Lupin seeds lower plasma lipid concentrations and normalize antioxidant parameters in rats
DOI:
https://doi.org/10.3989/gya.056310Keywords:
Bitter lupin, Hypercholesterolemia, Oxidative stress, Rats, Sweet lupinAbstract
This study was designed to test bitter and sweet lupin seeds for lipid-lowering and for their antioxidative activities in hypercholesterolemic rats. The levels of plasma lipid, malondialdehyde (MDA) and whole blood reduced glutathione (GSH), as well as the activities of transaminases (ALT and AST), lactate dehydrogenase (LDH) in plasma, superoxide dismutase (SOD), glutathione peroxidase (GPx) in erythrocytes and plasma glutathione reductase (GR), glutathione-S-transferase (GST) and catalase (CAT) were examined. A hypercholesterolemia-induced diet manifested in the elevation of total lipids (TL), total cholesterol (TC), triglycerides (TG), LDL-C and MDA levels, ALT, AST, LDH activities and the depletion of GSH and enzymic antioxidants. The supplementation of a hypercholesterolemia-induced diet with bitter and sweet lupin seeds significantly lowered the plasma levels of TL, TC, TG and LDL-C. ALT, AST and LDH activities slightly decreased in treated groups compared with the hypercholesterolemic group (HC). Furthermore, the content of GSH significantly increased while MDA significantly decreased in treated groups compared with the HC group. In addition, the bitter lupin seed group improved enzymic antioxidants compared with the HC group. In general, the results indicated that the bitter lupin seed supplements are better than those containing sweet lupin seeds. These results suggested that the hypocholesterolemic effect of bitter and sweet lupin seed supplements might be due to their abilities to lower the plasma cholesterol level as well as to slow down the lipid peroxidation process and to enhance the antioxidant enzyme activity.
Downloads
References
Aebi H. 1984. Catalase in vitro. Method. Enzymol. 105, 121–126. doi:10.1016/S0076-6879(84)05016-3
Ahmed FA., El-Desoky GE, El-Saadawy SS and Ramadan ME. 1987. Carbohydrates and lipids changes in rats administrated certain synthetic and natural food colors. Minia J. Agric. Res. Dev. 9, 1101- 1116.
Allain CC, Poon LS, Chan CS, Richmoud W and Fu PC. 1974. Enzymatic determination of total serum cholesterol. Clin. Chem. 20, 470-475. PMid:4818200
AOAC 2000. Method of analysis. Association of Official Agriculture Chemists. Washington D.C.USA, 17th ed.
Bettzieche A, Brandsch C, Weibe K, Hirche F, Eder K and Stangl GI. 2008. Lupin protein influences the expression of hepatic genes involved in fatty acid synthesis and triacylglycerol hydrolysis of adult rats. Br. J. Nutr. 99, 952–962. doi:10.1017/S0007114507857266 PMid:18096091
Beutler E, Duron O and Kelly BM, 1963. Improved method for the determination of blood glutathione. J. Lab. Clin. Med. 61, 882–888. PMid:13967893
Burstein M. 1970. A fully enzymatic colorimetric determination of HDL cholesterol in the serum. Lipid Res. 1, 583-595.
Carr TP, Gallaher DD, Yang CH and Hassel CA. 1996. Increased intestinal contents viscosity and cholesterol absorption efficiency in hamsters fed hydroxypropyl methylcellulose. J. Nutr. 126, 1463–1469. PMid:8618144
Chango A, Villaume C, Bau HM, Schwertz A, Nicolas J P and Mejean L. 1998. Effects of casein, sweet white lupin and sweet yellow lupin diet on cholesterol metabolism. J. Sci. Food Agric. 76, 303–309. doi:10.1002/(SICI)1097-0010(199802)76:2<303::AID-JSFA961>3.0.CO;2-#
Choct M and Annison G. 1990. Antinutritive activity of wheat pentosans in broiler diets. Br. Poult. Sci. 31, 811–821. doi:10.1080/00071669008417312 PMid:2097035
Costa NMB, Low AG, Walker AF, Owen RW and Englyst NH. 1994. Effect of baked beans (Phaseolus vulgaris) on steroid metabolism and non-starch polysaccharides output of hypercholesterolaemic pigs with or without an ileorectal anastomosis. Br. J. Nutr. 71, 871–886. doi:10.1079/BJN19940193 PMid:8031736
Cowling WA, Huyghe C and Swiecicki W. 1998. Lupin breeding. In Lupins as Crop Plants: Biology, Production, and Utilization. J.S. Gladstones, C.A. Atkins, and J. Hamblin, editors. CAB International, Wallingford, UK. 93–120.
Dringen R. 2000. Metabolism and functions glutathione in brain. Prog. Neurobiol. 62, 649-671. doi:10.1016/S0301-0082(99)00060-X
Duranti M, Consonni A, Magni C, Sessa F and Scarafoni A. 2008. The major proteins of lupin seed: Characterisation and molecular properties for use as functional and nutraceutical ingredients. Trends Food Sci. Technol. 19, 624-633. doi:10.1016/j.tifs.2008.07.002 PMid:21299575
Eder K, Roth-Maier D and Kirchgessner M. 1996. The effect of enzyme supplements and high amounts of white lupins on concentrations of lipids in serum and meat in fattening chickens. Arch. Anim. Nutr. 49, 221–228. doi:10.1080/17450399609381883 PMid:8767056
Eskander EF and Won Jun H. 1995. Hypoglycaemic and hyperinsulinemic effects of some Egyptian herbs used for the treatment of diabetes mellitus (type II) in rats. Egypt. J. Pharm. 36, 331–342.
Fisher RA. 1970. Statistical method for research workers Edinburgh ed. 14, Oliver and Boyed, p. 140. Fki I, Bouaziz M, Sahnoun Z and Sayadi S. 2005. Hypercholesterolemic effects of phenolic-rich extracts of Chemlali olive cultivar in rats fed a cholesterol-rich diet. Bioorg. Med. Chem. 13, 5362-5370.
Fossati P and Prencipe L. 1982. The determination of triglyceride using enzymatic methods. Clin. Chem. 28, 2077-2080. PMid:6812986
Fukushima M, Takayama Y, Habaguchi T and Nakano M. 1997. Comparative hypocholesterolemic effects of capybara (Hydrochoerus hydrochaeris dabbenei) oil, horse oil and sardine oil in cholesterol-fed rats. Lipids 32, 391-395. doi:10.1007/s11745-997-0050-z PMid:9113627
Gallaher DD, Hassel CA, Lee KJ and Gallaher C. 1993. Viscosity and fermentability as attributes of dietary fiber responsible for the hypocholesterolemic effect. J. Nutr. 123, 244–252. PMid:8381479
Gladstones JS. 1998. Distribution, origin, taxonomy, history and importance. In Lupins as Crop Plants: Biology, Production, and Utilization. J.S. Gladstones, C.A. Atkins, and J. Hamblin, editors. CAB International, Wallingford, UK. 1–39.
Goldberg DM and Spooner RJ. 1983. Glutathione reductase. In: Bergmeyer HU, Bergmeyer J and Bral M. (ed). Methods of enzymatic analysis, 3rd ed., vol. 3. Verlag Chemie, Weinheim, pp 258-265.
Habig W, Pabst M and Jakoby WB. 1974. Glulathione-Stransferase: The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249, 7130-7139. PMid:4436300
Hall RS, Johnson SK, Baxter AL and Ball MJ 2005b. Lupin kernel fiber-enriched food beneficially modify some lipids in men. Eur. J. Clin. Nutr. 59, 325–333. doi:10.1038/sj.ejcn.1602077 PMid:15508014
Hall RS, Thomas SJ and Johnson SK. 2005a. Australian sweet lupin flour addition reduces the glycaemic index of a white bread breakfast without affecting palatability in healthy human volunteers. Asia Pac. J. Clin. Nutr. 14, 91–97. PMid:15734714
Halliwell B and Gutteridge JMC. 1999. The chemistry of the free radicals and related reactive species. In: Halliwell, B. and Gutteridge, J.M.C., editors. Free radicals in biology and medicine. 3rd ed. Oxford: Oxford science publications, pp. 36-104.
Hughes JS. 1991. Potential contribution of dry bean dietary fiber to health. Food Technol. 9,122–126. Kempaiah RK and Srinivasan K. 2004. Antioxidant status of red blood cells and liver in hypercholesterolemic rats fed hypolipidemic spices. Int. J. Vitam. Nutr. Res. 74, 199– 208.
Kempaiah RK and Srinivasan K. 2005. Influence of dietary spices on the fluidity of erythrocytes in hypercholesterolemic rats. Br. J. Nutr. 93, 81–91. doi:10.1079/BJN20041317 PMid:15705229
Kerckhoffs DAJM, Brouns F, Hornstra G and Mensink RP. 2002. Effects on the human serum lipoprotein profile of ?-glucan, soy protein and isoflavones, plant sterols and stanols, garlic and tocotrienols. J. Nutr. 132, 2494–2505. PMid:12221200
Knight JA, Anderson SJ and Rawle JM. 1972. Chemical bases of the sulfo-phosphovanillin reaction for estimating serum total lipids. Clin. Chem. 18, 199–202. PMid:5020813
Lee Y, Mori T, Puddey I, Sipsas S, Ackland T and Beilin L. 2009. Effects of lupin kernel flour-enriched bread on blood pressure: A controlled intervention study. Am. J. Clin. Nutr. 89, 766–772. doi:10.3945/ajcn.2008.26708 PMid:19144734
Lee Y, Mori T, Sipsas S, Barden A, Puddey I and Burke V. 2006. Lupin-enriched bread increases satiety and reduces energy intake acutely. Am. J. Clin. Nutr. 84, 975–980. PMid:17093146
Lee R and Niemann D. 1996. Nutritional Assessment 2nd ed Mosby Missou USA.
Levy, A.L. 1981. A fully enzymatic colourimetric determination of LDL- cholesterol in the serum.Clin. Chem. 27, 653 –662. PMid:7226489
Magni C, Sessa F, Accardo E, Morazzoni P, Scarafoni A and Duranti M. 2004. Conglutin γ, a lupin seed protein, binds insulin in vitro and reduces plasma glucose levels in hyperglycaemic rats. J. Nutr. Biochem. 15, 646–650. doi:10.1016/j.jnutbio.2004.06.009 PMid:15590267
Mansour HA, Newairy AA, Yousef MI and Sheweita SA. 2002. Biochemical study on the effects of some Egyptian herbs in alloxan-induced diabetic rats. Toxicol. 170, 221–228. doi:10.1016/S0300-483X(01)00555-8
Marchesi M, Parolini C, Diani E, Rigamonti E, Cornelli L and Arnoldi A. 2008. Hypolipidaemic and antiatherosclerotic effects of lupin proteins in a rabbit model. Br. J. Nutr. 4, 1–4.
Martins JM, Riottot M, de Abreu MC, Viegas-Crespo AM, Lança MJ, Almeida JA, Freire JB and Bento O. 2004. Dietary raw peas (Pisum sativum L.) reduce plasma total and LDL cholesterol and hepatic esterified cholesterol in intact and ileorectal anastomosed pigs fed cholesterol-rich diets. J. Nutr. 134, 3305–3312. PMid:15570030
Martins JM, Riottot M, de Abreu MC, Viegas-Crespo AM, Lança MJ, Almeida JA, Freire JB and Bento O. 2005. Cholesterol-lowering effects of dietary blue lupin (Lupinus angustifolius L.) in intact and ileorectal anastomosed pigs. J. Lipid Res. 45, 1539-1547. doi:10.1194/jlr.M500129-JLR200 PMid:15834122
Nishikim, M, Roa NA and Yagi K. 1972. The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem. Biophys. Res. Commun. 46, 849-854. doi:10.1016/S0006-291X(72)80218-3
Novikov KN and Kagan V. 1985. Stabilization of cytochrome P450 in hepatocytes by free radical scavenger of different nature. Acta Physiol. Pharmacol. Bulg. 11, 61–69. PMid:3832795
Paglia DE and Valentine VW. 1970. Studies on the qualitative and quantitative characterization of erthyrocyte glutathione peroxidase. J. Lab. Clin. Med. 70, 158-178.
Petterson, D.S. 1998. Composition and food uses of lupins. In Lupins as Crop Plants: Biology, Production, and Utilization. J.S. Gladstones, C.A. Atkins, and J. Hamblin, editors. CAB International, Wallingford, UK. 353–384.
Pilvi TK, Jauhiainen T, Cheng ZJ, Mervaala EM, Vapaatalo H and Korpela R. 2006. Lupin protein attenuates the development of hypertension and normalises the vascular function of NaCl-loaded Goto-Kakizaki rats. J. Physiol. Pharmacol. 57, 167– 176. PMid:16845223
Putnam DH, Oplinger ES, Hardman LL and Doll JD. 1989. Lupin. In: Alternative field crops manual. Center for Alternative Plant and Animal Products, University of Minnesota, St. Paul.
Quist EE. 1980. Regulation of erythrocyte membrane shape by Ca2+. Biochem. Biophys. Res. Commun. 92, 631-637. doi:10.1016/0006-291X(80)90380-0
Rahman MH, Hossain A, Siddiqua A and Hossain I. 1996. Hemato-biochemical parameters in rats fed Lupinus angustifolius (sweet lupin) seed protein and fiber fractions. J. Clin. Biochem. Nutr. 20, 99–111.
Reitman S and Frankel S. 1957. A colourimetric method for the determination of serum glutamic oxaloacetic and glutamic pyruvic transaminases. Am. J. Clin. Path. 28, 56-62. PMid:13458125
Rubio LA, Brenes A and Centeno C. 2003. Effects of feeding growing broiler chickens with practical diets containing sweet lupin (Lupinus angustifolius) seed meal. Br. Poult. Sci. 44, 391–397. doi:10.1080/0007166031000085553 PMid:12964623
S.P.S.S. 1999. Statistical Package for the Social Science, Inc. Chicago.
Sheweita SA, Newairy AA, Mansour HA and Yousef MI. 2002. Effect of some hypoglycemic herbs on the activity of phase I and II drug-metabolizing enzymes in alloxan-induced diabetic rats. Toxicol. 174, 131–139. doi:10.1016/S0300-483X(02)00048-3
Shinnick FL, Lnk SL and Marlett JA. 1990. Dose response to a dietary oat bran fraction in cholesterol-fed rats. J. Nutr. 120, 561-568. PMid:2161914
Sirtori CR, Lovati MR, Manzoni C, Castiglioni S, Duranti M, Magni C, Morandi S, D’Agostina A and Arnoldi A. 2004. Proteins of white lupin seed, a naturally isoflavone-poor legume, reduce cholesterolemia in rats and increase LDL receptor activity in HepG2 cells. J. Nutr. 134, 18–23. PMid:14704287
Sirtori E, Resta D, Brambilla F, Zacherl C and Arnoldi A. 2010. The effects of various processing conditions on a protein isolate from Lupinus angustifolius. Food Chem. 120, 496–504. doi:10.1016/j.foodchem.2009.10.043
Souba WW and Wilmore DW 1983. Postoperative alteration of arteriovenous exchange of amino acids across the gastrointestinal tract. Surgery 94, 342-350. PMid:6879448
Spielmann J, Shukla A, Brandsch C, Hirche F, Stangl GI and Eder K. 2007. Dietary lupin protein lowers triglyceride concentrations in liver and plasma in rats by reducing hepatic gene expression of sterol regulatory element-binding protein-1c. Ann. Nutr. Metab. 51, 387–392. doi:10.1159/000107720 PMid:17785965
Sudhahar V, Kumar SA, Sudharsan PT and Varalakshmi P. 2007. Protective effect of lupeol and its ester on cardiac abnormalities in experimental hypercholesterolemia. Vascul. Pharmacol. 46, 412–418. doi:10.1016/j.vph.2006.12.005 PMid:17336164
Tauseef M, Sharma KK and Fahim M. 2007. Aspirin restores normal baroreflex function in hypercholesterolemic rats by its antioxidative action. Eur. J. Pharmacol. 556, 136- 143. doi:10.1016/j.ejphar.2006.11.029 PMid:17187777
Trinder, P. 1969. Determination of blood glucose using an oxidation peroxidase system with a non carsinogenic chromogene. Ann. Clin. Biochem. 6, 24.
Uchiyama M and Mihara M. 1978. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal. Biochem. 86, 271-278. doi:10.1016/0003-2697(78)90342-1
Van Barneveld R J. 1999. Understanding the nutritional chemistry of lupin (Lupinus spp.) seed to improve livestock production efficiency. Nutr. Res. Rev. 12, 203–230. doi:10.1079/095442299108728938 PMid:19087452
Viveros A, Centeno C, Arija I and Brenes A. 2007. Cholesterol-Lowering Effects of Dietary Lupin (Lupinus albus var Multolupa) in Chicken Diets. Poult. Sci. 86, 2631–2638. doi:10.3382/ps.2007-00128 PMid:18029810
Waller RA and Duncan DB. 1969. Aboys rule for symmetric multiple comparison problem. An. State Assoc. J. 65, 1485–1503.
Yoshie-Stark Y and Wäsche A. 2004. In vitro binding of bile acids by lupin protein isolates and their hydrolysates. Food Chem. 88, 179–184. doi:10.1016/j.foodchem.2004.01.033
Youness RI, Ahmaed HH, Fayez H, Mansour SA and Soliman FA. 1985. The hypoglycemic effects of some commonly used plants and seeds. Zool. Soc. Egypt. Bull. 35, 121–128.
Young DS. 2001. Effects of Disease on Clinical Laboratory Tests. 4th ed. Washington, DC: American Association for Clinical Chemistry.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2011 Consejo Superior de Investigaciones Científicas (CSIC)
This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the print and online versions of this journal are the property of the Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.
All contents of this electronic edition, except where otherwise noted, are distributed under a Creative Commons Attribution 4.0 International (CC BY 4.0) licence. You may read the basic information and the legal text of the licence. The indication of the CC BY 4.0 licence must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the final version of the work produced by the publisher, is not allowed.
