Abstract
The intake of food and control of blood glucose levels are very important in diabetic patients. α-Glucosidase inhibitors are a cost-effective means to prevent the progression of diabetes. To find a natural inhibitor from seaweed with anti-hyperglycemic effects, methanolic extract of a red seaweed, Kappaphycus alvarezii (Doty) Doty ex P. Silva, which contains complex mixtures of various types of bioactive compounds which have a hypoglycaemic effect was evaluated in alloxan-induced diabetic rats by using two different doses (200 and 400 mg kg−1 body weight). Blood glucose, glycosylated haemoglobin, haemoglobin, serum lipids of total cholesterol, triglyceride, high-density lipoprotein cholesterol (HDL-C), phospholipids, low density lipoprotein (LDL) and plasma insulin were examined in control and seaweed extract-treated experimental rats. The aqueous extract was orally administered for 28 days. The results showed that the aqueous extract of K. alvarezii significantly (p < 0.05) reduced blood glucose level and restored glycosylated haemoglobin and plasma insulin. These results demonstrate that K. alvarezii can be used as a health food and has strong anti-diabetic effects in vivo; thus, it may have beneficial properties in the prevention of diabetes and could be useful in the development of anti-diabetic drugs.
Similar content being viewed by others
References
Alberti KGMM, Press CM (1982) The biochemistry and the complications of diabetes. In: Keen H, Jarrett J (eds) Complications of diabetes. Edward Arnold, London, pp 231–270
Al-Shamaony I, Al-Khazaraji SM, Twaiji HA (1994) Hypoglycaemic effect of Artemisis berba alba-II. Effect of a valuable extract on some blood parameters in diabetic animals. J Ethanopharmacol 43:167–171
Ayyman MM, Mousa OG, Hassan AE, Khaled NME Sherif H Nermeen MM, Omnia EH (2014) Antidiabetic and insulin sensitizing effects of padina pavonia and turbenaria ornata in streptozotocin/nicotinamide diabetic rats. Asian J Pharm Clin Res 7:74–78
Anderson L, Dinesen B, Jorgensen PN, Poulsen F, Roder MF (1993) Enzyme immunoassay for intact human insulin in serum or plasma. Clin Chem 39:578–582
Balasubramaniam V, Mustar S, Khalid NM, Rashed AA, Noh MFM, Wilcox MD, Chater P, Brownlee IA, Pearson JP (2013) Inhibitory activities of three Malaysian edible seaweeds on lipase and α-amylase. J Appl Phycol 25:1405–1412
Bever BO, Zahnd GR (1979) Plants with oral hypoglycaemic action. Quart J Crude Drug Res 17:139–196
Bixler HJ, Porse H (2011) A decade of change in the seaweed hydrocolloids industry. J Appl Phycol 23:321–335
Celikler S, Tas S, Vatan O, Ziyanok-Ayvalik S, Yildiz G, Bilaloglu R (2009) Anti- hyperglycaemic and antigenotoxic potential of Ulva rigida ethanolic extract in the experimental diabetes mellitus. Food Chem Toxicol 47:1837–1840
Chan P, Matanjun P, Yasir S, Tan T (2014) Antioxidant and hypolipidaemic properties of red seaweed, Gracilaria changii. J Appl Phycol 26:987–997
Colca JR, Kotage N, Brooks CL, Lacy PE, Landt M, Mc Danield M (1983) Alloxan inhibition of a Ca2+ and calmodulin-dependent protein kinase in pancreatic islets. J Biol Chem 25:7260–7263
Cyriac B, Eswaran K (2015) In vitro antioxidant activity of Kappaphycus alvarezii (Doty) Doty ex P. Silva. J Harmonized Res Appl Sci 3:165–171
Dembinska-Kiec A, Mykkanen O, Kiec-Wilk B, Mykkanen H (2008) Antioxidant phytochemicals against type 2 diabetes. Br J Nutr 99E(1):ES109–ES117
Drabkin DL, Austin JM (1932) Spectrophotometric constants for common haemoglobin derivatives in human, dog and rabbit blood. J Biol Chem 98:719–733
Elavarasi S, Saravanan KC, Renuka C (2013) A systematic review on medicinal plants used to rat diabetes mellitus. Int J Pharmaceut Chem Biol Sci 3:983–992
Eswaran K, Ghosh PK, Siddhanta AK, Patolia JS, Periyasamy C, Mehta AS, Mody KH, Ramavat BK, Kamalesh Prasad, Rajyaguru MR, Kulandaivel Reddy CRK, Pandya JB, Tewari A (2005) Integrated method for production of carrageenan and liquid fertilizer from fresh seaweeds. U.S. Patent No. 6,893,479
Eswaran K, Ghosh PK, Subbarao PV, Mairh OP (2006) Field cultivation of Kappaphycus alvarezii in India. In: A.Tewari (ed.) Recent advances on applied aspects of Indian Marine algae with reference to global scenario, Central Salt & Marine Chemicals Research Institute, Bhavnagar, pp 250–261
Gidez WM, Webb M (1959) Revision of cholesterol determination. J Biochem 187:97–106
Gordan T, Castelli WP, Hjortland MC, Kannel WB, Dawber TR (1977) High density lipoprotein as a protective factor against heart disease. Am J Med 62:707–714
Guyton AC, Hall JE (2000) Medical physiology, 10th edn. WB. Saunders Co, Philadelphia, pp 810–818
Hakim ZS, Patel BK, Goyal RK (1997) Effects of chronic ramipril treatment in streptozotocin-induced diabetic rats. Indian J Physiol Pharmacol 41:353–36
Holdt SL, Kraan S (2011) Bioactive compounds in seaweed; functional food applications and legislation. J Appl Phycol 23:543–597
International Diabetes Federation 20th World Diabetes Congress (2009) (Montreal, Quebec, Canada, October 18–22)
Iwai K (2008) Antidiabetic and antioxidant effects of polyphenols in brown alga Ecklonia stolonifera in genetically diabetic KK-A9y mice. Plant Foods Human Nutr 63:163–169
Jackson RL, Hess RL, England JD (1979) Haemoglobin A1C values in children with over diabetes maintained in varying degree of control. Diabetes Care 2:391–395
Jones AF, Winkles JW, Jennings PE, Florkowski CM, Lunec J, Barnett AH (2008) Serum antioxidant activity in diabetes mellitus. Diabetes Res 7:89–92
Kameswara RB, Kesavalu MM, Apparaco C (2003) Evaluation of antidiabetic effect of Momordica cymbalaria fruit in alloxan-diabetic rats. Fitoterapia 74:7–13
Kim SN, Kim JY, Choi WH, Lee SS (2008) Effects of seaweed supplementation on blood glucose concentration, lipid profile, and antioxidant enzyme activities in patients with type 2 diabetes mellitus. Nutr Res Pract 2:62–67
Koenig RJ, Peterson CM, Jones R, Saudek C, Lehrman M, Cerami A (1976) A correlation of glucose regulation and haemoglobin A1C in diabetes mellitus. New Engl J Med 295:417–420
Laakso M (1995) Epidemiology of diabetic dyslipidaemia. Diabetes Rev 3:408–422
Lazarow A (1964) Alloxan diabetes and mechanism of β-cells damage by chemical agents. Experimental diabetes. Blackwell, Oxford, pp 49–69
Le Marche B, Paradis MV, Couture P (2010) Study of the acute impact of polyphenols form brown seaweeds on glucose control in healthy men and women. FASEB J 24:209
Lee SH, Li Y, Karadeniz F, Kim MM, Kim SK (2008) α-Glucosidase and α-amylase inhibitory activities of phloroglucinol derivatives from edible marine brown alga, Ecklonia cava. J Sci Food Agric 89:1552–1558
Lee SH, Han JS, Heo SJ, Hwang JY, Jeon YJ (2010) Protective effects of dieckol isolated from Ecklonia cava against high glucose-induced oxidative stress in human umbilical endothelial cells. Toxicol in Vitro 24:375–381
Ling ALM, Yasir S, Matanjun P, Abu Bakar MF (2015) Effect of different drying techniques on the phytochemical content and antioxidant activity of Kappaphycus alvarezii. J Appl Phycol 27:1717–1723
Mahmoud AM, Walaa GH, Soliman HA, Mostafa SR (2015) Enteromorpha flexuosa improves insulin sensitivity and metabolic control in fructose-induced diabetic rats. J Endocrinol Diabetes Obes 3:1072
Nagarani N, Kamaguru AK (2013) Evaluation of anti-inflammatory, antidiabetic, cytotoxic activity of Kapaphycus alvarezii. Int J Pharm Bio Sci 4:921–929
Nayak S, Pattabiraman TN (1981) A new colorimetric method for the estimation of glycosylated haemoglobin. Clin Chim Acta 109:267–274
Parkeh AC, Jung DH (1970) Cholesterol determination with ferric acetate uranium acetate reagent and sulphuric acid-ferrous sulphate reagents. Anal Chem 42:1423–1427
Prince PSM, Menon VP, Gunasekaran G (1999) Hypolipidaemic action of Tinospora cardifolia roots in Alloxan-induced diabetes rats. J Ethanopharmacol 64:53–57
Qi H, Zhao T, Zhang Q, Li Z, Zhao Z, Xing R (2005) Antioxidant activity of different molecular weight sulfated polysaccharides from Ulva pertusa Kjellm (Chlorophyta). J Appl Phycol 17:527–534
Rajkumar L, Srinivasan N, Balasubramanian K, Govindarajulu P (1991) Increased degradation of dermal collagen in diabetic rats. Indian J Exp Biol 29:1081–1083
Rhoads GG, Gulbrandsne CL, Kagan A (1976) Serum lipoproteins and coronary heart disease in a population study of Hawaii Japanese men. New Engl J Med 294:293–298
Rice EW, Roderick P, Mac-Donald RP (1970) Determination of triglycerides. Stand Meth Clin Chem 6:215–222
Segal P, Bachorik PS, Rifaind BM, Levy R (1984) Lipids & dyslipoproteinemia. Clin Diagn Manag 19:180–203
Sheela CG, Augusti KT (1992) Antidiabetic effects of garlic, Allium sativam Linn. Ind J Exp Biol 30:523–552
Siriwardhana N, Lee KW, Kim SH, Ha JW, Jeon YJ (2003) Antioxidant activity of Hizikia fusiformis on reactive oxygen species scavenging and lipid peroxidation inhibition. Food Sci Technol Int 9:339–347
Tolman KG, Fonseca V, Tan MH, Dalpiaz A (2004) Narrative review: hepatobiliary disease in type 2 diabetes mellitus. Ann Internal Med 141:946–956
Trigui M, Gasmi L, Zouari I, Tounsi S (2013) Seasonal variation in phenolic composition, antibacterial and antioxidant activities of Ulva rigida (Chlorophyta) and assessment of antiacetylcholinesterase potential. J Appl Phycol 25:319–328
Trinder P (1969) Determination of blood glucose using an oxidase peroxidases system with a non-carcinogenic chromogen. J Clin Pathol 22:158–161
Udoamaka F, Ezuruike N, Jose MP (2014) The use of plants in the tradition management of diabetes in Nigeria: Pharmacological and toxicological considerations. J Ethnopharmacol 155:857–924
Wadkar KA, Magdum CS, Patil SS, Naikwade NS (2008) Anti-diabetic potential and Indian medicinal plant. J Herb Med Toxicol 2:45–50
Waynforth BH (1980) Injection Techniques, In: Experimental and Surgical Techniques in the Rat. Academic Press, London, pp 3–61
Whiting DR, Guariguta L, Shaw JWC (2011) IDF Diabetes Atlas: Global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract 94:311–321
World Health Organization (2002): Diabetes mellitus. Fact sheet no. 138.
Yavuz JO, Cam O, Bukan N, Guven A, Silan F (2003) Protective effect of melatonin on β- cell damage in streptozotocin-induced diabetes in rats. Acta Histochemica 105:261–26
Zhang J, Tiller C, Shen J, Wang C, Giroraud G, Dennis D (2007) Antidiabetic properties of polysaccharide and polyphenolic-enriched fractions form the brown seaweed Ascophyllum nodosum. Can J Physiol Pharmacol 85:1115–1123
Zilversmit DB, Davis AK (1950) Micro determination of plasma phospholipids by trichloride acetic acid precipitation. J Lab Clin Med 35:155–161
Zimmet PZ, Mc Carty DJ, Courten MP (1997) The global epidemiology of non-insulin dependent diabetes mellitus and the metabolic syndrome. J Diabetes Complicat 11:60–68
Acknowledgments
The authors express their sincere thanks to Dr. Sr. A. Jospin Nirmala Mary, the Principal of Fatima College, Madurai, for her keen interest in this study and providing facilities to carry out the experiments. They also thank Dr. C. R. K. Reddy, Group leader, seaweed cultivation group, CSIR-CSMCRI for valuable suggestions in improve the manuscript and support in field cultivation work. The authors would also like to thank Dr. N. Chidambaranathan, M. Pharm. Ph.D., Vice Principal, K.M. College of Pharmacy, Uthangudi, Madurai, for giving permission to carry out the research in their institution. The contribution has CSIR-CSMCRI PRIS registration number 093/2015.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Cyriac, B., Eswaran, K. Anti- hyperglycemic effect of aqueous extract of Kappaphycus alvarezii (Doty) Doty ex. P. Silva in alloxan-induced diabetic rats. J Appl Phycol 28, 2507–2513 (2016). https://doi.org/10.1007/s10811-015-0762-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-015-0762-7