Journal of Applied Phycology

, Volume 25, Issue 5, pp 1405–1412 | Cite as

Inhibitory activities of three Malaysian edible seaweeds on lipase and α-amylase

  • Vimala BalasubramaniamEmail author
  • Suraiami Mustar
  • Norhayati Mustafa Khalid
  • Aswir Abd Rashed
  • Mohd Fairulnizal Mohd Noh
  • Matthew D. Wilcox
  • Peter I. Chater
  • Iain A. Brownlee
  • Jeffrey P. Pearson


Ethanol extracts, dried powders and fibres (total and soluble fibre) of the tropical red algae Kappaphycus alvarezii, Kappaphycus striatus and Eucheuma denticulatum were analysed for their effect on lipase and α-amylase activity using turbidimetric method and dinitrosalicylic acid (DNS) assay, respectively. The nutrient composition analyses were determined using standard methods. The ethanol extract of dried K. striatus (Ks-III) showed the highest reduction in lipase activity with 92 % inhibition followed by seaweed powders (K. alvarezii (Ka-III), K. striatus (Ks-III) and E. denticulatum (Ed-III)) with average inhibition of 60 %. Soluble fibres of K. alvarezii (Ka-V) and E. denticulatum (Ed-V) showed significant inhibition with 60 and 57 % reduction, respectively. Only the ethanol extract of fresh E. denticulatum (Ed-I) showed 88 % inhibition of α-amylase. Nutritional component analyses showed that all three seaweeds are low in crude fat, suggesting the possible use of seaweed as a dietary supplement and for potential weight and glycaemia management.


Nutrient composition Lipase α-Amylase Seaweed Turbidimetric method Dinitrosalicylic acid assay 



The authors thank the Director General of Health Malaysia and the Director of Institute for Medical Research (IMR) for giving the permission to publish this article. We also thank the staff of the Nutrition Unit, Institute for Medical Research for their continuous support. We sincerely thank the Department of Fisheries Sabah, Malaysia for the supply of seaweed samples. This project was funded by the Ministry of Health, Malaysia.


  1. Ali H, Houghton PJ, Soumyanath A (2006) α-Amylase inhibitory activity of some Malaysian plants used to treat diabetes; with particular reference to Phyllanthus amarus. J Ethnopharmacol 107:449–455PubMedCrossRefGoogle Scholar
  2. Ballinger A, Peikin SR (2002) Orlistat: its current status as an anti-obesity drug. Eur J Pharmacol 440:109–117PubMedCrossRefGoogle Scholar
  3. Barbagallo M, Dominguez LJ, Galioto A, Ferlisi A, Cani C, Malfa L, Pineo A, Busardo' A, Paolisso G (2003) Role of magnesium in insulin action, diabetes and cardio-metabolic syndrome X. Mol Aspects Med 24:39–52PubMedCrossRefGoogle Scholar
  4. Birari RB, Bhutani KK (2007) Pancreatic lipase inhibitors from natural sources: unexplored potential. Drug Discov Today 12:879–889PubMedCrossRefGoogle Scholar
  5. Bitou N, Ninomiya M, Tsujita T, Okuda H (1999) Screening of lipase inhibitors from marine algae. Lipids 34:441–445PubMedCrossRefGoogle Scholar
  6. Braune W, Guiry MD (2011) Seaweeds. A colour guide to common benthic green, brown and red algae of the world's oceans. A.R.G. Gantner, RuggellGoogle Scholar
  7. Butt MS, Shahzadi N, Sharif MK, Nasir M (2007) Guar gum: a miracle therapy for hypercholesterolemia, hyperglycemia and obesity. Crit Rev Food Sci Nutr 47:389–396PubMedCrossRefGoogle Scholar
  8. Cengiz S, Cavaz L, Yurdakoc K (2010) Alpha-amylase inhibition kinetics by caulerpenyne. Medit Mar Sci 11:93–103CrossRefGoogle Scholar
  9. Chakraborthy K, Lipton AP, Paulraj R, Vijayan KK (2010) Antibacterial labdane diterpernoids of Ulva fasciata Delile from southwestern coast of the Indian Peninsula. Food Chem 119:1399–1408CrossRefGoogle Scholar
  10. Christobel GJ, Lipton AP, Aishwarya MS, Sarika AR, Udayakumar A (2011) Antibacterial activity of aqueous extract from selected macroalgae of southwest coast of India. Seaweed Res Utiln 33:67–75Google Scholar
  11. Chee SY, Wong PK, Wong CL (2011) Extraction and characterisation of alginate from brown seaweeds (Fucales, Phaeophyceae) collected from Port Dickson, Peninsular Malaysia. J Appl Phycol 23:191–196CrossRefGoogle Scholar
  12. Connan S, Goulard F, Stiger V, Deslandes E, Ar Gall E (2004) Interspecific and temporal variation in phlorotannin levels in an assemblage of brown algae. Bot Mar 47:410–416CrossRefGoogle Scholar
  13. Dawra RK, Makkar HP, Singh B (1988) Protein-binding capacity of microquantities of tannins. Anal Biochem 170:50–53PubMedCrossRefGoogle Scholar
  14. FOSS Analytical AB (2003) The determination of nitrogen according to Kjeldahl using block digestion and steam distillation. AN 300. FOSS Analytical AB, SwedenGoogle Scholar
  15. Fujisawa T, Ikegami H, Inoue K, Kawabata Y, Ogihara T (2005) Effect of two alpha-glucosidase inhibitors, voglibose and acarbose, on postprandial hyperglycemia correlates with subjective abdominal symptoms. Metabolism 54:387–390PubMedCrossRefGoogle Scholar
  16. Galisteo M, Duarte J, Zarzuelo A (2008) Effects of dietary fibers on disturbances clustered in the metabolic syndrome. J Nutr Biochem 19:71–84PubMedCrossRefGoogle Scholar
  17. He J, Streiffer RH, Muntner P, Krousel-Wood MA, Whelton PK (2004) Effect of dietary fibre intake on blood pressure: a randomized, double-blind, placebo-controlled trial. J Hypertens 22:73–80PubMedCrossRefGoogle Scholar
  18. Heo SJ, Hwang JY, Choi JI, Han JS, Kim HJ, Jeon YJ (2009) Diphlorethohydroxycarmalol isolated from Ishige okamurae, a brown algae, a potent α-glucosidase and α-amylase inhibitor, alleviates postprandial hyperglycemia in diabetic mice. Eur J Pharmacol 615:252–256PubMedCrossRefGoogle Scholar
  19. Hiroyuki F, Tomohide Y, Kazunori O (2001) Efficacy and safety of Touchi extract, an α-glucosidase inhibitor derived from fermented soybeans in non-insulin-dependent diabetic mellitus. J Nutr Biochem 12:351–356PubMedCrossRefGoogle Scholar
  20. Huang YW, Liu Y, Dushenkov S, Ho CT, Huang MT (2009) Anti-obesity effects of epigallocatechin-3-gallate, orange peel extract, black tea extract, caffeine and their combinations in a mouse model. J Funct Foods 1:304–310CrossRefGoogle Scholar
  21. Ikarashi N, Takeda R, Ito K, Ochiai W, Sugiyama K (2011) The inhibition of lipase and glucosidase activities by Acacia polyphenol. eCAM. doi: 10.1093/ecam/neq043
  22. Ioannou E, Roussis V (2009) Natural products from seaweeds. In: Osbourn AE, Lanzotti V (eds) Plant-derived natural products. Springer, Berlin, pp 51–81CrossRefGoogle Scholar
  23. Institute for Public Health (IPH) (2011) National Health and Morbidity Survey 2011 (NHMS 2011). Vol. 2: Non-communicable diseases; 2011Google Scholar
  24. Isaksson G, Lundquist I, Ihse I (1982) In vitro inhibition of pancreatic enzyme activities by dietary fiber. Digestion 24:54–59PubMedCrossRefGoogle Scholar
  25. Ito K, Hori K (1989) Seaweed: chemical composition and potential food uses. Food Rev Int 5:101–144CrossRefGoogle Scholar
  26. Iwai K, Kim M-Y, Onodera A, Matsue H (2006) α-Glucosidase inhibitory and anti-hyperglycemic effects of polyphenols in the fruit of Viburnum dilatatum Thunb. J Agric Food Chem 54:4588–4592PubMedCrossRefGoogle Scholar
  27. Iwai K (2008) Antidiabetic and antioxidant effects of polyphenols in brown alga Ecklonia stolonifera in genetically diabetic KK-Ay mice. Plant Foods Hum Nutr 63:163–169PubMedCrossRefGoogle Scholar
  28. Karamadoukis L, Shivashankar GH, Ludeman L, Williams AJ (2009) An unusal complication of treatment with orlistat. Clin Nephrol 71:430–432PubMedGoogle Scholar
  29. Lee SH, Park MH, Heo SJ, Kang SM, Ko SC, Han JS, Jeon YJ (2010) Dieckol isolated from Ecklonia cava inhibits α-glucosidase and α-amylase in vitro and alleviates postprandial hyperglycemia in streptozotocin-induced diabetic mice. Food Chem Toxicol 48:2633–2637PubMedCrossRefGoogle Scholar
  30. Mabeau S, Fleurence J (1993) Seaweed in food products: biochemical and nutritional aspects. Trends Food Sci Technol 4:103–107CrossRefGoogle Scholar
  31. Maeda H, Tsukui T, Sashima T, Hosokawa M, Miyashita K (2008) Seaweed carotenoid, fucoxanthin as a multi-functional nutrient. Asia Pac J Clin Nutr 17:196–199PubMedGoogle Scholar
  32. Manilal A, Sujith S, Sabarathnam B, Kiran GS, Selvin J, Shakir C, Lipton AP (2010) Bioactivity of the red alga Asparagopsis taxiformis collected from the Southwestern coast of India. Braz J Oceanogr 58:93–100CrossRefGoogle Scholar
  33. Matanjun P, Mohamed S, Noordin MM, Kharidah M (2009) Nutrient content of tropical edible seaweeds, Eucheuma cottonii, Caulerpa lentillifera and Sargassum polycystum. J Appl Phycol 21:75–80CrossRefGoogle Scholar
  34. Matanjun P, Mohamed S, Mustapha NM, Muhammad K, Cheng HM (2008) Antioxidant activities and phenolic content of eight species of seaweeds from north Borneo. J Appl Phycol 20:367–373CrossRefGoogle Scholar
  35. Matanjun P, Mohamed S, Muhammad K, Mustapha NM (2010) Comparison of cardiovascular protective effects of tropical seaweeds, Kappaphycus alvarezii, Caulerpa lentillifera, and Sargassum polycystum, on high-cholesterol/high-fat diet in rats. J Med Food 13:792–800PubMedCrossRefGoogle Scholar
  36. Menezes EW, de Melo AT, Lima GH, Lajolo FM (2004) Measurement of carbohydrate components and their impact on energy value of foods. J Food Compos Anal 17:331–338CrossRefGoogle Scholar
  37. Ministry of Health Malaysia (2006) Noncommunicable disease risk factors in Malaysia Disease Control Division (NCD). Malaysian NCD SurveillanceGoogle Scholar
  38. Norziah MH, Ching CY (2000) Nutritional composition of edible seaweed Gracilaria changii. Food Chem 68:69–76CrossRefGoogle Scholar
  39. Fayaz M, Namitha KK, Chidambara Murthy KN, Mahadeva Swamy M, Sarada R, Khanam S, Subbarao PV, Ravishankar GA (2005) Chemical composition, iron bioavailability, and antioxidant activity of Kappaphycus alvarezii (Doty). J Agric Food Chem 53:792–797PubMedCrossRefGoogle Scholar
  40. Neish IC (2007) Assessment of the seaweed value chain in Indonesia. United States for International Development. Accessed 16 April 2012
  41. Newman DJ, Cragg GM, Snader KM (2003) Natural products as source of new drugs over the period 1981–2000. J Nat Prod 66:1022–1037PubMedCrossRefGoogle Scholar
  42. Nickavar B, Mosazadeh G (2009) Influence of three Morus species extracts on α-amylase activity. Iran J Pharm Res 8:115–119Google Scholar
  43. Nwosu F, Morris J, Lund VA, Stewart D, Ross HA, McDougall GJ (2011) Anti-proliferative and potential anti-diabetic effects of phenolic-rich extracts from edible marine algae. Food Chem 126:1006–1012CrossRefGoogle Scholar
  44. O’Connor CJ, Sun D, Smith BG, Melton LD (2003) Effect of soluble dietary fibers on lipase-catalyzed hydrolysis of tributyrin. J Food Sci 68:1093–1099CrossRefGoogle Scholar
  45. O’Connor CJ, Lai DT (1996) Pregastric enzymes: how do they work and what do they do? N Z BioScience 4:17–23Google Scholar
  46. Paolisso G, Scheen A, D’Onofrio F, Lefebvre P (1990) Magnesium and glucose homeostasis. Diabetologia 33:511–514PubMedCrossRefGoogle Scholar
  47. Pasquier B, Armand M, Guillon F, Castelain C, Borel P, Barry J-L, Pieroni G, Lairon D (1996) Viscous soluble dietary fibers alter emulsification and lipolysis of triacylglycerols in duodenal medium in vitro. J Nutr Biochem 7:295–302CrossRefGoogle Scholar
  48. Pereira L, Amado AM, Critchley AT, van de Velde F, Ribeiro-Claro PJA (2009) Identification of selected seaweed polysaccharides (phycocolloids) by vibrational spectroscopy (FTIR-ATR and FT-Raman). J Food Hydrocolloids 23:1903–1909CrossRefGoogle Scholar
  49. Rebah FB, Smaoui S, Frikha F, Gargouri Y, Miled N (2008) Inhibitory effects of Tunisian marine algal extracts on digestive lipases. Appl Biochem Biotechnol 151:71–79PubMedCrossRefGoogle Scholar
  50. Renaud SM, Luong-Van JT (2006) Seasonal variation in the chemical composition of tropical Australian marine macroalgae. J Appl Phycol 18:381–387CrossRefGoogle Scholar
  51. Rupérez P (2002) Mineral content of edible marine seaweeds. Food Chem 79:23–26CrossRefGoogle Scholar
  52. Saris NE, Mervaala E, Karppanen H, Khawaja JA, Lewenstam A (2000) Magnesium. An update on physiological, clinical and analytical aspects. Clin Chim Acta 294:1–26PubMedCrossRefGoogle Scholar
  53. Smit AJ (2004) Medicinal and pharmaceutical uses of seaweed natural products: a review. J Appl Phycol 16:245–262CrossRefGoogle Scholar
  54. Subramanian R, Asmawi MZ, Sadikun A (2008) In vitro α-glucosidase and α-amylase enzyme inhibitory effects of Andrographis paniculata extract and andrographolide. Acta Biochim Polon 55:391–398PubMedGoogle Scholar
  55. Tadera K, Minami Y, Takamatsu K, Matsuoka T (2006) Inhibition of α-glucosidase and α-amylase by flavonoids. J Nutr Sci Vitaminol 52:149–153PubMedCrossRefGoogle Scholar
  56. Tee ES, Kuladevan R, Young SI, Khor SC, Zakiyah HO (1996) Laboratory procedures in nutrient analysis of foods. Division of Human Nutrition, Institute of Medical Research, Kuala Lumpur, MalaysiaGoogle Scholar
  57. Vogel WC, Zieve L (1963) A rapid and sensitive turbidimetric method for serum lipase based upon differences between the lipases of normal and pancreatitis serum. Clin Chem 9:168–181PubMedGoogle Scholar
  58. Weibel EK, Hadvary P, Hochuli E, Kupfer E, Lengsfeld H (1987) Lipstatin, an inhibitor of pancreatic lipase, produced by Streptomyces toxytricini. J Antibiot 40:1081–1085PubMedCrossRefGoogle Scholar
  59. Xu BJ, Han LK, Zheng YN, Sung CK (2005) In vitro inhibitory effect of triterpenoidal saponins from Platycodi Radix on pancreatic lipase. Arch Pharm Res 28:180–185PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Vimala Balasubramaniam
    • 1
    Email author
  • Suraiami Mustar
    • 1
  • Norhayati Mustafa Khalid
    • 1
  • Aswir Abd Rashed
    • 1
  • Mohd Fairulnizal Mohd Noh
    • 1
  • Matthew D. Wilcox
    • 2
  • Peter I. Chater
    • 2
  • Iain A. Brownlee
    • 3
  • Jeffrey P. Pearson
    • 2
  1. 1.Cardiovascular, Diabetes and Nutrition Research Centre, Nutrition UnitInstitute for Medical ResearchKuala LumpurMalaysia
  2. 2.Institute for Cell and Molecular Biosciences, The Medical SchoolUniversity of Newcastle Upon TyneNewcastle upon TyneUK
  3. 3.Nanyang Polytechnic Food and Human Nutrition DepartmentNewcastle UniversitySingaporeSingapore

Personalised recommendations