Effect of a Diet Rich in Interesterified, Non-Interesterified and Trans Fats on Biochemical Parameters and Oxidative Status of Balb-c Mice — Oak Academic Publishing
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Effect of a Diet Rich in Interesterified, Non-Interesterified and Trans Fats on Biochemical Parameters and Oxidative Status of Balb-c Mice
Campus Florianópolis Continente, Federal Institute of Education, Science and Technology of Santa Catarina, Florianópolis-SC, Brazil
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Laboratory of Experimental Biochemistry, Department of Biochemistry, Federal University of Santa Catarina, Florianópolis, SC, Brazil
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Laboratory of Experimental Biochemistry, Department of Biochemistry, Federal University of Santa Catarina, Florianópolis, SC, Brazil
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Laboratory of Fats and Oils, Department of Food Science and Technology, Federal University of Santa Catarina, Florianópolis, SC, Brazil
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Laboratory of Experimental Biochemistry, Department of Biochemistry, Federal University of Santa Catarina, Florianópolis, SC, Brazil
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Laboratory of Experimental Biochemistry, Department of Biochemistry, Federal University of Santa Catarina, Florianópolis, SC, Brazil
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Faculty of Pharmaceutical Sciences, University of São Paulo, São Paulo-SP, Brazil
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Department of Food Science and Technology, Facultad de Química, Universidad de la República, Montevideo, Uruguay
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Laboratory of Lipids, Department of Clinical Analysis, Federal University of Santa Catarina, Florianópolis-SC, Brazil
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Laboratory of Experimental Biochemistry, Department of Biochemistry, Federal University of Santa Catarina, Florianópolis, SC, Brazil
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Laboratory of Fats and Oils, Department of Food Science and Technology, Federal University of Santa Catarina, Florianópolis, SC, Brazil
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Laboratory of Lipid Research, Department of Family and Consumer Sciences, College of Agriculture and Environmental Sciences, North Carolina A & T State University, NC, USA
1 Campus Florianópolis Continente, Federal Institute of Education, Science and Technology of Santa Catarina, Florianópolis-SC, Brazil
2 Laboratory of Experimental Biochemistry, Department of Biochemistry, Federal University of Santa Catarina, Florianópolis, SC, Brazil
3 Laboratory of Experimental Biochemistry, Department of Biochemistry, Federal University of Santa Catarina, Florianópolis, SC, Brazil
4 Laboratory of Fats and Oils, Department of Food Science and Technology, Federal University of Santa Catarina, Florianópolis, SC, Brazil
5 Laboratory of Experimental Biochemistry, Department of Biochemistry, Federal University of Santa Catarina, Florianópolis, SC, Brazil
6 Laboratory of Experimental Biochemistry, Department of Biochemistry, Federal University of Santa Catarina, Florianópolis, SC, Brazil
7 Faculty of Pharmaceutical Sciences, University of São Paulo, São Paulo-SP, Brazil
8 Department of Food Science and Technology, Facultad de Química, Universidad de la República, Montevideo, Uruguay
9 Laboratory of Lipids, Department of Clinical Analysis, Federal University of Santa Catarina, Florianópolis-SC, Brazil
10 Laboratory of Experimental Biochemistry, Department of Biochemistry, Federal University of Santa Catarina, Florianópolis, SC, Brazil
11 Laboratory of Fats and Oils, Department of Food Science and Technology, Federal University of Santa Catarina, Florianópolis, SC, Brazil
12 Laboratory of Lipid Research, Department of Family and Consumer Sciences, College of Agriculture and Environmental Sciences, North Carolina A & T State University, NC, USA
The aim of this study was to investigate the effects of different modified fats on the body weight, biochemical profile, and biomarkers of hepatic oxidative status in Balb- <i> c </i> mice. The animals were divided into four groups and fed for 75 days with a normolipidic (Control Group , CG) or hiperlipidic diets (40% kcal) containing a commercial interesterified fat (IFG) rich in palmitic acid (39%); a blend of non-interesterified fat (NIFG), with 2-fold less saturated fatty acids at the <i> sn </i> -2 position of triacylglycerols; or a partially hydrogenated vegetable oil ( PHFG), source of trans fatty acid (20%) and of linolenic acid (6%). The mice of the IFG and NIFG presented similar results in all evaluated parameters. The serum biochemical profile and hepatic oxidative stress markers in mice of the PHFG were similar to CG, except for total cholesterol (TC) which was significantly higher (p < 0.05) for the mice of th e PHFG. The mice feed with interesterified fat (IFG) showed serum TC (p < 0.01), non-HDL-C (p < 0.05), glucose (p < 0.05) and hepatic reduced glutathione values (2.7 fold, p < 0.05) and glutathione reductase activity (2.4 fold, p < 0.001) significantly higher when compared to the mice fed with partially hydrogenated vegetable oil (PHFG). The hydrogenated fat source of trans fatty acid (20%) had less important metabolic effects than fats containing amount s of palmitic acid (interesterified or non-interesterified). Our results suggest that the replacement of hydrogenated fats by interesterified fats may not be such a simple solution to reduce or eliminate <i> trans </i> fatty acids in foods.
Mensink, R.P., Sanders, T.A., Baer, D.J., Hayes, K.C., Howles, P.N. and Marangoni, A. (2016) The Increasing Use of Interesterified Lipids in the Food Supply and Their Effects on Health Parameters. Advances in Nutrition, 7, 719-729. https://doi.org/10.3945/an.115.009662
Mensink, R.P. and Katan, M.B. (1990) Effect of Dietary Trans Fatty Acids on High-Density and Low-Density Lipoprotein Cholesterol Levels in Healthy Subjects. The New England Journal of Medicine, 323, 439-445. https://doi.org/10.1056/NEJM199008163230703
Zock, P.L. and Mensink, R.P. (1996) Dietary Trans-Fatty Acids and Serum Lipoproteins in Humans. Current Opinion in Lipidology, 7, 34-37. https://doi.org/10.1097/00041433-199602000-00008
Itcho, K., Yoshii, Y., Ohno, H., Oki, K., Shinohara, M., Irino, Y., Toh, R., Ishida, T., Hirata, K.I. and Yoneda, M. (2017) Association between Serum Elaidic Acid Concentration and Insulin Resistance in Two Japanese Cohorts with Different Lifestyles. Journal of Atherosclerosis and Thrombosis, 24, 1206-1214. https://doi.org/10.5551/jat.39164
Liu, B., Sun, Y., Snetselaar, L.G., Sun, Q., Yang, Q., Zhang, Z., Liu, L., Hu, F.B. and Bao, W. (2018) Association between Plasma Trans-Fatty Acid Concentrations and Diabetes in a Nationally Representative Sample of US Adults. Journal of Diabetes, 10, 653-664. https://doi.org/10.1111/1753-0407.12652
Chajès, V., Thiébaut, A.C., Rotival, M., Gauthier, E., Maillard, V., Boutron-Ruault, et al. (2008) Association between Serum Trans-Monounsaturated Fatty Acids and Breast Cancer Risk in the E3N-EPIC Study. American Journal of Epidemiology, 167, 1312-1320. https://doi.org/10.1093/aje/kwn069
Hirko, K.A., Chai, B., Spiegelman, D., Campos, H., Farvid, M.S., Hankinson, S.E., et al. (2018) Erythrocyte Membrane Fatty Acids and Breast Cancer Risk: A Prospective Analysis in the Nurses’ Health Study II. International Journal of Cancer, 142, 1116-1129. https://doi.org/10.1002/ijc.31133
WHO World Health Organization (2018) Replace Trans Fat by 2023: An Action Package to Eliminate Industrially-Produced Trans Fat from the Global Food Supply. https://www.who.int/news/item/14-05-2018-who-plan-to-eliminate-industrially-produced-trans-fatty-acids-from-global-food-supply
Ghebreyesus, T.A. and Frieden, T.R. (2018) REPLACE: A Roadmap to Make the World Trans Fat Free by 2023. Lancet (London, England), 391, 1978-1980. https://doi.org/10.1016/S0140-6736(18)31083-3
Mills, C.E., Hall, W.L. and Berry, S. (2017) What Are Interesterified Fats and Should We Be Worried about Them in Our Diet? Nutrition Bulletin, 42, 153-158. https://doi.org/10.1111/nbu.12264
Berry, S.E. (2009) Triacylglycerol Structure and Interesterification of Palmitic and Stearic Acid-Rich Fats: An Overview and Implications for Cardiovascular Disease. Nutrition Research Reviews, 22, 3-17. https://doi.org/10.1017/S0954422409369267
Alfieri, A., Imperlini, E., Nigro, E., Vitucci, D., Orrù, S., Daniele, A., et al. (2017) Effects of Plant Oil Interesterified Triacylglycerols on Lipemia and Human Health. International Journal of Molecular Sciences, 19, 104. https://doi.org/10.3390/ijms19010104
Van Rooijen, M.A. and Mensink, R.P. (2020) Palmitic Acid versus Stearic Acid: Effects of Interesterification and Intakes on Cardiometabolic Risk Markers—A Systematic Review. Nutrients, 12, 615. https://doi.org/10.3390/nu12030615
Sundram, K., Karupaiah, T. and Hayes, K.C. (2007) Stearic Acid-Rich Interesterified Fat and Trans-Rich Fat Raise the LDL/HDL Ratio and Plasma Glucose Relative to Palm Olein in Humans. Nutrition & Metabolism, 4, 3. https://doi.org/10.1186/1743-7075-4-3
Sharma, M. and Lokesh, B.R. (2013) Modification of Serum and Tissue Lipids in Rats Fed with Blended and Interesterified Oils Containing Groundnut Oil with Linseed Oil. Journal of Food Biochemistry, 37, 220-230. https://doi.org/10.1111/j.1745-4514.2011.00627.x
Reena, M.B. and Lokesh, B.R. (2012) Effect of Blending and Lipase Catalyzed Interesterification Reaction on the Cholesterol Lowering Properties of Palm Oil with Rice Bran Oil in Rats. International Journal of Food Science and Technology, 47, 203-209. https://doi.org/10.1111/j.1365-2621.2011.02827.x
O’Fallon, J.V., Busboom, J.R., Nelson, M.L. and Gaskins, C.T. (2007) A Direct Method for Fatty Acid Methyl Ester Synthesis: Application to Wet Meat Tissues, Oils, and Feedstuffs. Journal of Animal Science, 85, 1511-1521. https://doi.org/10.2527/jas.2006-491
Vlahov, G. (1998) Regiospecific Analysis of Natural Mixtures of Triglycerides Using Quantitative 13C Nuclear Magnetic Resonance of Acyl Chain Carbonyl Carbons. Magnetic Resonance in Chemistry, 36, 359-362. https://doi.org/10.1002/(SICI)1097-458X(199805)36:5 3.0.CO;2-Z
Segura, N., Da Silva, R.C., Soares, F.A.S.M., Gioielli, L.A. and Jachmanián, I. (2011) Valorization of Beef Tallow by Lipase-Catalyzed Interesterification with High Oleic Sunflower Oil. JAOCS, Journal of the American Oil Chemists’ Society, 88, 1945-1954. https://doi.org/10.1007/s11746-011-1876-y
Gouk, S.W., Cheng, S.F., Ong, A.S. and Chuah, C.H. (2014) Stearic Acids at sn-1, 3 Positions of TAG Are More Efficient at Limiting Fat Deposition than Palmitic and Oleic Acids in C57BL/6 Mice. The British Journal of Nutrition, 111, 1174-1180. https://doi.org/10.1017/S0007114513003668
Bucolo, G. and David, H. (1973) Quantitative Determination of Serum Triglycerides by the Use of Enzymes. Clinical Chemistry, 19, 476-482. https://doi.org/10.1093/clinchem/19.5.476
Allain, C.C., Poon, L.S., Chan, C.S., Richmond, W. and Fu, P.C. (1974) Enzymatic Determination of Total Serum Cholesterol. Clinical Chemistry, 20, 470-475. https://doi.org/10.1093/clinchem/20.4.470
Sugiuchi, H., Uji, Y., Okabe, H., Irie, T., Uekama, K., Kayahara, N. and Miyauchi, K. (1995) Direct Measurement of High-Density Lipoprotein Cholesterol in Serum with Polyethylene Glycol-Modified Enzymes and Sulfated Alpha-Cyclodextrin. Clinical Chemistry, 41, 717-723. https://doi.org/10.1093/clinchem/41.5.717
Trinder, P. (1969) Determination of Blood Glucose Using an Oxidase-Peroxidase System with a Non-Carcinogenic Chromogen. Journal of Clinical Pathology, 22, 158-161. https://doi.org/10.1136/jcp.22.2.158
Rej, R. and Horder, M. (1983) Aspartate Aminotranspherase. In: Bergmeyer, H.U., Bergmeyer, J. and Grassl, M., Eds., Methods of Enzymatic Analysis, 3rd Edition, Verlag Chemie, Weinheim, 416-433.
Misra, H.P. and Fridovich, I. (1972) The Role of Superoxide Anion in the Autoxidation of Epinephrine and a Simple Assay for Superoxide Dismutase. The Journal of Biological Chemistry, 247, 3170-3175
Aebi, H. (1984) Catalase in Vitro. Methods in Enzymology, 105, 121-126. https://doi.org/10.1016/S0076-6879(84)05016-3
Flohé, L. and Günzler, W.A. (1984) Assays of Glutathione Peroxidase. Methods in Enzymology, 105, 114-121. https://doi.org/10.1016/S0076-6879(84)05015-1
Carlberg, I. and Mannervik, B. (1985) Glutathione Reductase. Methods in Enzymology, 113, 484-490. https://doi.org/10.1016/S0076-6879(85)13062-4
Beutler, E., Duron, O. and Kelly, B.M. (1963) Improved Method for the Determination of Blood Glutathione. The Journal of Laboratory and Clinical Medicine, 61, 882-888.
Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. (1951) Protein Measurement with the Folin Phenol Reagent. The Journal of Biological Chemistry, 193, 265-275.
Bird, R.P. and Draper, H.H. (1984) Comparative Studies on Different Methods of Malonaldehyde Determination. Methods in Enzymology, 105, 299-305. https://doi.org/10.1016/S0076-6879(84)05038-2
Levine, R.L., Garland, D., Oliver, C.N., Amici, A., Climent, I., Lenz, A.G., et al. (1990) Determination of Carbonyl Content in Oxidatively Modified Proteins. Methods in Enzymology, 186, 464-478. https://doi.org/10.1016/0076-6879(90)86141-H
AOAC Association of Official Analytical Chemists (1999) Physical and Chemical Characteristics of Oils, Fats, and Waxes. US FDA, Washington DC.
Soares, F.A.Z.D., Silva, R.C., Silva, K.C.G., Lourenço, M.B., Soares, D.F. and Gioielli, L.A. (2009) Effects of Chemical Interesterification on Physicochemical Properties of Blends of Palm Stearin and Palm Olein. Food Research International, 42, 1287-1294. https://doi.org/10.1016/j.foodres.2009.03.022
Costales, R. and Fernández, A. (2009) Hidrogenación e Interesterificación. In: Block, J. and Barrera-Arellano, D., Eds., Temas Selectos en Aceites y Grasas, Edgard Blucher, São Paulo.
Mozaffarian, D. and Stampfer, M.J. (2010) Removing Industrial Trans Fat from Foods. BMJ (Clinical Research ed.), 340, c1826. https://doi.org/10.1136/bmj.c1826
Nishikawa, S., Sugimoto, J., Okada, M., Sakairi, T. and Takagi, S. (2012) Gene Expression in Livers of BALB/C and C57BL/6J Mice Fed a High-Fat Diet. Toxicologic Pathology, 40, 71-82. https://doi.org/10.1177/0192623311422078
Gouk, S.W., Cheng, S.F., Mok, J.S., Ong, A.S. and Chuah, C.H. (2013) Long-Chain SFA at the sn-1,3 Positions of TAG Reduce Body Fat Deposition in C57BL/6 Mice. The British Journal of Nutrition, 110, 1987-1995. https://doi.org/10.1017/S0007114513001475
Afonso, M.S., Lavrador, M.S., Koike, M.K., Cintra, D.E., Ferreira, F.D., Nunes, V.S., et al. (2016) Dietary Interesterified Fat Enriched with Palmitic Acid Induces Atherosclerosis by Impairing Macrophage Cholesterol Efflux and Eliciting Inflammation. The Journal of Nutritional Biochemistry, 32, 91-100. https://doi.org/10.1016/j.jnutbio.2016.01.005
Lavrador, M., Afonso, M.S., Cintra, D.E., Koike, M., Nunes, V.S., Demasi, M., et al. (2019) Interesterified Fats Induce Deleterious Effects on Adipose Tissue and Liver in LDLr-KO Mice. Nutrients, 11, 466. https://doi.org/10.3390/nu11020466
Magri, T.P., Fernandes, F.S., Souza, A.S., Langhi, L.G., Barboza, T., Misan, V., Mucci, et al. (2015) Interesterified Fat or Palm Oil as Substitutes for Partially Hydrogenated Fat in Maternal Diet Can Predispose Obesity in Adult Male Offspring. Clinical Nutrition (Edinburgh, Scotland), 34, 904-910. https://doi.org/10.1016/j.clnu.2014.09.014
De Velasco, P., Fernandes, F., Mucci, D., Santos, R., Magri, T., Misan, V. and Tavares do Carmo, M.d.G. (2015) Interesterified Fat or Palm Oil as Substitutes for Trans Fat in Maternal Diet Can Predispose Obesity and Inflammation in Adult Male Offspring. The FASEB Journal, 29, 754.
Bispo, K.P., de Oliveira Rodrigues, L., da Silva Soares de Souza, é., Mucci, D., Tavares do Carmo, M.d., de Albuquerque, K.T. and de Carvalho Sardinha, F.L. (2015) Trans and Interesterified Fat and Palm Oil during the Pregnancy and Lactation Period Inhibit the Central Anorexigenic Action of Insulin in Adult Male Rat Offspring. The Journal of Physiological Sciences, 65, 131-138. https://doi.org/10.1007/s12576-014-0351-6
Ponnampalam, E.N., Lewandowski, P., Nesaratnam, K., Dunshea, F.R. and Gill, H. (2011) Differential Effects of Natural Palm Oil, Chemically- and Enzymatically-Modified Palm Oil on Weight Gain, Blood Lipid Metabolites and Fat Deposition in a Pediatric Pig Model. Nutrition Journal, 10, 53. https://doi.org/10.1186/1475-2891-10-53
Reena, M.B. and Lokesh, B.R. (2007) Hypolipidemic Effect of Oils with Balanced Amounts of Fatty Acids Obtained by Blending and Interesterification of Coconut Oil with Rice Bran Oil or Sesame Oil. Journal of Agricultural and Food Chemistry, 55, 10461-10469. https://doi.org/10.1021/jf0718042
Nagaraju, A. and Lokesh, B.R. (2007) Interesterified Coconut Oil Blends with Groundnut Oil or Olive Oil Exhibit Greater Hypocholesterolemic Effects Compared with Their Respective Physical Blends in Rats. Nutrition Research, 27, 580-586. https://doi.org/10.1016/j.nutres.2007.06.007
Reena, M.B., Gowda, L.R. and Lokesh, B.R. (2011) Enhanced Hypocholesterolemic Effects of Interesterified Oils Are Mediated by Upregulating LDL Receptor and Cholesterol 7-α-Hydroxylase Gene Expression in Rats. The Journal of Nutrition, 141, 24-30. https://doi.org/10.3945/jn.110.127027
Blaha, M.J., Blumenthal, R.S., Brinton, E.A., Jacobson, T.A. and National Lipid Association Taskforce on Non-HDL Cholesterol (2008) The Importance of non-HDL Cholesterol Reporting in Lipid Management. Journal of Clinical Lipidology, 2, 267-273. https://doi.org/10.1016/j.jacl.2008.06.013
Mensink, R.P., Zock, P.L., Kester, A.D. and Katan, M.B. (2003) Effects of Dietary Fatty Acids and Carbohydrates on the Ratio of Serum Total to HDL Cholesterol and on Serum Lipids and Apolipoproteins: A Meta-Analysis of 60 Controlled Trials. The American Journal of Clinical Nutrition, 77, 1146-1155. https://doi.org/10.1093/ajcn/77.5.1146
Sun, Y., Neelakantan, N., Wu, Y., Lote-Oke, R., Pan, A. and van Dam, R.M. (2015) Palm Oil Consumption Increases LDL Cholesterol Compared with Vegetable Oils Low in Saturated Fat in a Meta-Analysis of Clinical Trials. The Journal of Nutrition, 145, 1549-1558. https://doi.org/10.3945/jn.115.210575
Rodriguez-Leyva, D., Dupasquier, C.M., McCullough, R. and Pierce, G.N. (2010) The Cardiovascular Effects of Flaxseed and Its Omega-3 Fatty Acid, Alpha-Linolenic Acid. The Canadian Journal of Cardiology, 26, 489-496. https://doi.org/10.1016/S0828-282X(10)70455-4
Filippou, A., Teng, K.-T., Berry, S.E. and Sanders, T.A.B. (2014) Palmitic Acid in the sn-2 Position of Dietary Triacylglycerols Does Not Affect Insulin Secretion or Glucose Homeostasis in Healthy Men and Women. European Journal of Clinical Nutrition, 68, 1036-1041. https://doi.org/10.1038/ejcn.2014.141
Miyamoto, J.é., Ferraz, A.C.G., Portovedo, M., Reginato, A., Stahl, M.A., Ignacio-Souza, L.M., et al (2018) Interesterified Soybean Oil Promotes Weight Gain, Impaired Glucose Tolerance and Increased Liver Cellular Stress Markers. The Journal of Nutritional Biochemistry, 59, 153-159. https://doi.org/10.1016/j.jnutbio.2018.05.014
Masarone, M., Rosato, V., Dallio, M., Gravina, A.G., Aglitti, A., Loguercio, C., et al (2018) Role of Oxidative Stress in Pathophysiology of Nonalcoholic Fatty Liver Disease. Oxidative Medicine and Cellular Longevity, 2018, Article ID: 9547613. https://doi.org/10.1155/2018/9547613
Monguchi, T., Hara, T., Hasokawa, M., Nakajima, H., Mori, K., Toh, R., Irino, Y., Ishida, T., Hirata, K.I. and Shinohara, M. (2017) Excessive Intake of Trans Fatty Acid Accelerates Atherosclerosis through Promoting Inflammation and Oxidative Stress in a Mouse Model of Hyperlipidemia. Journal of Cardiology, 70, 121-127. https://doi.org/10.1016/j.jjcc.2016.12.012
Dhibi, M., Brahmi, F., Mnari, A., Houas, Z., Chargui, I., Bchir, L., Gazzah, N., Alsaif, M.A. and Hammami, M. (2011) The Intake of High Fat Diet with Different Trans Fatty Acid Levels Differentially Induces Oxidative Stress and Non Alcoholic Fatty Liver Disease (NAFLD) in Rats. Nutrition and Metabolism, 8, 65. https://doi.org/10.1186/1743-7075-8-65
Zhang, Y., Yang, X., Shi, H., Dong, L. and Bai, J. (2011) Effect of α-Linolenic Acid on Endoplasmic Reticulum Stress-Mediated Apoptosis of Palmitic Acid Lipotoxicity in Primary Rat Hepatocytes. Lipids in Health and Disease, 10, 122. https://doi.org/10.1186/1476-511X-10-122
Guo, W., Wong, S., Xie, W., Lei, T. and Luo, Z. (2007) Palmitate Modulates Intracellular Signaling, Induces Endoplasmic Reticulum Stress, and Causes Apoptosis in Mouse 3T3-L1 and Rat Primary Preadipocytes. American Journal of Physiology. Endocrinology and Metabolism, 293, E576-E586. https://doi.org/10.1152/ajpendo.00523.2006
Yao, J.K., Leonard, S. and Reddy, R. (2006) Altered Glutathione Redox State in Schizophrenia. Disease Markers, 22, 83-93. https://doi.org/10.1155/2006/248387
Pettersson, U.S., Waldén, T.B., Carlsson, P.O., Jansson, L. and Phillipson, M. (2012) Female Mice Are Protected against High-Fat Diet Induced Metabolic Syndrome and Increase the Regulatory T Cell Population in Adipose Tissue. PLoS One, 7, e46057. https://doi.org/10.1371/journal.pone.0046057