DOI QR코드

DOI QR Code

Antioxidant Effects of Spinach (Spinacia oleracea L.) Supplementation in Hyperlipidemic Rats

  • Ko, Sang-Heui (Department of Food and Nutrition, Sunchon National University) ;
  • Park, Jae-Hee (Department of Food and Nutritional Science, Kyungnam University) ;
  • Kim, So-Yun (Department of Food and Nutritional Science, Kyungnam University) ;
  • Lee, Seon Woo (Department of Food and Nutritional Science, Kyungnam University) ;
  • Chun, Soon-Sil (Department of Food and Nutrition, Sunchon National University) ;
  • Park, Eunju (Department of Food and Nutritional Science, Kyungnam University)
  • Received : 2014.03.13
  • Accepted : 2014.03.14
  • Published : 2014.03.31

Abstract

Increased consumption of fresh vegetables that are high in polyphenols has been associated with a reduced risk of oxidative stress-induced disease. The present study aimed to evaluate the antioxidant effects of spinach in vitro and in vivo in hyperlipidemic rats. For measurement of in vitro antioxidant activity, spinach was subjected to hot water extraction (WE) or ethanol extraction (EE) and examined for total polyphenol content (TPC), oxygen radical absorbance capacity (ORAC), cellular antioxidant activity (CAA), and antigenotoxic activity. The in vivo antioxidant activity of spinach was assessed using blood and liver lipid profiles and antioxidant status in rats fed a high fat-cholesterol diet (HFCD) for 6 weeks. The TPC of WE and EE were shown as $1.5{\pm}0.0$ and $0.5{\pm}0.0mg$ GAE/g, respectively. Increasing the concentration of the extracts resulted in increased ORAC value, CAA, and antigenotoxic activity for all extracts tested. HFCD-fed rats displayed hyperlipidemia and increased oxidative stress, as indicated by a significant rise in blood and liver lipid profiles, an increase in plasma conjugated diene concentration, an increase in liver thiobarbituric acid reactive substances (TBARS) level, and a significant decrease in manganese superoxide dismutase (Mn-SOD) activity compared with rats fed normal diet. However, administration of 5% spinach showed a beneficial effect in HFCD rats, as indicated by decreased liver TBARS level and DNA damage in leukocyte and increased plasma conjugated dienes and Mn-SOD activity. Thus, the antioxidant activity of spinach may be an effective way to ameliorate high fat and cholesterol diet-induced oxidative stress.

References

  1. Singh PN, McCoy MT, Tice RR, Schneider EL. 1988. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175: 184-191. https://doi.org/10.1016/0014-4827(88)90265-0
  2. Lomnitski L, Carbonatto M, Ben-Shaul V, Peano S, Conz A, Corradin L, Maronpot RR, Grossman S, Nyska A. 2000. The prophylactic effects of natural water-soluble antioxidant from spinach and apocynin in a rat model of lipopolysaccharide-induced endotoxemia. Toxicol Pathol 28: 588-600. https://doi.org/10.1177/019262330002800413
  3. Park JH, Kim RY, Park E. 2011. Antioxidant and $\alpha$-glucosidase inhibitory activities of different solvent extracts of skullcap (Scuellaria baicalensis). Food Sci Biotechnol 20: 1107-1112. https://doi.org/10.1007/s10068-011-0150-2
  4. Park JH, Seo BY, Lee KH, Park E. 2009. Onion supplementation inhibits lipid peroxidation and leukocyte DNA damage due to oxidative stress in high fat-cholesterol fed male rats. Food Sci Biotechnol 18: 179-184.
  5. Friedewald WT, Levey RI, Fredrickson DS. 1972. Estimation of the concentration of low-density lipoprotein cholesterol plasma, without use of the preparative ultracentrifuge. Clin Chem 18: 499-502.
  6. Zhu L, Luo X, Jin Z. 2008. Effect of resveratrol on serum and liver lipid profile and antioxidant activity in hyperlipidemia rats. Asian-Aust J Anim Sci 21: 890-895. https://doi.org/10.5713/ajas.2008.70638
  7. Fu H, Xie B, Ma S, Zhu X, Fan G, Pan S. 2011. Evaluation of antioxidant activities of principal carotenoids available in water spinach (Ipomoea aquatica). J Food Compos Anal 24:288-297. https://doi.org/10.1016/j.jfca.2010.08.007
  8. Bergman M, Parelman A, Dubinsky Z, Grossman S. 2003. Scavenging of reactive oxygen species by a novel glucurinated flavonoid antioxidant isolated and purified from spinach. Phytochemistry 62: 753-762. https://doi.org/10.1016/S0031-9422(02)00537-X
  9. Xu J, Zhou X, Deng Q, Huang Q, Yang J, Huang F. 2011. Rapeseed oil fortified with micronutrients reduces atherosclerosis risk factors in rats fed a high-fat diet. Lipids Health Disease 10: 96-103. https://doi.org/10.1186/1476-511X-10-96
  10. Aritomi M, Kawasaki T. 1984. Three highly oxygenated flavone glucuronides in leaves of Spinacia oleracea. Phytochemistry 23:2043-2047. https://doi.org/10.1016/S0031-9422(00)84967-5
  11. Gil MI, Ferreres F, Tomas-Barberan FA. 1999. Effect of postharvest storage and processing on the antioxidant constituents (flavonoids and vitamin C) of fresh-cut spinach. J Agric Food Chem 47: 2213-2217. https://doi.org/10.1021/jf981200l
  12. Edenharder R, Keller G, Platt KL, Unger KK. 2001. Isolation and characterization of structurally novel antimutagenic flavonoids from spinach (Spinacia oleracea). J Agric Food Chem 49: 2767-2773. https://doi.org/10.1021/jf0013712
  13. Ma M, Liu GH, Yu ZH, Chen G, Zhang X. 2009. Effect of the Lycium barbarum polysaccharides administration on blood lipid metabolism and oxidative stress of mice fed high-fat diet in vivo. Food Chem 113: 872-877. https://doi.org/10.1016/j.foodchem.2008.03.064
  14. Korean Statistical Information Service. Analysis on the actual conditions of deaths. http://kosis.kr/wnsearch/totalSearch.jsp(accessed September 2010).
  15. Chen X, Zhong HY, Zeng JH, Ge J. 2008. The pharmacological effect of polysaccharides from Lentinus edodes on the oxidative status and expression of VCAM-1mRNA of thoracic aorta endothelial cell in high-fat-diet rats. Carbohyd Polym 74: 445-450. https://doi.org/10.1016/j.carbpol.2008.03.018
  16. Lieber CS, Leo MA, Cao Q, Mak KM, Ren CL, Ponomarenko A. 2007. The combination of S-adenosylmethionine and dilinoleoylphosphatidylcholine attenuates nonalcoholic steatohepatitis produced by a high-fat diet in rats. Nutr Res 27:565-573. https://doi.org/10.1016/j.nutres.2007.07.005
  17. Schreibelt G, van Horssen J, van Rossum S, Dijkstra CD, Drukarch B, de Vries HE. 2007. Therapeutic potential and biological role of endogenous antioxidant enzymes in multiple sclerosis pathology. Brain Res Rev 56: 322-330. https://doi.org/10.1016/j.brainresrev.2007.07.005
  18. Hait-Darshan R, Grossman S, Bergman M, Deutsch M, Zurgil N. 2009. Synergistic activity between a spinachderived natural antioxidant (NAO) and commercial antioxidants in a variety of oxidation system. Food Res Int 42:246-253. https://doi.org/10.1016/j.foodres.2008.11.006
  19. Yoneda T, Inagaki S, Hayashi Y, Nomura T, Takagi H. 1992. Differential regulation of manganese and copper/zinc superoxide dismutases by the facial nerve transection. Brain Res 582: 342-345. https://doi.org/10.1016/0006-8993(92)90153-Z
  20. Moron MS, Dipierre JW, Mannervik B. 1979. Levels of glutathione reductase and glutathione-S-transferase activities in rat lung and liver. Biochim Biophys Acta 582: 67-68. https://doi.org/10.1016/0304-4165(79)90289-7
  21. Qi X, Guy J, Nick H, Valentine J, Rao N. 1997. Increase of manganese superoxide dismutase, but not of Cu/Zn-SOD, in experimental optic neuritis proinvestigative. Invest Ophthalmol Visual Sci 38: 1203-1212.
  22. Bergeron C, Petrunka C, Weyer L. 1996. Copper/zinc superoxide dismutase expression in the human central nervous system. Correlation with selective neuronal vulnerability. Am J Pathol 148: 273-279.
  23. Oliveira PS, Saccon TD, da Silva TM, Costa MZ, Dutra FS, de Vasconcelos A, Lencina CL, Stefanello FM, Barschak AG. 2013. Green juice as a protector against reactive species in rats. Nutr Hosp 28: 1407-1412.
  24. Verma AR, Vijayakumar M, Rao CV, Mathela CS. 2010. In vitro and in vivo antioxidant properties and DNA damage protective activity of green fruit of Ficus glomerata. Food Chem Toxicol 48: 704-709. https://doi.org/10.1016/j.fct.2009.11.052
  25. Kim MY, Cheong SH, Kim MH, Son C, Yook HS, Sok DE, Kim JH, Cho Y, Chun H, Kim MR. 2009. Leafy vegetable mix supplementation improves lipid profiles and antioxidant status in C57BL/6J mice fed a high fat and high cholesterol diet. J Med Food 12: 877-884. https://doi.org/10.1089/jmf.2008.1125
  26. Rice-Evans CA, Miller NJ, Paganga G. 1996. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med 20: 933-956. https://doi.org/10.1016/0891-5849(95)02227-9
  27. Nyska A, Lomnitski L, Spalding J, Dunson DB, Goldsworthy TL, Grossman S, Bergman M, Boorman G. 2001. Topical and oral administration of the natural water-soluble antioxidant from spinach reduces the multiplicity of papillomas in the Tg.AC mouse model. Toxicol Lett 122: 33-44. https://doi.org/10.1016/S0378-4274(01)00345-9
  28. Zhu L, Luo X, Jin Z. 2008. Effect of resveratrol on serum and liver lipid profile and antioxidant activity in hyperlipidemia rats. Asian-Aust J Anim Sci 21: 890-895. https://doi.org/10.5713/ajas.2008.70638
  29. Dreosti IE. 2000. Antioxidant polyphenols in tea, cocoa, and wine. Nutr 16: 692-701. https://doi.org/10.1016/S0899-9007(00)00304-X
  30. Cieslik E, Gręda A, Adamus W. 2006. Contents of polyphenols in fruit and vegetables. Food Chem 94: 135-142. https://doi.org/10.1016/j.foodchem.2004.11.015
  31. Trajkovic LMH, Mijatovic SA, Maksimovic-Ivanic DD, Stojanovic ID, Momcilovic MB, Tufegdzic SJ, Maksimovic VM, Marjanovi ZS, Stosic-Grujicic SD. 2009. Anticancer properties of Ganoderma lucidum methanol extracts in vitro and in vivo. Nutr Cancer 61: 696-707. https://doi.org/10.1080/01635580902898743
  32. Lee HS, Won NH, Kim KH, Lee H, Jun W, Lee KW. 2005. Antioxidant effects of aqueous extract of Terminalia chebula in vivo and in vitro. Biol Pharm Bull 28: 1639-1644. https://doi.org/10.1248/bpb.28.1639
  33. Celep E, Aydın A, Kırmızıbekmez H, Yesilada E. 2013. Appraisal of in vitro and in vivo antioxidant activity potential of cornelian cherry leaves. Food Chem Toxicol 11: 448-455.
  34. Lee LS, Cho CW, Hong HD, Lee YC, Choi UK, Kim YC. 2013. Hypolipidemic and antioxidant properties of phenolic compound-rich extracts from white ginseng (Panax ginseng) in cholesterol-fed rabbits. Molecules 18: 12548-12560. https://doi.org/10.3390/molecules181012548
  35. Kang SY, Kim SH, Schini VB, Kim ND. 1995. Dietary ginsenosides improve endothelium-dependent relaxation in the thoracic arota of hypercholesterolemic rabbit. Gen Pharmac 26: 483-487. https://doi.org/10.1016/0306-3623(95)94002-X
  36. Bogdanska JJ, Korneti P, Todorova B. 2003. Erythrocyte superoxide dismutase, glutathione peroxidase and catalase activities in healthy male subjects in Republic of Macedonia. Bratisl Lek Listy 104: 108-114.
  37. Folch J, Lees M, Sloan-Stanley GH. 1956. A simple method for isolation and purification of total lipids from animal tissues. J Biol Chem 226: 497-509.
  38. Buege JA, Aust SD. 1978. Microsomal lipid peroxidation. Methods Enzymol 52: 302-310. https://doi.org/10.1016/S0076-6879(78)52032-6
  39. Ohkawa H, Ohishi N, Yagi K. 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95: 351-358. https://doi.org/10.1016/0003-2697(79)90738-3
  40. Carrillo MC, Kanai S, Nokubo M, Kitani K. 1991. (-) deprenyl induces activities of both superoxide dismutase and catalase but not of glutathione peroxides in the striatum of young male rats. Life Sci 48: 517-521. https://doi.org/10.1016/0024-3205(91)90466-O
  41. Bunea A, Andjelkovic M, Socaciu C, Bobis O, Neacsu M, Verhe R, Camp JV, Bunea A, Andjelkovic M, Socaciu C, Bobis O. 2008. Total and individual carotenoids and phenolic acids content in fresh, refrigerated and processed spinach (Spinacia oleracea L.). Food Chem 108: 649-656. https://doi.org/10.1016/j.foodchem.2007.11.056
  42. Lomnitski L, Foley J, Grossman S, Ben-Shaul V, Maronpot R, Moomaw C, Carbonatto M, Nyska A. 2000. Effects of apocynin and natural antioxidants from spinach on iNOS and COX-2 induction in LPS-induced hepatic injury in rat. Pharmacol Toxicol 87: 18-25.
  43. Lomnitski L, Nyska A, Ben-Shaul V, Maronpot RR, Haseman JK, Harrus TL, Bergman M, Grossman S. 2000. Effects of antioxidants apocynin and the natural water-soluble antioxidant from spinach on cellular damage induced by lipopolysaccaride in the rat. Toxicol Pathol 28: 580-587. https://doi.org/10.1177/019262330002800412

Cited by

  1. Effect of Spinach Extract on RANKL-Mediated Osteoclast Differentiation vol.44, pp.4, 2015, https://doi.org/10.3746/jkfn.2015.44.4.532
  2. Polyphenols and DNA Damage: A Mixed Blessing vol.8, pp.12, 2016, https://doi.org/10.3390/nu8120785
  3. Amelioration of Abnormalities Associated with the Metabolic Syndrome by Spinacia oleracea (Spinach) Consumption and Aerobic Exercise in Rats vol.2017, 2017, https://doi.org/10.1155/2017/2359389
  4. Glycolipids from spinach suppress LPS-induced vascular inflammation through eNOS and NK-κB signaling vol.91, 2017, https://doi.org/10.1016/j.biopha.2017.04.052
  5. Detection of cellular redox reactions and antioxidant activity assays vol.37, 2017, https://doi.org/10.1016/j.jff.2017.08.008
  6. Functional properties of spinach (Spinacia oleracea L.) phytochemicals and bioactives vol.7, pp.8, 2016, https://doi.org/10.1039/C6FO00051G
  7. Antioxidant Activity of Orange Flesh and Peel Extracted with Various Solvents vol.19, pp.4, 2014, https://doi.org/10.3746/pnf.2014.19.4.291
  8. Effect of a barley-vegetable soup on plasma carotenoids and biomarkers of cardiovascular disease vol.57, pp.1, 2015, https://doi.org/10.3164/jcbn.15-11
  9. Spinacia oleracea extract attenuates disease progression and sub-chondral bone changes in monosodium iodoacetate-induced osteoarthritis in rats vol.18, pp.1, 2018, https://doi.org/10.1186/s12906-018-2117-9
  10. -MS/MS techniques pp.1478-6427, 2018, https://doi.org/10.1080/14786419.2018.1489395
  11. Opposite Effects of the Spinach Food Matrix on Lutein Bioaccessibility and Intestinal Uptake Lead to Unchanged Bioavailability Compared to Pure Lutein vol.62, pp.11, 2018, https://doi.org/10.1002/mnfr.201800185
  12. The Essential Element Manganese, Oxidative Stress, and Metabolic Diseases: Links and Interactions vol.2018, pp.1942-0994, 2018, https://doi.org/10.1155/2018/7580707