Skip to main content
SpringerLink
Log in

Effect of seaweed mixture intake on plasma lipid and antioxidant profile of hyperholesterolaemic rats

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Cardiovascular disease (CVD) is the leading cause of death in many countries. Hypercholesterolaemia is a recurring risk factor in CVD leading to coronary atherosclerosis, stroke and ischemic heart disease. Previous research has proven that seaweeds are highly nutritious, providing a good source of dietary fibre, minerals, proteins and vitamins as well as being high in antioxidants. Antioxidants have been known to retard low-density lipoprotein (LDL) oxidation to reduce CVD risk in hypercholesterolaemia. However, there is yet to be a study on the effect of a mixture of different seaweed species on cholesterol lowering properties. Therefore, this study was designed to investigate the effects of a mixture of extracts from two seaweed species, red seaweed Kappaphycus alvarezii and brown seaweed Sargassum polycystum on plasma lipid and antioxidant profiles of rats fed high-cholesterol diet. S. polycystum extract significantly decreased plasma cholesterol by 37.52 % over an 8-week treatment period compared to K. alvarezii and mixture groups. However, S. polycystum showed an increase in plasma triglyceride (TG) levels by 16.66 %. K. alvarezii extract most effectively decreased TG levels by 40.11 % and the mixture extract most effectively increased high-density lipoprotein cholesterol by 56.71 %. All treatment groups were able to reduce LDL cholesterol levels compared to the high-cholesterol group, with no significant differences between them. K. alvarezii and S. polycystum mixture extract had the best atherogenic index, which is an indicator of lipid disorder in coronary diseases, among treatment and high-cholesterol-fed groups. All treatment groups were able to restore enzyme antioxidant levels (superoxide dismutase and catalase) to normal.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Aebi H (1984) Catalase in vitro. Method Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • AOAC (2000) Official methods of analysis (17th edition). AOAC, Gaithersburg

    Google Scholar 

  • Benzie IFF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76

    Article  CAS  PubMed  Google Scholar 

  • Chee S-Y, Wong P-K, Wong C-L (2011) Extraction and characterisation of alginate from brown seaweeds (Fucales, Phaeophyceae) collected from Port Dickson, Peninsular Malaysia. J Appl Phycol 23:191–196

    Article  Google Scholar 

  • Dobiásová M, Frohlich J (2001) The plasma parameter log (TG/HDL-C) as an atherogenic index: correlation with lipoprotein particle size and esterification rate inapob-lipoprotein-depleted plasma (FERHDL). Clin Biochem 34:583–588

    Article  PubMed  Google Scholar 

  • Duarte M, Moresco R, Duarte T, Santi A, Bagatini M, Da Cruz I, Schetinger M, Loro V (2010) Oxidative stress in hypercholesterolemia and its association with Ala16Val superoxide dismutase gene polymorphism. Clin Biochem 43:1118–1123

    Article  CAS  PubMed  Google Scholar 

  • Fakoya K, Owodeinde F, Akintola SF, Adewolo MA, Abass MA, Ndimele PE (2011) An exposition on potential seaweed resources for exploitation, culture and utilization in West Africa: a case study of Nigeria. J Fish Aquat Sci 6:37–47

    Article  Google Scholar 

  • Garewal HS (1997) Antioxidants and disease prevention. CRC Press, Florida

    Google Scholar 

  • Gomez-Gutierrez CM, Guerra-Rivas G, Soria-Mercado IE, Ayala-Sanchez NE (2011) Marine edible algae as disease preventers. In: Kim S-K (ed) Advances in food and nutrition research, vol 64. Academic Press, London, pp 29–39

    Google Scholar 

  • Hassan S, El-Twab SA, Hetta M, Mahmoud B (2011) Improvement of lipid profile and antioxidant of hypercholesterolemic albino rats by polysaccharides extracted from the green alga Ulva lactuca Linnaeus. Saudi J Biol Sci 18:333–340

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hayashi L, Oliveira E, Bleicher-Lhonneur G, Boulenguer P, Pereira RL, Seckendorff R, Shimoda V, Leflamand A, Vallée P, Critchley A (2007) The effects of selected cultivation conditions on the carrageenan characteristics of Kappaphycus alvarezii (Rhodophyta, Solieriaceae) in Ubatuba Bay, São Paulo, Brazil. J Appl Phycol 19:505–511

    Article  CAS  Google Scholar 

  • Howarth NC, Saltzman E, Roberts SB (2001) Dietary fiber and weight regulation. Nutr Rev 59:129–139

    Article  CAS  PubMed  Google Scholar 

  • Hrapkiewicz K, Medina L (2006) Clinical laboratory animal medicine: an introduction. Wiley-Blackwell, Iowa

    Google Scholar 

  • Huang L, Wen K, Gao X, Liu Y (2010) Hypolipidemic effect of fucoidan from Laminaria japonica in hyperlipidemic rats. Pharm Biol 48:422–426

    Article  CAS  PubMed  Google Scholar 

  • Jeon S-M, Kim HK, Kim HJ, Do GM (2007) Hypocholesterolemic and antioxidative effects of naringenin and its two metabolites in high cholesterol fed rats. Transl Res 149:15–21

    Article  CAS  PubMed  Google Scholar 

  • Jeon S-M, Kim H-J, Woo M-N, Lee M-K, Shin YC, Park YB, Choi M-S (2010) Fucoxanthin-rich seaweed extract suppresses body weight gain and improves lipid metabolism in high-fat-fed C57BL/6J mice. Biotechnol J 5:961–969

    Article  CAS  PubMed  Google Scholar 

  • Jialal I, Scaccini C (1992) Antioxidants and atherosclerosis. Curr Opin Lipidol 3:324

    Article  CAS  Google Scholar 

  • Jimenez-Escrig A, Sanchez-Muniz FJ (2000) Dietary fibre from edible seaweeds: chemical structure, physicochemical properties and effects on cholesterol metabolism. Nutr Res 20:585–598

    Article  CAS  Google Scholar 

  • Jiménez-Escrig A, Sánchez-Muniz FJ (2000) Dietary fibre from edible seaweeds: chemical structure, physicochemical properties and effects on cholesterol metabolism. Nutr Res 20:585–598

    Article  Google Scholar 

  • Jiménez-Escrig A, Gómez-Ordóñez E, Rupérez P (2011) Brown and red seaweeds as potential sources of antioxidant nutraceuticals. J Appl Phycol 24:1123–1132

    Article  Google Scholar 

  • Jiménez-Escrig A, Gómez-Ordóñez E, Tenorio M, Rupérez P (2013) Antioxidant and prebiotic effects of dietary fiber co-travelers from sugar Kombu in healthy rats. J Appl Phycol 25:503–512

    Article  Google Scholar 

  • Josephine A, Nithya K, Amudha G, Veena CK, Preetha S, Varalakshmi P (2008) Role of sulphated polysaccharides from Sargassum wighitii in cyclosporine A-induced oxidative liver injury in rat. BMC Pharmacol 8:4. doi:10.1186/1471-2210-8-4

  • Kanthe PS, Patil BS, Bagali S, Deshpande A, Shaikh GB, Aithala M (2012) Atherogenic index as a predictor of cardiovascular risk among women with different grades of obesity. Int J Collab Res Int Med Public Health 4:1767–1774

    Google Scholar 

  • Kantz K, Singleton VL (1990) Isolation and determination of polymeric polyphenols using Sephadex LH-20 and analysis of grape tissue extracts. Am J Enol Vitic 41:223–228

    CAS  Google Scholar 

  • Kim S-N, Lee W, Bae G-U, Kim YK (2012a) Anti-diabetic and hypolipidemic effects of Sargassum yezoense in db/db mice. Biochem Biophys Res Commun 424:675–680

    Article  CAS  PubMed  Google Scholar 

  • Kim S, Jung Y-J, Kwon O-N, Cha K, Um B-H, Chung D, Pan C-H (2012b) A potential commercial source of fucoxanthin extracted from the microalga Phaeodactylum tricornutum. Appl Biochem Biotechnol 166:1843–1855

    Article  CAS  PubMed  Google Scholar 

  • Lewis SM, Ulrey DE, Barnard DE, Knapka JJ (2006) Nutrition. In: Everitt JI, Gross EA (eds) The laboratory rat (2nd edition). Elsevier, London, p 219

    Google Scholar 

  • Lyon TP, Yankley A, Gofman JW, Strisower B (1956) Lipoproteins and diet in coronary heart disease: a five year study. Calif Med 84:325–328

    CAS  PubMed Central  PubMed  Google Scholar 

  • Maeda H, Hosokawa M, Sashima T, Funayama K, Miyashita K (2005) Fucoxanthin from edible seaweed, Undaria pinnatifida, shows antiobesity effect through UCP1 expression in white adipose tissues. Biochem Biophys Res Commun 332:392–397

    Google Scholar 

  • Maeda H, Hosogawa M, Sadhima T, Funayama K, Miyashita K (2007) Effect of medium-chain triacylglycerols on anti-obesity effect on fucoxanthin. J Oleo Sci 56:615–621

    Article  CAS  PubMed  Google Scholar 

  • Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474

    Article  CAS  PubMed  Google Scholar 

  • Matanjun P, Mohamed S, Mustapha NM, Muhammad K, Cheng HM (2008) Antioxidant activities and phenolics content of eight species of seaweeds from north Borneo. J Appl Phycol 20:367–373

    Article  CAS  Google Scholar 

  • Matanjun P, Mohamed S, Muhammad K, Mustapha NM (2010) Comparison of cardioprotective efffects of tropical seaweed Kappaphycus alvarezii, Caulerpa lentillifera, and Sargassum polycystum, on high-cholesterol/high-fat diet in rats. J Med Food 13:792–800

    Article  CAS  PubMed  Google Scholar 

  • McHugh D (2003) A guide to the seaweed industry. In: FAO Fisheries Technical Paper No. 441. FAO, Rome, 27 pages

  • Meddings JB, Spady DK, Dietschy JM (1987) Kinetic characteristics and mechanisms of regulation of receptor-dependent and receptor-independent LDL transport in the liver of different animal species and humans. Am Heart J 113:475–481

    Article  CAS  PubMed  Google Scholar 

  • Montolalu R, Tashiro Y, Matsukawa S, Ogawa H (2009) Effects of extraction parameters on gel properties of carrageenan from Kappaphycus alvarezii (Rhodophyta). J Appl Phycol 20:71–76

    Google Scholar 

  • Nakajima K, Nakano T, Tanaka A (2006) The oxidative modification hypothesis of atherosclerosis: the comparison of atherogenic effects on oxidized LDL and remnant lipoproteins in plasma. Clin Chim Acta 367:36–47

    Article  CAS  PubMed  Google Scholar 

  • Nelson S, Bose S, Grunwald G, Myhill P, McCord J (2006) The induction of human superoxide dismutase and catalase in vivo: a fundamentally new approach to antioxidant therapy. Free Radical Biol Med 40:341–347

    Article  CAS  Google Scholar 

  • Pandey KB, Rizvi SI (2009) Plant polyphenols as dietary antioxidants in human health and disease. Oxidative Med Cell Longev 2:270–278

    Article  Google Scholar 

  • Phillips G, William P (2000) Carrageenan. In: Imeson A (ed) Handbook of hydrocolloids. Woohead Publishing, Cambridge, p 87

    Google Scholar 

  • Placer ZA, Cushman LL, Johnson BC (1966) Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems. Anal Biochem 16:359–364

    Article  CAS  PubMed  Google Scholar 

  • Qi H, Zhang Q, Zhao T, Hu R, Zhang K, Li Z (2006) In vitro antioxidant activity of acetylated and benzoylated derivatives of polysaccharide extracted from Ulva pertusa (Chlorophyta). Bioorg Med Chem Lett 16:2441–2445

    Article  CAS  PubMed  Google Scholar 

  • Raghavendran H, Sathivel A, Devaki T (2005) Effect of Sargassum polycystum (Phaeophyceae)-sulphated polysaccharide extract against acetaminophen-induced hyperlipidemia during toxic hepatitis in experimental rats. Mol Cell Biochem 276:89–96

    Article  CAS  PubMed  Google Scholar 

  • Reagan-Shaw S, Nihal M, Ahmad N (2008) Dose translation from animal to human studies revisited. FASEB J 22:659–661

    Article  CAS  PubMed  Google Scholar 

  • Ren D, Noda H, Amano H, Nishino T, Nishizawa K (1994) Study on antihypertensive and antihyperlipidemic effects of marine algae. Fish Sci 60:83–88

    CAS  Google Scholar 

  • Saqui-Salces M, Dowdle WE, Reiter JF, Merchant JL (2012) A high-fat diet regulates gastrin and acid secretion through primary cilia. FASEB J 26:3127–3139

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schauss AG, Wu X, Prior RL, Ou B, Huang D, Owens J, Agarwal A, Jensen GS, Hart AH, Shanbrom E (2006) Antioxidant capacity and other bioactivities of the freeze-dried Amazonian Palm Berry, Euterpe oleraceae Mart. (Acai). J Agric Food Chem 54:8604–8610

    Article  CAS  PubMed  Google Scholar 

  • Swefy SE, Asker ME, Sousou LA, Mohammed HE (2002) A novel concept to preserve the beneficial effects of hormone replacement therapy in bilaterally female ovariectomised rats: role of lovastatin therapy. Pharmacol Res 45:167–173

    Article  PubMed  Google Scholar 

  • Tan MH, Johns D, Glazer NB (2004) Pioglitazone reduces atherogenic index of plasma in patients with type 2 diabetes. Clin Chem 50:1184–1188

    Article  CAS  PubMed  Google Scholar 

  • Vassalle C, Pratali L, Boni C, Mercuri A, Ndreu R (2008) An oxidative stress score as a combined measure of the pro-oxidant and anti-oxidant counterparts in patients with coronary artery disease. Clin Biochem 41:1162–1167.

    Google Scholar 

  • Walter MF, Jacob RF, Jeffers B, Ghadanfar MM, Preston GM, Buch J (2004) Serum levels of thiobarbituric acid reactive substances predict cardiovascular events in patients with stable coronary artery disease: a longitudinal analysis of the PREVENT study. J Am Coll Cardiol 44:1996–2002

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Yang G (1997) Comparison of effects of two kinds of soluble algae polysaccharide on blood lipid, liver lipid, platelet aggregation and growth in rats. Clin J Prev Med 31:342–345

    CAS  Google Scholar 

  • Wang B-G, Zhang W-W, Duan X-J, Li X-M (2009) In vitro antioxidative activities of extract and semi-purified fractions of the marine red alga, Rhodomela confervoides (Rhodomelaceae). Food Chem 113:1101–1105

    Article  CAS  Google Scholar 

  • Washington IM, Van Hoosier G (2012) Chapter 3—clinical biochemistry and hematology. In: Suckow MA, Stevens KA, Wilson RP (eds) The laboratory rabbit, guinea pig, hamster, and other rodents. Academic Press, Boston, pp 57–116

    Chapter  Google Scholar 

  • Yan XJ, Nagata T, Fan X (1998) Antioxidative activities in some common seaweeds. Plant Foods Hum Nutr 52:253–262

    Article  CAS  PubMed  Google Scholar 

  • Yen G-C, Chen H-Y (1995) Antioxidant activity of various tea extract in relation to their antimutagenicity. J Agric Food Chem 43:27–32

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by Ministry of Higher Education of Malaysia, project code: FRG0250-SKK-2/2010.

Author information

Authors and Affiliations

  1. School of Food Science and Nutrition, Universiti Malaysia Sabah, Jalan UMS, 88400, Kota Kinabalu, Sabah, Malaysia

    Amanda Dousip, Patricia Matanjun, Mohd Rosni Sulaiman, Yasmin Beng Houi Ooi & Tee Ping Lim

  2. School of Medicine, Universiti Malaysia Sabah, Jalan UMS, 88400, Kota Kinabalu, Sabah, Malaysia

    Tek Song Tan

Authors
  1. Amanda Dousip
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patricia Matanjun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohd Rosni Sulaiman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tek Song Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yasmin Beng Houi Ooi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tee Ping Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Patricia Matanjun.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dousip, A., Matanjun, P., Sulaiman, M.R. et al. Effect of seaweed mixture intake on plasma lipid and antioxidant profile of hyperholesterolaemic rats. J Appl Phycol 26, 999–1008 (2014). https://doi.org/10.1007/s10811-013-0128-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-013-0128-y

Keywords

Search

Navigation