The Indian Journal of Nutrition and Dietetics

Open Access Open Access  Restricted Access Subscription Access
Open Access Open Access Open Access  Restricted Access Restricted Access Subscription Access

Dietary Fat and Cholesterol Interactively Alter Serum Lipids and Gut Microbiota in Wistar Rats


Affiliations
1 Department of Nutrition and Food Technology, Human Nutrition and Dietetics, The University of Jordan, Amman 11942, Jordan
     

   Subscribe/Renew Journal


Effects of dietary fat type on serum lipids and gut microbiota in cholesterol-fed rats were investigated. Forty-eight male Wistar rats were assigned (8/group) into three cholesterol-free (control) diets containing Corn Oil (CO), Sheep Tallow (ST) or Olive Oil (OO) or three cholesterol-supplemented (experimental) diets (COC, STC, OOC) and given ad libtium for nine weeks. Serum lipids, atherogenic indexes and several biological parameters were determined. Total Bacterial Counts (TBC) and seven bacterial groups were assessed. High-density lipoprotein cholesterol was higher (p<0.003) in CO (89.9 ± 6.5 mg/dl) and OO (80.9 ± 3.0 mg/dl) than ST (55.9 ± 4.3 mg/dl). Higher (p<0.05) total cholesterol and atherogenic coefficient were respectively found in OOC (131.4 ± 9.9 mg/dl, 1.20 ± 0.03 mg/dl) and COC (113.6 ± 10.6 mg/dl, 1.46 ± 0.35 mg/dl) than OO (96.4 ± 2.6 mg/dl, 0.19 ± 0.03 mg/dl) and CO (93.6 ± 2.6 mg/dl, 0.04 ± 0.03 mg/dl), but not in STC (95.8 ± 6.5 mg/dl, 0.70 ± 0.20 mg/dl) versus ST (87.0 ± 7.8 mg/dl, 0.60 ± 0.06 mg/dl). Neither fat nor cholesterol affected body weight, food intake, Bacteroidetes, Clostridium cluster IV, Lactobacillus, and Prevotella. Total Bacterial Count, Clostridium Coccoides-Eubacterium rectalae and Bacteroides were respectively higher (p<0.001) in ST (74.0 ± 20.0, 53.1 ± 8.5, 103.6 ± 32.3) than OO (24.8 ± 3.1, 18.9 ± 5.8, 32.3 ± 15.5). Bacteroides was higher (p<0.05) in ST (103.6 ± 32.3) than COC (38.7 ± 7.8), and STC (97.2 ± 13.5) than OO (32.3 ± 15.5) or COC (38.7 ± 7.8). Firmicutes and Clostridium Coccoides-Eubacterium rectalae were respectively lower (p<0.05) in STC (15.3 ± 1.2, 19.0 ± 4.3) and COC (19.0 ± 2.8, 14.4 ± 1.5) than ST (30.3 ± 4.7, 53.3 ± 8.5) and CO (32.7 ± 2.8, 33.0 ± 7.8), but not in OOC (23.5 ± 3.7, 34.4 ± 6.0) versus OO (25.3 ± 4.7, 18.9 ± 5.8).In conclusion, dietary fat and cholesterol alter serum lipids and gut microbiota in an interaction that is likely to have clinical connotations in cholesterol-related disorders.

Keywords

Cholesterol, Dietary Fat, Dyslipidemia, Gut Microbiota, Lipid Profile, Serum, Wistar Rats.
User
Notifications

  • Alberti, K.G., Eckel, R.H., Grundy, S.M., Zimmet, P.Z., Cleeman, J.I., Donato, K.A., Fruchart, J. C., James, W.P.T., Loria, C. M. and Smith Jr. S.C., NHLBI; AHA; WHF; IAS; and IASO. Harmonizing the metabolic syndrome: A joint interim statement of the IDF task force on epidemiology and Prevention;. Circulat., 2009, 120, 1640-1645.

  • Balakumar, P., Maung, U.K. and Jagadeesh, G. Prevalence and prevention of cardiovascular disease and diabetes mellitus. Pharmacol. Res., 2016, 113, 600-609.

  • Hooper, L., Martin, N., Abdelhamid, A. and Davey Smith, G. Reduction in saturated fat intake for cardiovascular disease. Cochrane Database of Syst. Rev., 2015, 6, 1-160.

  • Briggs, M.A., Petersen, K.S. and Kris-Etherton, P.M. Saturated fatty acids and cardiovascular disease: Replacements for saturated fat to reduce cardiovascular risk. Healthcare (Basel)., 2017, 5, 1-29.

  • Ahmad, M. N. The effect of lentil on cholesterol-induced changes of serum lipid cardiovascular indexes in rats. Prog. Nutr., 2017, 19, 48-56.

  • Mazzocchi, A., Leone, L., Agostoni, C. and Pali-Scholl, I. The secrets of the Mediterranean diet. Does [Only] olive oil matter? Nutr., 2019, 11, 2941-2955.

  • Ley, R.E., Turnbaugh, P.J., Klein, S. and Gordon, J. I. Microbial ecology: human gut microbes associated with obesity. Nature, 2006, 444, 1022-1310.

  • Cani, P.D., Amar, J., Iglesias, M.A., Poggi, M., Knauf, C., Bastelica, D., Neyrinck, A.M., Fava, F., Tuohy, K.M., Chabo, C., Waget, A., Delmée, E., Cousin, B., Sulpice, T., Chamontin, B., Ferrières, J., Tanti, J.F., Gibson, G.R., Casteilla, L., Delzenne, N.M., Alessi, M.C. and Burcelin, R. Metabolic endotoxemia initiates obesity and insulin resistance. Diabet., 2007, 56, 1761-1772.

  • Caesar, R., Tremaroli, V., Kovatcheva-Datchary, P., Cani, P.D. and Backhed F. Crosstalk between gut microbiota and dietary lipids aggravates WAT inflammation through TLR signaling. Cell Metab., 2015, 22, 658-681.

  • Tremaroli, V. and Backhed, F. Functional interactions between the gut microbiota and host metabolism. Nature, 2012, 489, 242-249.

  • Muralidharan, J., Galie, S., Hernandez-Alonso, P., Bullo, M. and Salas-Salvado, J. Plant-based fat, dietary patterns rich in vegetable fat and gut microbiota modulation. Front Nutr., 2019, 6, 157-168.

  • Lam, Y.Y., Ha, C.W.Y., Hoffmann, J.M.A., Oscarsson, J., Dinudom, A., Mather, T.J., Cook, D.I., Hunt, N.H., Caterson, I.D., Holmes, A.J. and Storlien, L.H. Effects of dietary fat profile on gut permeability and microbiota and their relationships with metabolic changes in mice. Obesity (Silver Spring), 2015, 23, 1429-1439.

  • Kubeck, R., Bonet-Ripoll, C., Hoffmann, C., Walker, A., Muller, V.M., Schuppel, V.L., Lagkouvardos, I., Scholz, B., Engel, K.H., Daniel, H., Schmitt-Kopplin, P., Haller, D., Clavel,T. and Klingenspor, M. Dietary fat and gut microbiota interactions determine diet-induced obesity in mice. Mol. Metab., 2016, 5, 1162-1174.

  • Martinez, I., Perdicaro, D.J., Brown, A.W., Hammons, S., Carden, T.J., Carr, T.P., Eskridge, K.M. and Walter, J. Diet-induced alterations of host cholesterol metabolism are likely to affect the gut microbiota composition in hamsters. Appl. Environ. Microbiol., 2013, 79, 516-524.

  • Bo, T., Shao, S., Wu, D., Niu, S., Zhao, J. and Gao, L. Relative variations of gut microbiota in disordered cholesterol metabolism caused by high-cholesterol diet and host genetics. Microbiol. Open., 2017, 6, 1-11.

  • Dimova, L.G., Zlatkov, N., Verkade, H.J., Uhlin, B.E. and Tietge, U.J.F. High-cholesterol diet does not alter gut microbiota composition in mice. Nutr. Metab (Lond)., 2017, 14, 15-22.

  • Ahmad, M.N. and Khatib, F. Effects of dietary saturated, monounsaturated and polyunsaturated fats on plasma lipids and lipoproteins in diabetic rats. Ecol. Fd. Nutr., 1990, 24, 141-148.

  • Reeves, P.G. Components of the AIN-93 diets as improvements in the AIN-76A diet. J. Nutr., 1997, 127, 838-841.

  • National Academy of Sciences, Guide for the care and use of laboratory animals. 8th ed. Washington: National Academic Press; 2011.

  • Mujico, J.R., Baccan, G.C., Gheorghe, A., Diaz, L.E. and Marcos, A. Changes in gut microbiota due to supplemented fatty acids in diet-induced obese mice. Br. J. Nutr., 2013, 110, 711-720.

  • Bonot, S., Courtois, S., Block, J.C. and Merlin C. Improving the recovery of qPCR-grade DNA from sludge and sediment. Appl. Microbiol. Biotechnol., 2010, 87, 2303-2311.

  • Remely, M., Tesar, I., Hippe, B., Gnauer, S., Rust, P. and Haslberger, A.G. Gut microbiota composition correlates with changes in body fat content due to weight loss. Beneficial Microbes, 2015, 1-9.

  • Rinttila, T., Kassinen, A., Malinen, E., Krogius, L. and Palva, A. Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J. Appl. Microbiol., 2004, 97, 1166-1177.

  • Xu, W., Li, L., Lu, J., Luo, Y., Shang, Y. and Huang, K. Analysis of caecal microbiota in rats fed with genetically modified rice by real-time quantitative PCR. J. Fd. Sci., 2011, 76, 88-93.

  • Matsuki, T., Watanabe, K., Fujimoto, J., Miyamoto, Y., Takada, T., Matsumoto, K., Oyaizu, H. and Tanaka, R. Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl. Environ. Microbiol., 2002, 68, 5445-5451.

  • Pedersen, R., Andersen, A.D., Molbak, L., Stagsted, J. and Boye, M. Changes in the gut microbiota of cloned and non-cloned control pigs during development of obesity: gut microbiota during development of obesity in cloned pigs. BMC Microbiol., 2013, 13, 30-39.

  • Friedewald, W.T., Levy, R.I. and Fredrickson, D.S. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin. Chem., 1972, 18, 499-502.

  • Katsarou, A.I., Kaliora, A.C., Papalois, A., Chiou, A., Kalogeropoulos, N., Agrogiannis, G. and Andrikopoulos, N.K. Serum lipid profile and inflammatory markers in the aorta of cholesterol-fed rats supplemented with extra virgin olive oil, sunflower oils and oil-products. Int. J. Fd. Sci. Nutr., 2015, 66, 766-773.

  • Hashimoto, Y., Yamada, K., Tsushima, H., Miyazawa, D., Mori, M., Nishio, K., Ohkubo, T., Hibino, H., Ohara, N. and Okuyama, H. Three dissimilar high fat diets differentially regulate lipid and glucose metabolism in obesity-resistant Slc:Wistar/ST rats. Lipids, 2013, 48, 803-815.

  • de Wit, N., Derrien, M., Bosch-Vermeulen, H., Oosterink, E., Keshtkar, S., Duval, C., Johan de Vogel-van den Bosch, Kleerebezem, M., Müller, M. and Roelof van der Meer. 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, 589-599.

  • Buettner, R., Parhofer, K.G., Woenckhaus, M., Wrede, C.E., Kunz-Schughart, L.A., Scholmerich, J. and Bollheimer, L.C. Defining high-fat-diet rat models: metabolic and molecular effects of different fat types. J. Mol. Endocrinol., 2006, 36, 485-501.

  • Gnoni, A. and Giudetti, A.M. Dietary long-chain unsaturated fatty acids acutely and differently reduce the activities of lipogenic enzymes and of citrate carrier in rat liver. J. Physiol. Biochem., 2016, 72, 485-494.

  • Alphonse, P.A., Ramprasath, V. and Jones, P.J. Effect of dietary cholesterol and plant sterol consumption on plasma lipid responsiveness and cholesterol trafficking in healthy individuals. Br. J. Nutr., 2017, 117, 56-66.

  • Hur, S.J., Min, B., Nam, K.C., Lee, E.J. and Ahn, D.U. Effect of dietary cholesterol and cholesterol oxides on blood cholesterol, lipids, and the development of atherosclerosis in rabbits. Int. J. Mol. Sci., 2013, 14, 12593-12606.

  • Subramanian, S., Goodspeed, L., Wang, S., Kim, J., Zeng, L., Ioannou, G.N., Haigh,W.G., Yeh, M.M., Kowdley, K.V., O’Brien, K.D., Pennathur, S. and Chait, A. Dietary cholesterol exacerbates hepatic steatosis and inflammation in obese LDL receptor-deficient mice. J. Lipid Res., 2011, 52, 1626-1635.

  • Ahmad, M.N. and Abdoh, M.J. The Effect of date palm fruit (Phoenix dactylifera L.) on serum lipid and lipoprotein concentrations in rats fed cholesterol-supplemented diet. Medit. J. Nutr. Metab., 2015, 8, 51-60.

  • Szajewska, H. and Szajewski, T. Saturated fat controversy: importance of systematic reviews and meta-analyses. Crit. Rev. Fd. Sci. Nutr., 2016, 59, 1947-1951.

  • Trautwein, E.A, Rieckhoff, D., Kunath-Rau, A. and Erbersdobler, H.F. Replacing saturated fat with PUFA-rich (sunflower oil) or MUFA-rich (rapeseed, olive and high-oleic sunflower oil) fats resulted in comparable hypocholesterolemic effects in cholesterol-fed hamsters. Ann. Nutr. Metab., 1999, 43, 159-172.

  • Ahmad, M.N. and Takruri, H.R. The effect of dietary wheat bran on sucrose-induced changes of serum glucose and lipids in rats. Nutr. Hosp., 2015, 32, 1636-1644.

  • Calder, P.C. and Deckelbaum, R.J. Dietary fatty acids in health and disease: greater controversy, greater interest. Curr. Opin. Clin. Nutr. Metab. Care., 2014, 17, 111-115.

  • Diniz, Y.S., Cicogna, A.C., Padovani, C.R., Santana, L.S., Faine, L.A. and Novelli, E.L. Diets rich in saturated and polyunsaturated fatty acids: metabolic shifting and cardiac health. Nutr., 2004, 20, 230-234.

  • Legrand, P., Beauchamp, E., Catheline, D., Pedrono, F. and Rioux, V. Short chain saturated fatty acids decrease circulating cholesterol and increase tissue PUFA content in the rat. Lipids, 2010, 45, 975-986.

  • Jurgonski, A., Juskiewicz, J. and Zdunczyk, Z. A high-fat diet differentially affects the gut metabolism and blood lipids of rats depending on the type of dietary fat and carbohydrate. Nutr. 2014, 6, 616-626.

  • Newberry, E.P., Kennedy, S.M., Xie, Y., Luo, J. and Davidson, N.O. Diet-induced alterations in intestinal and extrahepatic lipid metabolism in liver fatty acid binding protein knockout mice. Mol. Cell Biochem., 2009, 326, 79-86.

  • Chen, Y.L., Peng, H.C., Wang, X.D. and Yang, S.C. Dietary saturated fatty acids reduce hepatic lipid accumulation but induce fibrotic change in alcohol-fed rats. Hepatobil Surg Nutr. 2015, 4, 172-183.

  • Rabot, S., Membrez, M., Bruneau, A., Gerard, P., Harach, T., Moser, M., Raymond, F., Mansourian, R. and Chou, C.J. Germ-free C57BL/6J mice are resistant to high-fat-diet-induced insulin resistance and have altered cholesterol metabolism. FASEB J., 2010, 24, 4948-4959.

  • Caesar, R., Nygren, H., Oresic, M. and Backhed, F. Interaction between dietary lipids and gut microbiota regulates hepatic cholesterol metabolism. J. Lipid Res., 2016, 57, 474-481.

  • Maukonen, J., Matto, J., Satokari, R., Soderlund, H., Mattila-Sandholm, T. and Saarela, M. PCR DGGE and RT-PCR DGGE show diversity and short-term temporal stability in the Clostridium coccoides-Eubacterium rectale group in the human intestinal microbiota. FEMS. Microbiol. Ecol., 2006, 58, 517-528.

  • Zwielehner, J., Liszt, K., Handschur, M., Lassl, C., Lapin, A. and Haslberger, A.G. Combined PCR-DGGE fingerprinting and quantitative-PCR indicates shifts in fecal population sizes and diversity of Bacteroides, bifidobacteria and Clostridium cluster IV in institutionalized elderly. Exp. Gerontol., 2009, 44, 440-446.

  • Kurakawa, T., Ogata, K., Matsuda, K., Tsuji, H., Kubota, H., Takada, T., Kado, Y., Asahara, T., Takahashi, T. and Nomoto, N. Diversity of intestinal Clostridium coccoides group in the Japanese population, as demonstrated by reverse transcription-quantitative PCR. PLoS One, 2015, 10, 0126226.

  • Lee, S.M., Han, H.W. and Yim, S.Y. Beneficial effects of soy milk and fiber on high cholesterol diet-induced alteration of gut microbiota and inflammatory gene expression in rats. Fd. Funct., 2015, 6, 492-500.

  • David, L.A., Maurice, C.F., Carmody, R.N., Gootenberg. D.B., Button, J.E., Wolfe, B.E., Ling , A.V., Devlin, A. S., Varma, Y., Fischbach, M.A., Biddinger, S.B., Dutton, R. J. and Turnbaugh, P. J. Diet rapidly and reproducibly alters the human gut microbiome. Nature, 2014, 505, 559-563.

  • Patterson, E., RM, O.D., Murphy, E.F., Wall, R., O, O.S., Nilaweera, K., Fitzgerald, G.F., Cotter, P.D., Ross, R.P. and Stanton, C. Impact of dietary fatty acids on metabolic activity and host intestinal microbiota composition in C57BL/6J mice. Br. J. Nutr., 2014, 111, 1905-1917.

  • Devkota, S., Wang, Y., Musch, M.W., Leone, V., Fehlner-Peach, H., Nadimpalli, A., Antonopoulos, D. A., Jabri, B. and Chang, E.B. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature, 2012, 487, 104-108.

  • Okazaki, Y. and Katayama, T. Phytic acid actions on hepatic lipids and gut microbiota in rats fed a diet high in sucrose is influenced by dietary fat level. Nutr. Res., 2020, 74, 45-51.


Abstract Views: 224

PDF Views: 1




  • Dietary Fat and Cholesterol Interactively Alter Serum Lipids and Gut Microbiota in Wistar Rats

Abstract Views: 224  |  PDF Views: 1

Authors

Mousa Numan Ahmad
Department of Nutrition and Food Technology, Human Nutrition and Dietetics, The University of Jordan, Amman 11942, Jordan
Ghadeer A. Othman
Department of Nutrition and Food Technology, Human Nutrition and Dietetics, The University of Jordan, Amman 11942, Jordan

Abstract


Effects of dietary fat type on serum lipids and gut microbiota in cholesterol-fed rats were investigated. Forty-eight male Wistar rats were assigned (8/group) into three cholesterol-free (control) diets containing Corn Oil (CO), Sheep Tallow (ST) or Olive Oil (OO) or three cholesterol-supplemented (experimental) diets (COC, STC, OOC) and given ad libtium for nine weeks. Serum lipids, atherogenic indexes and several biological parameters were determined. Total Bacterial Counts (TBC) and seven bacterial groups were assessed. High-density lipoprotein cholesterol was higher (p<0.003) in CO (89.9 ± 6.5 mg/dl) and OO (80.9 ± 3.0 mg/dl) than ST (55.9 ± 4.3 mg/dl). Higher (p<0.05) total cholesterol and atherogenic coefficient were respectively found in OOC (131.4 ± 9.9 mg/dl, 1.20 ± 0.03 mg/dl) and COC (113.6 ± 10.6 mg/dl, 1.46 ± 0.35 mg/dl) than OO (96.4 ± 2.6 mg/dl, 0.19 ± 0.03 mg/dl) and CO (93.6 ± 2.6 mg/dl, 0.04 ± 0.03 mg/dl), but not in STC (95.8 ± 6.5 mg/dl, 0.70 ± 0.20 mg/dl) versus ST (87.0 ± 7.8 mg/dl, 0.60 ± 0.06 mg/dl). Neither fat nor cholesterol affected body weight, food intake, Bacteroidetes, Clostridium cluster IV, Lactobacillus, and Prevotella. Total Bacterial Count, Clostridium Coccoides-Eubacterium rectalae and Bacteroides were respectively higher (p<0.001) in ST (74.0 ± 20.0, 53.1 ± 8.5, 103.6 ± 32.3) than OO (24.8 ± 3.1, 18.9 ± 5.8, 32.3 ± 15.5). Bacteroides was higher (p<0.05) in ST (103.6 ± 32.3) than COC (38.7 ± 7.8), and STC (97.2 ± 13.5) than OO (32.3 ± 15.5) or COC (38.7 ± 7.8). Firmicutes and Clostridium Coccoides-Eubacterium rectalae were respectively lower (p<0.05) in STC (15.3 ± 1.2, 19.0 ± 4.3) and COC (19.0 ± 2.8, 14.4 ± 1.5) than ST (30.3 ± 4.7, 53.3 ± 8.5) and CO (32.7 ± 2.8, 33.0 ± 7.8), but not in OOC (23.5 ± 3.7, 34.4 ± 6.0) versus OO (25.3 ± 4.7, 18.9 ± 5.8).In conclusion, dietary fat and cholesterol alter serum lipids and gut microbiota in an interaction that is likely to have clinical connotations in cholesterol-related disorders.

Keywords


Cholesterol, Dietary Fat, Dyslipidemia, Gut Microbiota, Lipid Profile, Serum, Wistar Rats.

References





DOI: https://doi.org/10.21048/ijnd.2020.57.4.25502