390/ijms160612871
  8. Lee AY, Choi JM, Lee MH, Lee J, Lee S, Cho EJ. Protective effects of perilla oil and alpha linolenic acid on SH-SY5Y neuronal cell death induced by hydrogen peroxide. Nutr Res Pract 2018;12:93-100. https://doi.org/10.4162/nrp.2018.12.2.93
  9. Schwingshackl L, Hoffmann G. Monounsaturated fatty acids, olive oil and health status: a systematic review and meta-analysis of cohort studies. Lipids Health Dis 2014;13:154. https://doi.org/10.1186/1476-511X-13-154
  10. Hsu SC, Huang CJ. Reduced fat mass in rats fed a high oleic acid-rich safflower oil diet is associated with changes in expression of hepatic $PPAR{\alpha}$ and adipose SREBP-1c-regulated genes. J Nutr 2006;136:1779-85. https://doi.org/10.1093/jn/136.7.1779
  11. Hooper L, Martin N, Abdelhamid A, Davey Smith G. Reduction in saturated fat intake for cardiovascular disease. Cochrane Database Syst Rev 2015:CD011737.
  12. Simopoulos AP. An Increase in the omega-6/omega-3 fatty acid ratio increases the risk for obesity. Nutrients 2016;8:128. https://doi.org/10.3390/nu8030128
  13. Lee AY, Choi JM, Lee J, Lee MH, Lee S, Cho EJ. Effects of vegetable oils with different fatty acid compositions on cognition and memory ability in $A{\beta}$ 25-35-induced Alzheimer's disease mouse model. J Med Food 2016;19:912-21. https://doi.org/10.1089/jmf.2016.3737
  14. Li Y, Hou MJ, Ma J, Tang ZH, Zhu HL, Ling WH. Dietary fatty acids regulate cholesterol induction of liver $CYP7{\alpha}1$ expression and bile acid production. Lipids 2005;40:455-62. https://doi.org/10.1007/s11745-005-1404-2
  15. Bhurosy T, Jeewon R. Overweight and obesity epidemic in developing countries: a problem with diet, physical activity, or socioeconomic status? Sci World J 2014;2014:964236.
  16. de Wit N, Derrien M, Bosch-Vermeulen H, Oosterink E, Keshtkar S, Duval C, de Vogel-van den Bosch J, Kleerebezem M, Muller M, van der Meer R. Saturated fat stimulates obesity and hepatic steatosis and affects gut microbiota composition by an enhanced overflow of dietary fat to the distal intestine. Am J Physiol Gastrointest Liver Physiol 2012;303:G589-99. https://doi.org/10.1152/ajpgi.00488.2011
  17. Siri-Tarino PW, Chiu S, Bergeron N, Krauss RM. Saturated fats versus polyunsaturated fats versus carbohydrates for cardiovascular disease prevention and treatment. Annu Rev Nutr 2015;35:517-43. https://doi.org/10.1146/annurev-nutr-071714-034449
  18. Ananthakrishnan AN, Khalili H, Konijeti GG, Higuchi LM, de Silva P, Fuchs CS, Willett WC, Richter JM, Chan AT. Long-term intake of dietary fat and risk of ulcerative colitis and Crohn's disease. Gut 2014;63:776-84. https://doi.org/10.1136/gutjnl-2013-305304
  19. Tian Y, Wang H, Yuan F, Li N, Huang Q, He L, Wang L, Liu Z. Perilla oil has similar protective effects of fish oil on high-fat diet-induced nonalcoholic fatty liver disease and gut dysbiosis. BioMed Res Int 2016;2016:9462571. https://doi.org/10.1155/2016/9462571
  20. Chen T, Yuan F, Wang H, Tian Y, He L, Shao Y, Li N, Liu Z. Perilla oil supplementation ameliorates high-fat/high-cholesterol diet induced nonalcoholic fatty liver disease in rats via enhanced fecal cholesterol and bile acid excretion. BioMed Res Int 2016;2016:2384561.
  21. Wani FA, Albahrawy AZ, Rahiman S. Hypolipidemic activity of olive oil (Olea europaea) against high fat diet-induced nonalcoholic fatty liver disease (NAFLD) in mice. Open J Pathol 2015;5:720-6.
  22. Thomas SS, Kim M, Lee SJ, Cha YS. Antiobesity effects of purple perilla (Perilla frutescens var. acuta) on adipocyte differentiation and mice fed a high-fat diet. J Food Sci 2018;83:2384-93. https://doi.org/10.1111/1750-3841.14288
  23. Kim SR, Je J, Jeong K, Kim SJ, Lee KY, Choi SG, Kim H, Park SW. Perilla oil decreases aortic and hepatic lipid accumulation by modulating lipogenesis and lipolysis in high-fat diet-fed mice. J Med Food 2019;22:14-21. https://doi.org/10.1089/jmf.2018.4226
  24. Zhang T, Zhao S, Li W, Ma L, Ding M, Li R, Liu Y. High-fat diet from perilla oil induces insulin resistance despite lower serum lipids and increases hepatic fatty acid oxidation in rats. Lipids Health Dis 2014;13:15. https://doi.org/10.1186/1476-511X-13-15
  25. Kim KA, Gu W, Lee IA, Joh EH, Kim DH. High fat diet-induced gut microbiota exacerbates inflammation and obesity in mice via the TLR4 signaling pathway. PLoS One 2012;7:e47713. https://doi.org/10.1371/journal.pone.0047713
  26. Lee JC, Lee HY, Kim TK, Kim MS, Park YM, Kim J, Park K, Kweon MN, Kim SH, Bae JW, Hur KY, Lee MS. Obesogenic diet-induced gut barrier dysfunction and pathobiont expansion aggravate experimental colitis. PLoS One 2017;12:e0187515. https://doi.org/10.1371/journal.pone.0187515
  27. Lim SM, Kim DH. Bifidobacterium adolescentis IM38 ameliorates high-fat diet-induced colitis in mice by inhibiting $NF-{\kappa}B$ activation and lipopolysaccharide production by gut microbiota. Nutr Res 2017;41:86-96. https://doi.org/10.1016/j.nutres.2017.04.003
  28. de La Serre CB, Ellis CL, Lee J, Hartman AL, Rutledge JC, Raybould HE. Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am J Physiol Gastrointest Liver Physiol 2010;299:G440-8. https://doi.org/10.1152/ajpgi.00098.2010
  29. Hassan A, Ibrahim A, Mbodji K, Coeffier M, Ziegler F, Bounoure F, Chardigny JM, Skiba M, Savoye G, Dechelotte P, Marion-Letellier R. An ${\alpha}$-linolenic acid-rich formula reduces oxidative stress and inflammation by regulating $NF-{\kappa}B$ in rats with TNBS-induced colitis. J Nutr 2010;140:1714-21. https://doi.org/10.3945/jn.109.119768
  30. Bigagli E, Toti S, Lodovici M, Giovannelli L, Cinci L, D'Ambrosio M, Luceri C. Dietary extra-virgin olive oil polyphenols do not attenuate colon inflammation in transgenic HLAB-27 rats but exert hypocholesterolemic effects through the modulation of HMGCR and PPAR-${\alpha}$ gene expression in the liver. Lifestyle Genom 2018;11:99-108. https://doi.org/10.1159/000495516
  31. Liao FH, Liou TH, Chiu WC, Shieh MJ, Chien YW. Differential effects of high MUFA with high or low P/S ratio (polyunsaturated to saturated fatty acids) on improving hepatic lipolytic enzymes and mediating $PPAR{\gamma}$ related with lipoprotein lipase and hormone-sensitive lipase of white adipose tissue in diet-induced obese hamster. Int J Obes 2010;34:1608-17. https://doi.org/10.1038/ijo.2010.88
  32. Liao FH, Liou TH, Shieh MJ, Chien YW. Effects of different ratios of monounsaturated and polyunsaturated fatty acids to saturated fatty acids on regulating body fat deposition in hamsters. Nutrition 2010;26:811-7. https://doi.org/10.1016/j.nut.2009.09.009
  33. Li Y, Hruby A, Bernstein AM, Ley SH, Wang DD, Chiuve SE, Sampson L, Rexrode KM, Rimm EB, Willett WC, Hu FB. Saturated fats compared with unsaturated fats and sources of carbohydrates in relation to risk of coronary heart disease: a prospective cohort study. J Am Coll Cardiol 2015;66:1538-48. https://doi.org/10.1016/j.jacc.2015.07.055

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