Effect of Linseed Oil Supplementation on Lipid Peroxidation and Antioxidant Capacity in Pregnant Overfed Obese Rats and Their Offspring

Abstract

The aim of the present study was to evaluate the protective effects of linseed oil on lipid peroxidation, antioxidative capacity, as well as serum glucose, total cholesterol (TC), LDL-C and TG levels, in cafeteria-diet-fed dams during gestation and lactation, and in their offspring throughout adulthood. Food and energy intakes were also evaluated. The cafeteria diet led to higher energy intake, body weight, hyperglycemia and hyperlipidemia (higher TC, LDL-C and TG) in dams’ rats and their pups. Plasma vitamin C, Erythrocyte GSH levels and catalase activity were lower, whereas plasma diene conjugates (DC), Malondialdehyde and protein carbonyl levels (PC) in plasma and erythrocytes were higher in cafeteria-diet-fed mothers and their pups compared to controls. Supplement of linseed oil significantly enhanced plasma antioxidant defense capacities, as evaluated by the marked increase in the levels of plasma vitamin C and erythrocyte GSH as well as the activities of CAT and the significant reduction in lipid peroxidation (lower DC and MDA) and PC in CAFL-diet-fed mothers and their offspring. Simultaneous intake of linseed oil also reduced body weight, plasma TG, TC and LDL-C contents in obese pregnant and lactating dams and their pups at day 30 and day 90. The flaxseed oil supplementation may prevent lipid peroxidation and metabolic disorders which might be helpful in preventing obesity complications in mothers during pregnancy and lactation and in their offspring.

REFERENCES:
Adeoye, O., Olawumi, J., Opeyemi, A., & Christiania, O. (2016). Review on the role of
glutathione on oxidative stress and infertility. JBRA Assisted Reproduction, 22(1), 61-
66.
Aebi, H. (1974). Catalase. In Methods of Enzymatic Analysis, 2nd edn, vol. 2 (Bergmeyer, H.
U., ed.), pp. 673–684, Verlag Chemie, Weinheim
Ambrozova, G., Pekarova, M., & Lojek, A. (2010). Effect of polyunsaturated fatty acids on
the reactive oxygen and nitrogen species production by raw 264.7 macrophages.
European Journal of Nutrition, 49,133–139.
Ayad, A., Merzouk, H., Merzouk, S.A., & Narce, M. (2013). Blood Oxidant/Antioxidant
Status in overfed Aging Rats: Comparative Effects of Sunflower and Olive-Linseed
Mixture Oil Rich Diets. Biomedical and Environmental Sciences, 9, 765–768
Benkalfat, N.B, Merzouk, H., Bouanane, S., Merzouk, S.A., Bellenger, J., Gresti, J., Tessie,
C., & Narce, M. (2011). Altered adipose tissue metabolism in offspring of dietary obese
rat dams. Clinical Science, 121, 19–28.
Bouanane, S., Benkalfat, N.B., Baba Ahmed, F.Z., Merzouk, H., Soulimane Mokhtari, N.,
Merzouk, S., Gresti, J., Tessier, C., & Narce M. (2009). Time course of changes in serum oxidant/antioxidant status in overfed obese rats and their offspring. Clinical
Science, 116, 669–680.
Bradlee, M.L, Singer, M.R, Qureshi, M.M, & Moore, L.L. (2010). Food group intake and
central obesity among children and adolescents in the Third National Health and
Nutrition Examination Survey (NHANES III). Public Health Nutrition, 22, 1–9.
Cetin, I., Alvino, G., & Cardellicchio, M. (2009). Long chain fatty acids and dietary fats in
fetal nutrition. Journal of Physiology, 14, 3441–3451.
Catalano, PM., & Shankar, K. (2017). Obesity and pregnancy: Mechanisms of short term and
long term adverse consequences of mother and child. British Medical Journal, 8, 356.
D’Archivio, M., Annuzzi, G., Varì, R., Filesi, C., Giacco, R., Scazzocchio, B., Santangelo, C.,
Giovannini, C., Rivellese, A.A., & Masella, R. (2012). Predominant role of
obesity/insulin resistance in oxidative stress development. European Journal of
Clinical Investigation, 42, 70–78.
Denisenko, Y.K., & Novgorodtseva, T.P. (2013). Effect of Prolonged High-Fat Diet on
Thiol-Disulfide Homeostasis in Rats. International Journal of BioMedicine, 3, 197–
200.
Duttaroy, A.K. (2009). Transport of fatty acids across the human placenta. Progress in Lipid
Research, 48, 52–61.
Falcone, V., Stopp, T., Feichtinger, M ., Kiss,H., Eppel,W., Husslein,PW., Prager,G., & Göbl,
CS. (2018). Pregnancy after bariatric surgery: a narrative literature review and
discussion of impact on pregnancy management and outcome. BMC Pregnancy
Childbirth, 18, 507.
Fang, Y.Z., Yang, S., & Wu, G. (2002). Free radicals, antioxidants, and nutrition.
Nutrition,18, 872– 879.
Galtier-Dereure, F., Boegner, C., & Bringer J. (2000). Obesity and pregnancy: complications
and cost. American Journal of Clinical Nutrition, 71, 1242–1248
Goutzourelas, N., Orfanou, M., Charizanis, I., Leon, G., Spandidos, DA., Kouretas, D. (2018).
GSH levels affect weight loss in individuals with metabolic syndrome and obesity
following dietary therapy. Experimental and Therapeutic Medicine, 16(2), 635-642.
Haggarty, P. (2002). Placental regulation of fatty acid delivery and its effect on fetal Growth
- a review. Placenta, 23, 28–38.
Havel, R.J, Eder, H.A., & Bragdon, J.H. (1955). The distribution and chemical composition
of ultra centrifugally separated lipoproteins in human serum. Journal of Clinical
Investigation, 34, 1345–1353
Khan, N.I, Naz, L., & Yasmeen, G. (2006). Obesity: an independent risk factor for systemic
oxidative stress. Pakistan Journal of Pharmaceutical Sciences, 19, 62–65
Laissouf, A., Mokhtari-Soulimane, N., Merzouk, H., & Benhabib, N. (2013). Dietary flaxseed
oil supplementation improves the oxidant/antioxidant status in obese aged rats.
International Journal of Medicine and Pharmaceutical Sciences, 2, 87–94.
Levine, R.L, Garland, D., Oliver, C.N., Amici, A., Climent, I., Lenz, A.G., Ahn, B.W.,
Shaltiel, S., & Stadtman, E.R. (1990). Determination of carbonyl content in oxidatively
modified proteins. Methods in Enzymology, 186, 464–478
Jones, M.L., Mark, P.J., Mori, T.A., & Keelan, J.A., Waddell, B.J. (2013). Maternal dietary
omega-3 fatty acid supplementation reduces placental oxidative stress and increases
fetal and placental growth in the rat. Biology of Reproduction, 88 (2):1–8.
Meghelli-Bouchenak, M., Boquillon, M., & Belleville., J. (1989). Serum lipoprotein
composition and amounts during the consumption of two different low protein diets
followed by a balanced diet. Nutrition Reports International, 39, 323–34.
Moll, U., Olsson, H., & Landin-Olsson, M. (2017). Impact of Pregestational Weight and
Weight Gain during Pregnancy on Long-Term Risk for Diseases. PLOS One, 3, 12(1).

Ohkawa, H., Ohishi, N., & Yagi, K. (1979). Assay for lipid peroxides in animal tissues by
thiobarbituric acid reaction. Analytical Biochemistry, 95, 351–351.
Oken, E., Ning, Y., Rifas-Shiman, S.L., Rich-Edwards, J.W., Olsen, S.F., & Gillman, M.W.
(2007). Diet during pregnancy and risk of preeclampsia or gestational hypertension.
Annals of Epidemiology, 17, 663-668.
Rasmy, G.E. (2007). Protective effect of linseed oil on hyperlipidemia in experimental
animals. Journal of Genetic Engineering and Biotechnology, 5, 9–17.
Redgrave, T.G, Robert, D.C.K, & West, C.E. (1975). Separation of plasma lipoproteins by
density-gradient ultracentrifugation. Analytical Biochemistry, 65, 42–49
Rezaei, A., & Heidarian, E. (2013). Co-administration of trientine and flaxseed oil on
oxidative stress, serum lipids and heart structure in diabetic rats. Indian Journal of
Experimental Biology, 51,646–652.
Roe, J.H, & Kuether, C.A. (1943). The determination of ascorbic acid in whole blood and
urine through the 2,4- dinitrophenylhydrazine derivatives of dehydroascorbic acid.
Journal of Biological Chemistry,14, 399–407.
Ross, S.R., Lexin, W., & Herbert, J. (2007). Erythrocyte Oxidative Damage in Chronic
Fatigue Syndrome. Archives of Medical Research, 38, 94–98.
Savini, I., Catani, M.V., Evangelista, D., Gasperi, V., & Avigliano, L. (2013). ObesityAssociated Oxidative Stress: Strategies Finalized to Improve Redox State. International
Journal of Molecular Sciences, 14, 10497–10538.
Sen, S., & Simmons, R.A. (2010). Maternal Antioxidant Supplementation Prevents Adiposity
in the Offspring of Western Diet–Fed Rats. Diabetes, 59, 3058–3065.
Simko, M., Totka, A., Vondrova, D., Samohyl, M., Jurkovicova, J., Trnka, M., Cibulkova, A.,
Stofko, J., & Argalasova, L. (2019). Maternal Body Mass Index and Gestational Weight
Gain and Their Association with Pregnancy Complications and Perinatal Conditions.
International Journal of Environmental Research and Public Health,16 (10), 1751.
Song, J.H., Fujimoto, K., & Miyazawa, T. (2000). Polyunsaturated (n-3) Fatty Acids
Susceptible to Peroxidation Are Increased in Plasma and Tissue Lipids of Rats Fed
Docosahexaenoic Acid Containing Oils. Journal of Nutrition, 130, 3028–3033.
Tang, Z., Ying, R.F., Lv, B.F., Yang, L.H., Xu, Z., Yan, L.Q ., Bu, J.Z., & Wei, Y.S. (2021).
Flaxseed oil: Extraction, Health benefits and products. Quality Assurance and Safety of
Crops & Foods, 13(1), 1-19.
Tran, B., Oliver, S., Rosa, J., & Galassetti, P. (2012). Aspects of inflammation and oxidative
stress in pediatric obesity and type 1 diabetes: An overview of ten years of studies.
Experimental Diabetes Research, 683–680.
Vincent, H.K., & Taylor, A.G. (2006). Biomarkers and potential mechanisms of obesityinduced oxidant stress in humans. International Journal of Obesity, 30,400–418
Whitaker, R.C. (2004) Predicting preschooler obesity at birth: the role of maternal obesity in
early pregnancy. Pediatrics, 114, 29–36
Xu, J., Gao, H., Song, L., Yang, W., Chen, C., Deng, Q., Huang, Q., Yang, J., & Huang, F.
(2013). Flaxseed oil and alpha-lipoic acid combination ameliorates hepatic oxidative
stress and lipid accumulation in comparison to lard. Lipids in Health and Disease,12, 58
1–7
Xu, J., Yang, W., Deng, Q., Huang, Q., Yang, J, & Huang, F. (2012). Flaxseed oil and αlipoic acid combination reduces atherosclerosis risk factors in rats fed a high-fat diet.
Lipids in Health and Disease, 11,148–155
Yagi, K. (1987). Lipid peroxides and human diseases. chemistry physics lipids, 45, 337–51.
Yanes, O., Clark, J., Wong, D.M., Patti, G.J., Sanchez-Ruiz, A., Benton, H.P.0, Trauger, S.A.,
Desponts, C., Ding, S., & Siuzdak, G. (2010) Metabolic oxidation regulates embryonic
stem cell differentiation. Nature Chemical Biology, 6, 411–41

Yang, W., Fu, J., Yu, M., Huang, Q., Wang, D., Xu, J., Deng, Q., Yao, P., Huang, F., & Liu,
L. (2012). Effects of flaxseed oil on anti-oxidative system and membrane deformation
of human peripheral blood erythrocytes in high glucose level. Lipids in Health and
Disease, 11, 88.
Yessoufou, A., Soulimane, N., Merzouk, S., Moutairou, K., Ahissou, H., Prost, J., Simonin,
AM., Merzouk, H., Hichami, A., & Khan, N.A. (2006). N-3 Fatty acids modulate
antioxidant status in diabetic rats and their macrosomic offspring. International Journal
of Obesity, 30, 739–750.