Evaluation of the inhibition of carbohydrate hydrolysing enzymes, antioxidant activity and polyphenolic content of extracts of ten African Ficus species (Moraceae) used traditionally to treat diabetes
Some Ficus species have been used in traditional African medicine in the treatment of diabetes. The antidiabetic potential of certain species has been confirmed in vivo but the mechanism of activity remains uncertain. The aim of this study was to determine the activity and to investigate the mechanism of antidiabetic activity of ten selected Ficus species through inhibition of α-amylase and α-glucosidase activity, and the possible relationship between these activities, the total polyphenolic content and the antioxidant activity.
Dried acetone leaf extracts were reconstituted with appropriate solvents and used to determine total polyphenolic content antioxidant activity, α-amylase and α-glucosidase inhibitory activity.
The crude acetone extract of F. lutea had the highest polyphenolic content (56.85 ± 1.82 mg GAE/g of dry material) and the strongest antioxidant activity with a TEAC value of 4.80 ± 0.90. The antioxidant activity of the acetone extracts of the Ficus species may not be ascribed to total polyphenolic content alone. The crude extract at a concentration of 0.5 mg/ml of F. lutea (64.3 ± 3.6%) had the best α-glucosidase (sucrase) inhibitory activity. The EC50 of F. lutea (290 ± 111 μg/ml) was not significantly different from that of F. sycomorus (217 ± 69 μg/ml). The α-amylase inhibitory activity of F. lutea (95.4 ± 1.2%) at a concentration of 1 mg/ml was the highest among the Ficus species screened. The EC50 for F. lutea (9.42 ± 2.01 μ g/ml), though the highest, was not significantly different (p < 0.05) from that of F. craterostoma and F. natalensis. It was apparent that the crude acetone extract of F. lutea is a partially non-competitive inhibitor of α-amylase and α-glucosidase. Based on correlation coefficients polyphenolics may be responsible for α-glucosidase activity but probably not for α-amylase activity.
Antidiabetic activity potential via inhibition of α-amylase and α-glucosidase was discovered in Ficus lutea which has not been previously reported. The acetone extract of the leaves was high in total polyphenolic content and antioxidant activity, and was a potent inhibitor of α-amylase activity. Research is underway to isolate the active compound(s) responsible for the antidiabetic activity and to confirm the in vitro antidiabetic activity and to investigate in vitro toxicity.
- Anonymous: Definition, diagnosis and classification of diabetes mellitus and its complications. In Part 1: diagnosis and classification of diabetes mellitus. Geneva: Report of a WHO Consultation; 1999.
- Kaneto H, Katakami N, Kawamori D, Miyatsuka T, Sakamota K, Matsuoka T-A, Matsuhisa M, Yamasaki Y: Involvement of oxidative stress in the pathogenesis of diabetes. Antioxid Redox Signal 2007, 9:355–366. CrossRef
- Jung M, Park M, Lee HC, Kang YH, Kang ES, Kim SK: Antidiabetic agents from medicinal plants. Curr Med Chem 2006, 13:1203–1218. CrossRef
- Jain S, Saraf S: Review on Type 2 diabetes mellitus—its global prevalence and therapeutic strategies. Diabetes and Metabolic Syndrome: Clinical Research and Reviews 2010, 4:48–56. CrossRef
- Wild S, Roglic G, Green A, Sicree R, King H: Global prevalence of diabetes Estimates for the year 2000 and projections for 2030. Diabetes Care 2004, 27:1047–1053. CrossRef
- Ogunbodede EO, Fatusi OA, Akintomide A, Kolawole K, Ajayi A: Oral health status in a population of Nigerian diabetics. J Contemp Dent Pract 2005, 6:75–84.
- Deutschländer MS, van de Venter M, Roux S, Louw J, Lall N: Hypoglycaemic activity of four plant extracts traditionally used in South Africa for diabetes. J Ethnopharmacol 2009, 124:619–624. CrossRef
- Johansen JS, Harris AK, Rychly DJ, Ergul A: Oxidative stress and the use of antioxidants in diabetes: Linking basic science to clinical practice. Cardiovasc Diabetol 2005,4(1):5. CrossRef
- Mai TT, Chuyen NV: Anti-hyperglycemic activity of an aqueous extract from flower buds of Cleistocalyx operculatus (Roxb.) Merr and Perry. Biosci Biotechnol Biochem 2007, 71:69–76. CrossRef
- Youn JY, Park HY, Cho KH: Anti-hyperglycemic activity of Commelina communis L: inhibition of alpha-glucosidase. Diabetes Res Clin Pract 2004, 66S:S149-S155. CrossRef
- Kim YM, Jeong YK, Wang MH, Lee WY, Rhee HI: Inhibitory effect of pine extract on alpha-glucosidase activity and postprandial hyperglycemia. Nutrition 2005, 21:756–761. CrossRef
- De Fronzo RA: Pharmacologic therapy for type 2 diabetes mellitus. Ann Intern Med 1999, 131:281–303. CrossRef
- Rhabasa-Lhoret R, Chiasson JL: α-Glucosidase inhibitors. In International Textbook of Diabetes Mellitus, vol. 1. 3rd edition. Edited by: Defronzo RA, Ferrannini E, Keen H, Zimmet P. UK.: John Wiley & Sons Ltd.; 2004:901–914.
- Moller DE: New drug targets for type 2 diabetes and the metabolic syndrome. Nature 2001, 414:821–827. CrossRef
- Serrato A, Ibarra-ManriqueZ G, Oyama K: Biogeography and conservation of the genus Ficus (Moraceae) in Mexico. J Biogeogr 2004, 31:475–485. CrossRef
- Hansson A, Zelada JC, Noriega HP: Re-evaluation of risks with the use of Ficus insipida latex as a traditional anthelmintic remedy in the Amazon. J Ethnopharmacol 2005, 98:251–257. CrossRef
- Koné WM, Atindehou KK, Terreaux C, Hostettmann K, Traoré D, Dosso M: Traditional medicine in North Côte-D’Ivoire: Screening of 50 medicinal plants for antibacterial activity. J Ethnopharmacol 2004, 93:43–49. CrossRef
- Watt JM, Breyer-Brandwijk MG: Medicinal and poisonous plants of Southern and Eastern Africa. London: Livingstone Ltd; 1962:773–780.
- Trivedi P, Hind S, Sharma RC: Preliminary phytochemical and pharmacological studies on Ficus racemosa . J Med Res 1969, 56:1070–1074.
- Ramadan MA, Ahmad AS, Nafady AM, Mansour AI: Chemical composition of the stem bark and leaves of Ficus pandurata Hance. Nat Prod Res 2009, 23:1218–1230. CrossRef
- Andrade-Cetto A, Becerra-Jiménez J, Cárdenas-Vázquez R: Alpha-glucosidase inhibiting activity of some Mexican plants used in the treatment of type 2 diabetes. J Ethnopharmacol 2008, 116:27–32. CrossRef
- Mai TT, Thu NN, Tien PG, Van Chuyen N: Alpha-glucosidase inhibitory and antioxidant activities of Vietnamese edible plants and their relationships with polyphenol contents. J Nutr Sci Vitaminol 2007, 53:267–276. CrossRef
- Singh RK, Mehta S, Jaiswal D, Rai PK, Watal G: Antidiabetic effect of Ficus bengalensis aerial roots in experimental animals. J Ethnopharmacol 2009, 123:110–114. CrossRef
- Perez C, Dominguez E, Ramiro JM, Romero A, Campillo JE, Torres MD: A study on the glycaemic balance in streptozotocin-diabetic rats treated with an aqueous extract of Ficus carica (fig tree) leaves. Phytother Res 1996, 10:82–83. CrossRef
- Rao RB, Murugesan T, Sinha S, Saha BP, Pal M, Mandal SC: Glucose lowering efficacy of Ficus racemosa bark extract in normal and alloxan diabetic rats. Phytother Res 2002, 16:590–592. CrossRef
- Ghosh R, Sharatchandra KH, Rita S, Thokchom IS: Hypoglycaemic activity of Ficus hispida (bark) in normal and diabetic albino rats. Indian J Pharmacol 2004, 36:222–225.
- Kumar KA, Maheshwari MU, Sivashanmugam AT, Devi VS, Prasanth NV, Ravi TK: Hypoglycemic effect of Ficus microcarpa leaves (Chinese banyan) on alloxan- induced diabetic rats. J Biol Scie 2007,7(2):321–326. CrossRef
- Pandit R, Phahke A, Jagtap A: Antidiabetic effects of Ficus religiosa extract in streptozotocin-induced diabetic rats. J Ethnopharmacol 2010, 128:462–466. CrossRef
- Musabayane CT, Gondwe M, Kamadyaapa DR, Chuturgoon AA, Ojewole JAO: Effects of Ficus thonningii (Blume) [Moraceae] stem-bark ethanolic extract on blood glucose, cardiovascular and kidney functions of rats, and on kidney cell lines of the proximal (LLC-PK1) and distal tubules (MDBK). Ren Fail 2007, 29:389–397. CrossRef
- Madubunyi II, Onoja SO, Asuzu IU: In vitro antioxidant and in vivo antidiabetic potential of the methanolic extract of Ficus glumosa Del (Moraceae) stem bark in alloxan-induced diabetic mice. Comp Clin Pathol 2012, 21:389–394. CrossRef
- Mazumder PM, Farswan M, Parcha V: Hypoglycaemic effect of Ficus arnottiana Miq. bark extracts on streptozotocin induced diabetes in rats. Natural Product Radiance 2009, 8:478–482.
- Kar A, Choudhary BK, Bandyopadhyay NG: Comparative evaluation of hypoglycaemic activity of some Indian medicinal plants in alloxan diabetic rats. J Ethnopharmacol 2003, 84:105–108. CrossRef
- Adoum OA, Michael BO, Mohammad IS: Phytochemicals and hypoglycaemic effect of methanol stem-bark extract of Ficus sycomorus Linn (Moraceae) on allozan induced diabetic Wistar albino rats. Afr J Biotechnol 2012,11(17):4095–4097.
- Adam Z, Khamis S, Ismail A, Hamid M: Ficus deltoidea: a potential alternative medicine for diabetes mellitus. Evidence-Based Complementary and Alternative Medicine 2012.
- Brink M: Ficus capreifolia Delile. In [Internet] Record from Protabase. Edited by: Brink M, Achigan-Dako EG. Wageningen, Netherlands: PROTA (Plant Resources of Tropical Africa /Resources végétales de l’Afrique tropicale); 2010.
- Kuete V, Ngameni B, Fotso Simo CC, Tankeu RK, Ngadjui BT, Meyer JJM, Lall N, Kuiate JR: Antimicrobial activity of the crude extract and compounds from Ficus chlamydocarp and Ficus cordata (Moraceae). J Ethnopharmacol 2008, 120:17–24. CrossRef
- Bhat RB, Jacobs TY: Traditional herbal medicine in Transkei. J Ethnopharmacol 1995, 48:7–12. CrossRef
- Hutchings A, Scott AH, Lewis G, Cunningham AB: Zulu medicinal plants. An inventory. Pietermaritzburg: University of Natal Press; 1996:352.
- Marwah RG, Fatope MO, Al Mahrooqi R, Varma GB, Al Abadi H, Al-Burtamani SKS: Antioxidant capacity of some edible and wound healing plants in Oman. Food Chem 2006, 101:465–470. CrossRef
- Chifundera K: Livestock diseases and the traditional medicine in the Bushi area, Kive province, Democratic Republic of Congo. African Study Monographs 1998, 19:13–33.
- Cousins D, Huffman MA: Medicinal properties in the diet of gorillas: an ethno- pharmacological evaluation. African Studies Monographs 2002, 23:65–89.
- Kuete V, Kamga J, Sandjo LP, Ngameni B, Poumale HMP, Ambassa P, Ngadjui BT: Antimicrobial activities of the methanol extract, fractions and compounds from Ficus polita Vahl. (Moraceae). BMC Complement Altern Med 2011, 11:10. 1186/1472–6882–11–6.
- Kirtikar J, Basu B: Ficus religiosa. In Indian Medicinal Plants, vol. 10, 2nd edition. Edited by: Blatter E, Caius J, Mhaskar K. New Delhi: Oriental Enterprises; 2001:3200–3202.
- Simmonds MSJ, Howes MJR: Plants used in the treatment of diabetes. In Traditional medicine for modern times - Antidiabetic Plants, 6th volume. Edited by: Soumyanath A. UK: CRC Press/Taylor and Frances Group; 2006:19–82.
- Lansky EP, Paavilainen HM, Pawlus AD, Newman RA: Ficus spp. (fig): ethnobotany and potential as anticancer and anti-inflammatory agents. J Ethnopharmacol 2008, 119:195–213. CrossRef
- Sandabe UK, Onyeyili PA, Chibuzo GA: Phytochemical screening and effect of aqueous extract of Ficus sycomorus L. (Moraceae) stembark on muscular activity in laboratory animals. J Ethnopharmacol 2006, 104:283–285. CrossRef
- Etuk EU, Bello SO, Isezuo SA, Mohammed BJ: Ethnobotanical survey of medicinal plants used for the treatment of diabetes mellitus in the north western region of Nigeria. Asian J Exp Biol Sci 2010, 1:55–59.
- Kotze M, Eloff JN: Extraction of antibacterial compounds from Combretum microphyllum (Combretaceae). South African J Botany 2002, 66:62–70.
- Eloff JN: Which extractant should be used for the screening and isolation of antimicrobial components from plants? J Ethnopharmacol 1998, 60:1–8. CrossRef
- Ali H, Houghton PJ, Soumyanath A: Alpha-amylase inhibitory activity of some Malaysian plants used to treat diabetes; with particular reference to Phyllanthus amarus . J Ethnopharmacol 2006, 107:449–455. CrossRef
- Djeridane A, Yousfi M, Nadjemi B, Boutassouna D, Stocher P, Vidal N: Antioxidant activity of some Algerian medicinal plants extracts containing phenolic compounds. Food Chem 2006, 97:654–660. CrossRef
- Re-Roberta P, Proteggente N, Pannala A, Yang A, Rice-Evans C: Antioxidant activity applying an improved ABTS radical cation decolourization assay. Free Radic Biol Med 1999, 26:1231–1237. CrossRef
- Oki T, Matsui T, Osajima Y: Inhibitory effect of alpha-glucosidase inhibitor varies according to its origin. Journal of Agriculture and Food Chemistry 1999, 47:550–553. CrossRef
- Bhandari MR, Jong-Anurakkun N, Hong G, Kawabata J: Alpha-glucosidase and α- amylase inhibitory activities of Nepalese medicinal herb Pakhanbhed ( Bergenia ciliata , Haw.). Food Chem 2008, 106:247–252. CrossRef
- Tiwari AK, Rao JM: Diabetes mellitus and multiple therapeutic approaches of phytochemicals: Present status and future prospects. Curr Sci 2002, 83:30–38.
- Lebovitz HE: α-Glucosidase inhibitors as agents in the treatment of diabetes. Diabetes Review 1998, 6:132–145.
- Baron AD: Postprandial hyperglycaemia and alpha-glucosidase inhibitors. Diabetes Res Clin Pract 1998, 40:51–55. CrossRef
- Kim J-S, Kwon C-S, Son K-H: Inhibition of alpha glucosidase and amylase by luteolin, a flavonoid. Biosci Biotechnol Biochem 2000, 64:2458–2461. CrossRef
- McDougall GJ, Shpiro F, Dobson P, Smith P, Blake A, Stewart D: Different polyphenolic components of soft fruits inhibit α-amylase and α-glucosidase. Journal of Agriculture and Food Chemistry 2005, 53:2760–2766. CrossRef
- Ahmed F, Urooj A: Effect of Ficus racemosa stem bark on the activities of carbohydrate hydrolysing enzymes: an in vitro study. Pharm Biol 2010,48(5):518–523. CrossRef
- Ahmed F, Chavan S, Satish A, Punith Kumar R: Inhibitory activities of Ficus benghalensis bark against carbohydrate hydrolysing enzymes- An in vitro study. Pharmacognosy Journal 2011,3(20):33–37. CrossRef
- Farsi E, Shafaei A, Hor SY, Khadeer Ahamed MB, Yam MF, Attitalla IH, Asmawi MZ, Ismail Z: Correlation between enzymes inhibitory effects and antioxidant activities of standardised fractions of methanolic extract obtained from Ficus deltoidea leaves. Afr J Biotechnol 2011,10(67):15184–15194. CrossRef
- Ponnusamy S, Ravindran R, Zinjarde S, Bhargava S, Kumar AR: Evaluation of traditional Indian antidiabetic medicinal plants for human pancreatic amylase inhibitory effect in vitro . Evidence-Based Complementary and Alternative Medicine 2011.
- Tadera K, Minami Y, Takamatsu K, Matsuoka T: Inhibition of α-glucosidase and α- amylase by flavonoids. J Nutr Sci Vitaminol 2006, 52:149–152. CrossRef
- Brown JE, Khodr H, Hider RC, Rice-Evans CA: Structural dependence of flavonoid interactions with Cu2+ ions: implications for their antioxidant properties. Biochem J 1998, 330:1173–1178.
- Carlsen H, Myhrstad MCW, Thoreson M, Moskaug JO, Blomhoff R: Berry intake increases the activity of the gamma-glutamyl cysteine synthetase promoter in transgenic reporter mice. J Nutr 2003, 133:2137–2140.
- Rice-Evans CA, Miller NJ, Paganga G: Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med 1996, 20:933–956. CrossRef
- Pulido R, Bravo L, Saura-Calixto F: Antioxidant activity of dietary polyphenols as determined by a modified ferric reducing/antioxidant power assay. Journal of Agriculture and Food Chemistry 2000, 48:3396–3402. CrossRef
- Abdel-Hameed E-SS: Total phenolic contents and free radical scavenging activity of certain Egyptian Ficus species leaf samples. Food Chem 2009, 114:1271–1277. CrossRef
- Hagerman AE, Riedl KM, Jones GA, Sovik KN, Ritchard NT, Hartzfeld PW, Riechel TL: High molecular weight plant polyphenolics (tannins) as biological antioxidants. Journal of Agriculture and Food Chemistry 1998, 46:1887–1892. CrossRef
- Ivanova D, Gerova D, Chervenkov T, Yankova T: Polyphenols and antioxidant capacity of Bulgarian medicinal plants. J Ethnopharmacol 2005, 96:145–150. CrossRef
- Manian R, Anusuya N, Siddhuraju P, Manian S: The antioxidant activity and free radical scavenging potential of two different solvent extracts of Camellia sinensis (L.) O. Kuntz, Ficus bengalensis L. and Ficus racemosa L. Food Chem 2008, 107:1000–1007. CrossRef
- Dixon M, Webb EC: Enzyme inhibition and activation. In Enzymes. 3rd edition. New York: Academic Press Inc; 1999:332–380. Longman Group Ltd. London
- The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1472-6882/13/94/prepub
- Evaluation of the inhibition of carbohydrate hydrolysing enzymes, antioxidant activity and polyphenolic content of extracts of ten African Ficus species (Moraceae) used traditionally to treat diabetes
- Open Access
- Available under Open Access This content is freely available online to anyone, anywhere at any time.
BMC Complementary and Alternative Medicine
- Online Date
- May 2013
- Online ISSN
- BioMed Central
- Additional Links
- African Ficus species
- Ficus lutea
- α-amylase inhibitory activity
- α- glucosidase inhibitory activity
- Antioxidant activity
- Polyphenol content
- Author Affiliations
- 1. Phytomedicine Programme, Department of Paraclinical Sciences, University of Pretoria, Private Bag X04, Onderstepoort, 0110, South Africa
- 3. Federal Institute of Industrial Research Oshodi (FIIRO), Ikeja, Nigeria
- 2. Biomedical Research Centre, Faculty of Veterinary Sciences, University of Pretoria, Onderstepoort, 0110, South Africa