Antioxidant and hypolipidaemic properties of red seaweed, Gracilaria changii

Abstract

The edible red seaweed, Gracilaria changii, was collected from the coastal area of Sarawak, Malaysia, and evaluated for its hypolipidaemic properties using high cholesterol/high fat (HF) induced male Sprague–Dawley rats. In the in vivo study, the HF diet group showed significantly higher total cholesterol (TC), low density lipoprotein cholesterol (LDL-C), atherogenic index (AI) and body weight gain as compared to other treatment groups. At the end of treatment period, rats fed with a HF diet supplemented with 5 % freeze-dried G. changii powder had significantly reduced plasma TC (−39.19 %), LDL-C (−36.36 %), and triglycerides (TG) content (− 25.45 %). Meanwhile, 10 % seaweed powder significantly lowered the plasma TC, LDL-C and TG content by −40.34, −35.95 and −30.91 % respectively, compared to the HF group. The AI of rats supplemented with 10 % seaweed powder was the lowest among the treatment groups and indicates a lowered risk for cardiovascular diseases. The plasma lipid peroxidation of the seaweed powder-fed groups was also significantly lower than the HF group, while the erythrocyte enzyme antioxidant activities of superoxide dismutase, catalase and glutathione peroxidase of the treatment groups were also improved. Diets supplemented with seaweed powder also decreased plasma aspartate aminotransferase and the alanine aminotransferase levels.

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References

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

    CAS  Article  Google Scholar 

  2. Amano H, Kakinuma M, Coury DA, Ohno H, Hara T (2005) Effect of a seaweed mixture on serum lipid level and platelet aggregation in rats. Fisheries Sci 71:1160–1166

    CAS  Article  Google Scholar 

  3. Barasi ME (2003) Human nutrition: a health perspective (2nd edition). CRC Press, Boca Raton, pp 304–323

    Google Scholar 

  4. Bocanegra A, Nieto A, Blas B, Muniz FJS (2003) Diets containing a high percentage of Nori or Konbu algae are well-accepted and efficiently utilised by growing rats but induce different degrees of histological changes in the liver an bowel. Food Chem Toxicol 41:1473–1480

    CAS  PubMed  Article  Google Scholar 

  5. Bocanegra A, Nieto A, Bastida S, Benedi J, Sánchez-Muniz FJ (2008) A Nori not a Konbu, dietary supplement decreases the cholesterolaemia, liver fat infiltration and mineral bioavailability in hypercholesterolaemic growing Wistar rats. Brit J Nutr 99:272–280

    CAS  PubMed  Article  Google Scholar 

  6. Car BD, Eng VM, Everds NE, Bounous DI (2006) Clinical pathology of the rat. In: Suckow MA, Weisbroth SH, Franklin CL (eds) The Laboratory Rat, 2nd edn. Elsevier, San Diego, pp 127–146

    Google Scholar 

  7. Čejková J, Veiražka M, Pláteník J, Štípek S (2004) Age-related changes in superoxide dismutase, glutathione peroxidase, catalase and xanthine oxidoreductase/xanthine oxidase activities in the rabbit cornea. Exp Gerentol 39:1537–1543

    Article  Google Scholar 

  8. Evan GO (2009) Animal clinical chemistry. Taylor & Francis, Boca Raton, pp 48–49

    Google Scholar 

  9. Hercberg S, Galan P, Preziosi P, Alfarez M, Vazquezm C (1998) The potential role of antioxidant vitamins in preventing cardiovascular diseases and cancers. Nutrition 14:513–520

    CAS  PubMed  Article  Google Scholar 

  10. Hirunpanich V, Utaipat A, Morales NP, Bunyapraphatsara N, Sato H, Herunsale A, Suthisisang C (2006) Hypocholesterolemic and antioxidant effects of aqueous extracts from the dried calyx of Hibiscus sabdariffa L. in hypercholesterolemic rats. J Ethnopharmacol 103:252–260

    PubMed  Article  Google Scholar 

  11. Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597

    CAS  Article  Google Scholar 

  12. Jalili T, Medeiros DM, Wildman EC (2007) Dietary fiber and coronary heart disease. In: Wildman EC (ed) Handbook of nutraceuticals and functional foods, 2nd edn. Taylor and Francis, Boca Raton, pp 131–143

    Google Scholar 

  13. Jeon SM, Park YB, Kwan OS, Huh TL, Lee WH, Do KM, Park T, Choi MS (2005) Vitamin E supplementation alters HDL-cholesterol concentration and paraoxonase activity in rabbits fed high cholesterol diet: comparison with probucol. J Biochem Mol Toxi 19:336–346

    CAS  Article  Google Scholar 

  14. Jiménez-Escrig A, Gómez-Ordóñez E, Tenorio MD, 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 

  15. Kaliora AC, Dedoussis GVZ (2007) Natural antioxidant compounds in risk factors for CVD. Pharmacol Res 56:99–109

    CAS  PubMed  Article  Google Scholar 

  16. Kang MY, Kim SM, Rico CW, Lee SC (2012) Hypolipideamic and antioxidantive effects of rice bran and phytic acid in high fat fed mice. Food Sci Biotechnol 21:123–128

    CAS  Article  Google Scholar 

  17. Khan KH (2009) The effect of regular intake of Terminalia chebula on oxidative stress in mice originated from Salmonella typhimurium. Eurasia J Biosci 3:113–121

    Article  Google Scholar 

  18. Lecumberri E, Goya L, Mateos R, Alia M, Ramos S, Pulido MI, Bravo L (2007) A diet rich in dietary fiber from cocoa improve lipid profile and reduce malondialdehyde in hypercholesterolaemic rats. Nutrition 23:332–341

    CAS  PubMed  Article  Google Scholar 

  19. Manjunatha H, Srinivasan K (2007) Hypolipideamic and antioxidant effects of dietary curcumin and capsaicin in induced hypercholesterolaemic rats. Lipids 42:1133–1142

    Google Scholar 

  20. Marimuthu J, Essakimuthu P, Narayanan J, Anantham B, Joy R, Tharmaraj JM, Arumugan A (2012) Phytochemical characterization of brown seaweed Sargassum wightii. Asian Pac J Trop Dis 109 – 113

  21. 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

    CAS  PubMed  Article  Google Scholar 

  22. Martín-Carrón N, Saura-Calixto F, Goñi I (2000) Effects of dietary fibre-and polyphenol-rich grape products on lipidaemia and nutritional parameters in rats. J Sci Food Agr 80:1183–1188

    Article  Google Scholar 

  23. Maschek JA, Baker BJ (2008) The chemistry of algal secondary metabolism. In: Amsler CD (ed) Algal chemical ecology. Springer, Berlin, pp 1–24

    Google Scholar 

  24. Matanjun P, Mohammed S, Mustapha NM, Muhammad K (2009) Nutrient content of tropical seaweeds, Eucheuma cottonii, Caulerpa lentillifera and Sargassum polycystum. J Appl Phycol 21:75–80

    CAS  Article  Google Scholar 

  25. Matanjun P, Mohamed SM, Kharidah M, Noordin MM (2010) Comparison of cardiovascular protective effects of tropical seaweeds, Kappaphycus alravezii, Caulerpa lentillifera, and Sargassum polycystum, on high-cholesterol/high-fat diet in rats. J Med Food 13:792–800

    CAS  PubMed  Article  Google Scholar 

  26. Micallef MA, Garg ML (2009) Beyond blood lipids: phytosterols, statin and omega-3 polyunsaturated fatty acid therapy for hyperlipidemia. J Nutr Biochem 20:927–939

    CAS  PubMed  Article  Google Scholar 

  27. Namvar F, Mohamed S, Fard SG, Behravan J (2012) Polyphenol-rich seaweed (Eucheuma cottonii) extract suppresses breast tumour via hormone modulation and apoptosis induction. Food Chem 130:376–382

    CAS  Article  Google Scholar 

  28. Niki E (2009) Lipid peroxidation: physiological levels and dual biological effects. Free Radical Bio Med 47:469–484

    CAS  Article  Google Scholar 

  29. Norziah MH, Ching CY (2000) Nutritional composition of edible seaweed Gracilaria changii. Food Chem 68:69–76

    CAS  Article  Google Scholar 

  30. Patarra RF, Paiva L, Neto AI, Lima E, Baptista J (2011) Nutritional value of selected macroalgae. J Appl Phycol 23:205–208

    CAS  Article  Google Scholar 

  31. Rahman K (2007) Studies on free radicals, antioxidants and co-factors. Clin Interv Aging 2/2:219–236

    CAS  PubMed Central  PubMed  Google Scholar 

  32. Raja B, Saravanakumar M, Sathya G (2012) Veratic acid ameliorates hyperlipidemia and oxidative stress in Wistar rats fed an antherogenic diet. Mol Cell Biochem 366:21–30

    CAS  PubMed  Article  Google Scholar 

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

    CAS  Google Scholar 

  34. Saura-Calixto F (2011) Dietary fiber as a carrier of dietary antioxidants: an essential physiological function. J Agric Food Chem 59:43–49

    CAS  PubMed  Article  Google Scholar 

  35. Sivoňová M, Tatarková Z, Ďuračková Z, Dobrota D, Lehotsky J, Matáková T, Kaplán P (2007) Relationship between antioxidant potential and oxidative damage to lipids, proteins and DNA in aged rats. Physiol Res 56:757–764

    PubMed  Google Scholar 

  36. Smit AJ (2004) Medicinal and pharmaceutical uses of seaweed natural products: a review. J Appl Phycol 16:245–262

    CAS  Article  Google Scholar 

  37. Stancu C, Sima A (2001) Statins: mechanism of action and effects. J Cell Mol Med 5:378–387

    CAS  PubMed  Article  Google Scholar 

  38. Theuwissen E, Mensink RP (2008) Water-soluble dietary fibers and cardiovascular disease. Physiol Behav 94:285–292

    CAS  PubMed  Article  Google Scholar 

  39. Urbano MG, Goñi I (2002) Bioavailability of nutrients in rats fed on edible seaweeds, Nori (Porphyra tenera) and Wakame (Undaria pinnatifida), as a source of dietary fiber. Food Chem 76:281–286

    CAS  Article  Google Scholar 

  40. Weichselbaum E, Buttriss JL (2010) Polyphenols in the diet. Nutr Bull 35:157–164

    Article  Google Scholar 

  41. Wong KH, Sam SW, Cheung PCK, Ang PO (1999) Changes in lipid profiles of rats fed with seaweed-based diets. Nutr Res 19:1519–1527

    CAS  Article  Google Scholar 

  42. Woo MN, Bok SH, Choi MS (2009) Hypolipidemic and body fat-lowering effects of Fatclean in rats fed a high-fat diet. Food Chem Toxicol 47:2076–2082

    CAS  PubMed  Article  Google Scholar 

  43. Wong CK, Ooi VEC, Ang PO (2000) Protective effects of seaweeds against liver injury caused by carbon tetrachloride in rats. Chemosphere 41:173–176

    CAS  PubMed  Article  Google Scholar 

  44. Yang DJ, Chang YY, Hsu CL, Liu CW, Lin YL, Lin YH, Liu KC, Chen YC (2010) Antiobesity and hypolipidemic effects of polyphenol-rich Longan (Dimocarpus longans Lour.) flower water extract in hypercaloric-dietary rats. J Agr Food Chem 58:2020–2027

    CAS  Article  Google Scholar 

Download references

Acknowledgments

The authors thank the Fisheries Research Institute Malaysia Sarawak and the Seaweed Research Unit at Universiti Malaysia Sabah for supplying the seaweed. This study was funded by the Ministry of Higher Education of Malaysia, project code: FRG0250-SKK-2/2010.

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Correspondence to Patricia Matanjun.

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Chan, P.T., Matanjun, P., Yasir, S.M. et al. Antioxidant and hypolipidaemic properties of red seaweed, Gracilaria changii . J Appl Phycol 26, 987–997 (2014). https://doi.org/10.1007/s10811-013-0135-z

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Keywords

  • Rhodophyta
  • Gracilaria
  • Body weight
  • Dietary fibre
  • Enzyme antioxidants
  • Hypercholesterolaemic
  • Lipid peroxidation
  • Lipid profile