Feeding Soy with Probiotic Attenuates  Obesity-Related Metabolic Syndrome Traits in Obese Zucker Rats

Lauren Mounts; Rajitha Sunkara; Louis Shackelford; Simon Ogutu; Lloyd T. Walker; Martha Verghese

doi:10.4236/fns.2015.69081

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Food and Nutrition Sciences > Vol.6 No.9, June 2015

Feeding Soy with Probiotic Attenuates Obesity-Related Metabolic Syndrome Traits in Obese Zucker Rats ()

Lauren Mounts¹, Rajitha Sunkara¹, Louis Shackelford¹, Simon Ogutu², Lloyd T. Walker², Martha Verghese^1*

¹Nutritional Biochemistry Laboratory, Department of Food & Animal Sciences, Alabama A & M University, Normal, AL, USA.
²Food Chemistry Laboratory, Department of Food & Animal Sciences, Alabama A & M University, Normal, AL, USA.

DOI: 10.4236/fns.2015.69081 PDF HTML XML 2,325 Downloads 2,768 Views

Abstract

Obesity has reached pandemic levels, being a major concern of health. Overweight and obesity are the precursors for metabolic disturbances in the body. Probiotics and prebiotics administrations have shown to reduce the characteristics of obesity-induced metabolic syndrome in animals. The present study examined the effects of dietary supplementation of soybean meal and Bifidobacterium longum (BB536) singly and in combination on obesity-related traits in obese Zucker rats. Control group rats were fed with AIN93-M diet and treatment groups were fed with soybean meal (5 % or 10%) and Bifidobacterium longum (0.1%) in single and combinations for 100 days. Weight gain, feed intake, and % of fat in liver were recorded. Serum biochemical parameters such as cholesterol, triglycerides, insulin and glucose were analyzed. Activities of liver enzymatic markers (alanine aminotransferase (ALT), gamma glutamyl-transferase (GGT), and alkaline phosphatase (ALP)) were determined. Dietary supplementation of soymeal at 10% with B. longum reduced the weight gain by 30% and liver fat content by 35%. Feeding Bifidobacterium longum alone did not have any effect in analyzing serum biochemical parameters and activity of liver enzymatic markers. Serum glucose and insulin levels in rats were lowered by 18% - 24% and 22% - 25% respectively when fed with administration of combinational feeding of soymeal at 5% and 10% with Bifidobacterium longum. Hepatic enzyme activity was reduced by 1.3 fold with the combinational diet at higher concentration (soy 10%). The present study provides evidence that supplementation with soymeal with probiotic, B. longum attenuates the metabolic disorders induced by obesity in obese Zucker rats.

Keywords

Obesity, Metabolic Syndrome, Soy, Bifidobacterium longum

Share and Cite:

Mounts, L. , Sunkara, R. , Shackelford, L. , Ogutu, S. , T. Walker, L. and Verghese, M. (2015) Feeding Soy with Probiotic Attenuates Obesity-Related Metabolic Syndrome Traits in Obese Zucker Rats. Food and Nutrition Sciences, 6, 780-789. doi: 10.4236/fns.2015.69081.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Ogden, C.L., Carroll, M.D., Kit, B.K. and Flegal, K.M. (2012) Prevalence of Obesity and Trends in Body Mass Index among US Children and Adolescents, 1999-2010. JAMA, 307, 483-490. http://dx.doi.org/10.1001/jama.2012.40
[2]	Sarti, C. and Gallagher, J. (2006) The Metabolic Syndrome: Prevalence, CHD Risk, and Treatment. Journal of Diabetes and Its Complications, 20, 121-132. http://dx.doi.org/10.1016/j.jdiacomp.2005.06.014
[3]	Devalaraja, S., Jain, S. and Yadav, H. (2011) Exotic Fruits as Therapeutic Complements for Diabetes, Obesity and Metabolic Syndrome. Food Research International, 44, 1856-1865. http://dx.doi.org/10.1016/j.foodres.2011.04.008
[4]	Fuller, R. (1992) History and Development of Probiotics. In: Probiotics, Springer, Netherlands, 1-8. http://dx.doi.org/10.1007/978-94-011-2364-8_1
[5]	Hamilton-Miller, J.M.T., Gibson, G.R. and Bruck, W. (2003) Some Insights into the Derivation and Early Uses of the Word ‘Probiotic’. British Journal of Nutrition, 90, 845-845. http://dx.doi.org/10.1079/BJN2003954
[6]	Vasiljevic, T. and Shah, N.P. (2008) Probiotics—From Metchnikoff to Bioactives. International Dairy Journal, 18, 714-728. http://dx.doi.org/10.1016/j.idairyj.2008.03.004
[7]	Metchnikoff, I.I. (2004) The Prolongation of Life: Optimistic Studies (Classics in Longevity and Aging). Springer Publishing Company, New York.
[8]	Shah, N.P. (2007) Functional Cultures and Health Benefits. International Dairy Journal, 17, 1262-1277. http://dx.doi.org/10.1016/j.idairyj.2007.01.014
[9]	B?ckhed, F., Ding, H., Wang, T., Hooper, L.V., Koh, G.Y., Nagy, A. and Gordon, J.I. (2004) The Gut Microbiota as an Environmental Factor That Regulates Fat Storage. Proceedings of the National Academy of Sciences of the United States of America, 101, 15718-15723. http://dx.doi.org/10.1073/pnas.0407076101
[10]	B?ckhed, F., Manchester, J.K., Semenkovich, C.F. and Gordon, J.I. (2007) Mechanisms Underlying the Resistance to Diet-Induced Obesity in Germ-Free Mice. Proceedings of the National Academy of Sciences, 104, 979-984. http://dx.doi.org/10.1073/pnas.0605374104
[11]	Fleissner, C.K., Huebel, N., Abd El-Bary, M.M., Loh, G., Klaus, S. and Blaut, M. (2010) Absence of Intestinal Microbiota Does Not Protect Mice from Diet-Induced Obesity. British Journal of Nutrition, 104, 919-929. http://dx.doi.org/10.1017/S0007114510001303
[12]	Rabot, S., Membrez, M., Bruneau, A., Gérard, P., Harach, T., Moser, M., et al. (2010) Germ-Free C57BL/6J Mice Are Resistant to High-Fat-Diet-Induced Insulin Resistance and Have Altered Cholesterol Metabolism. The FASEB Journal, 24, 4948-4959. http://dx.doi.org/10.1096/fj.10-164921
[13]	Ley, R.E., Turnbaugh, P.J., Klein, S. and Gordon, J.I. (2006) Microbial Ecology: Human Gut Microbes Associated with Obesity. Nature, 444, 1022-1023. http://dx.doi.org/10.1038/4441022a
[14]	Moze?, ?., Bujňáková, D., ?ef?íková, Z. and Kme?, V. (2008) Developmental Changes of Gut Microflora and Enzyme Activity in Rat Pups Exposed to Fat-Rich Diet. Obesity, 16, 2610-2615. http://dx.doi.org/10.1038/oby.2008.435
[15]	Turnbaugh, P.J., Ley, R.E., Mahowald, M.A., Magrini, V., Mardis, E.R. and Gordon, J.I. (2006) An Obesity-Associated Gut Microbiome with Increased Capacity for Energy Harvest. Nature, 444, 1027-1131. http://dx.doi.org/10.1038/nature05414
[16]	Wang, H.J. and Murphy, P.A. (1994) Isoflavone Content in Commercial Soybean Foods. Journal of Agricultural and Food Chemistry, 42, 1666-1673. http://dx.doi.org/10.1021/jf00044a016
[17]	Caldwell, C.R., Britz, S.J. and Mirecki, R.M. (2005) Effect of Temperature, Elevated Carbon Dioxide, and Drought during Seed Development on the Isoflavone Content of Dwarf Soybean [Glycine max (L.) Merrill] Grown in Controlled Environments. Journal of Agricultural and Food Chemistry, 53, 1125-1129. http://dx.doi.org/10.1021/jf0355351
[18]	Bhathena, S.J. and Velasquez, M.T. (2002) Beneficial Role of Dietary Phytoestrogens in Obesity and Diabetes. The American Journal of Clinical Nutrition, 76, 1191-1201.
[19]	Wang, W., Mejia, D. and Gonzalez, E. (2005) A New Frontier in Soy Bioactive Peptides That May Prevent Age-Related Chronic Diseases. Comprehensive Reviews in Food Science and Food Safety, 4, 63-78. http://dx.doi.org/10.1111/j.1541-4337.2005.tb00075.x
[20]	Sarti, C. and Gallagher, J. (2006) The Metabolic Syndrome: Prevalence, CHD Risk, and Treatment. Journal of Diabetes and Its Complications, 20, 121-132. http://dx.doi.org/10.1016/j.jdiacomp.2005.06.014
[21]	Kurtz, T.W., Morris, R.C. and Pershadsingh, H.A. (1989) The Zucker Fatty Rat as a Genetic Model of Obesity and Hypertension. Hypertension, 13, 896-901. http://dx.doi.org/10.1161/01.HYP.13.6.896
[22]	Lieber, C.S. (2004) Alcoholic Fatty Liver: Its Pathogenesis and Mechanism of Progression to Inflammation and Fibrosis. Alcohol, 34, 9-19. http://dx.doi.org/10.1016/j.alcohol.2004.07.008
[23]	Reeves, P.G. (1997) Components of the AIN-93 Diets as Improvements in the AIN-76A Diet. The Journal of Nutrition, 127, 838S-841S.
[24]	Lukaczer, D., De Ann, J.L., Lerman, R.H., Darland, G., Schiltz, B., Tripp, M. and Bland, J.S. (2006) Effect of a Low Glycemic Index Diet with Soy Protein and Phytosterols on CVD Risk Factors in Postmenopausal Women. Nutrition, 22, 104-113. http://dx.doi.org/10.1016/j.nut.2005.05.007
[25]	Merritt, J.C. (2004) Metabolic Syndrome: Soybean Foods and Serum Lipids. Journal of the National Medical Association, 96, 1032-1041.
[26]	Azadbakht, L., Kimiagar, M., Mehrabi, Y., Esmaillzadeh, A., Padyab, M., Hu, F.B. and Willett, W.C. (2007) Soy Inclusion in the Diet Improves Features of the Metabolic Syndrome: A Randomized Crossover Study in Postmenopausal Women. The American Journal of Clinical Nutrition, 85, 735-741.
[27]	Gadang, V., Gilbert, W., Hettiararchchy, N., Horax, R., Katwa, L. and Devareddy, L. (2011) Dietary Bitter Melon Seed Increases Peroxisome Proliferator-Activated Receptor-γ Gene Expression in Adipose Tissue, Down-Regulates the Nuclear Factor-κB Expression, and Alleviates the Symptoms Associated with Metabolic Syndrome. Journal of Medicinal Food, 14, 86-93. http://dx.doi.org/10.1089/jmf.2010.0010
[28]	Hurley, C., Richard, D., Deshaies, Y. and Jacques, H. (1998) Soy Protein Isolate in the Presence of Cornstarch Reduces Body Fat Gain in Rats. Canadian Journal of Physiology and Pharmacology, 76, 1000-1007. http://dx.doi.org/10.1139/y98-119
[29]	Iritani, N., Sugimoto, T., Fukuda, H., Komiya, M. and Ikeda, H. (1997) Dietary Soybean Protein Increases Insulin Receptor Gene Expression in Wistar Fatty Rats When Dietary Polyunsaturated Fatty Acid Level Is Low. The Journal of Nutrition, 127, 1077-1083.
[30]	Cani, P.D. and Delzenne, N.M. (2009) The Role of the Gut Microbiota in Energy Metabolism and Metabolic Disease. Current Pharmaceutical Design, 15, 1546-1558. http://dx.doi.org/10.2174/138161209788168164
[31]	Cani, P.D., Joly, E., Horsmans, Y. and Delzenne, N.M. (2006) Oligofructose Promotes Satiety in Healthy Human: A Pilot Study. European Journal of Clinical Nutrition, 60, 567-572. http://dx.doi.org/10.1038/sj.ejcn.1602350
[32]	Delzenne, N.M. and Cani, P.D. (2008) Gut Microflora Is a Key Player in Host Energy Homeostasis. Médecine/ Sciences: M/S, 24, 505-510. http://dx.doi.org/10.1051/medsci/2008245505
[33]	Takahashi, Y. and Ide, T. (2008) Effects of Soy Protein and Isoflavone on Hepatic Fatty Acid Synthesis and Oxidation and mRNA Expression of Uncoupling Proteins and Peroxisome Proliferator-Activated Receptor γ in Adipose Tissues of Rats. The Journal of Nutritional Biochemistry, 19, 682-693. http://dx.doi.org/10.1016/j.jnutbio.2007.09.003
[34]	Nagarajan, S. (2010) Mechanisms of Anti-Atherosclerotic Functions of Soy-Based Diets. The Journal of Nutritional Biochemistry, 21, 255-260. http://dx.doi.org/10.1016/j.jnutbio.2009.09.002
[35]	Galisteo, M., Duarte, J. and Zarzuelo, A. (2008) Effects of Dietary Fibers on Disturbances Clustered in the Metabolic Syndrome. The Journal of Nutritional Biochemistry, 19, 71-84. http://dx.doi.org/10.1016/j.jnutbio.2007.02.009
[36]	Ng, T.B., Li, W.W. and Yeung, H.W. (1987) Effects of Ginsenosides, Lectins and Momordica charantia Insulin-Like Peptide on Corticosterone Production by Isolated Rat Adrenal Cells. Journal of Ethnopharmacology, 21, 21-29. http://dx.doi.org/10.1016/0378-8741(87)90090-0
[37]	Madar, Z. (1985) Long-Term Effect of Feeding a New Fiber Fraction from Soybean to Zucker Fatty Rats. Nutrition Research, 5, 1161-1164. http://dx.doi.org/10.1016/S0271-5317(85)80148-2
[38]	Trujillo, J., Ramírez, V., Pérez, J., Torre-Villalvazo, I., Torres, N., Tovar, A.R., et al. (2005) Renal Protection by a Soy Diet in Obese Zucker Rats Is Associated with Restoration of Nitric Oxide Generation. American Journal of Physiology-Renal Physiology, 288, F108-F116. http://dx.doi.org/10.1152/ajprenal.00077.2004
[39]	Hotamisligil, G.S., Shargill, N.S. and Spiegelman, B.M. (1993) Adipose Expression of Tumor Necrosis Factor-Alpha: Direct Role in Obesity-Linked Insulin Resistance. Science, 259, 87-91. http://dx.doi.org/10.1126/science.7678183
[40]	Hotamisligil, G.S., Arner, P., Caro, J.F., Atkinson, R.L. and Spiegelman, B.M. (1995) Increased Adipose Tissue Expression of Tumor Necrosis Factor-Alpha in Human Obesity and Insulin Resistance. Journal of Clinical Investigation, 95, 2409-2415. http://dx.doi.org/10.1172/JCI117936
[41]	Artiss, J.D., Brogan, K., Brucal, M., Moghaddam, M. and Jen, K.L.C. (2006) The Effects of a New Soluble Dietary Fiber on Weight Gain and Selected Blood Parameters in Rats. Metabolism, 55, 195-202. http://dx.doi.org/10.1016/j.metabol.2005.08.012
[42]	Olson, B.H., Anderson, S.M., Becker, M.P., Anderson, J.W., Hunninghake, D.B., Jenkins, D.J., et al. (1997) Psyllium-Enriched Cereals Lower Blood Total Cholesterol and LDL Cholesterol, but Not HDL Cholesterol, in Hypercholesterolemic Adults: Results of a Meta-Analysis. The Journal of Nutrition, 127, 1973-1980.
[43]	Brown, L., Rosner, B., Willett, W.W. and Sacks, F.M. (1999) Cholesterol-Lowering Effects of Dietary Fiber: A Meta-Analysis. The American Journal of Clinical Nutrition, 69, 30-42.
[44]	Brennan, C.S. (2005) Dietary Fibre, Glycemic Response, and Diabetes. Molecular Nutrition & Food Research, 49, 560-570. http://dx.doi.org/10.1002/mnfr.200500025
[45]	Kao, Y.H., Hiipakka, R.A. and Liao, S. (2000) Modulation of Endocrine Systems and Food Intake by Green Tea Epigallocatechin Gallate. Endocrinology, 141, 980-987.
[46]	Diehl, A.M. (2005) Lessons from Animal Models of NASH. Hepatology Research, 33, 138-144. http://dx.doi.org/10.1016/j.hepres.2005.09.022
[47]	Neyrinck, A.M., Alexiou, H. and Delzenne, N.M. (2004) Kupffer Cell Activity Is Involved in the Hepatoprotective Effect of Dietary Oligofructose in Rats with Endotoxic Shock. The Journal of Nutrition, 134, 1124-1129.