Hypoglycemic Activity of Water Soluble Polysaccharides of Yam (Dioscorea hispida Dents) Prepared by Aqueous, Papain, and Tempeh Inoculum Assisted Extractions

Authors: Teti Estiasih, Harijono, Weny Bekti Sunarharum, Atina Rahmawati

Abstract:

This research studied the hypoglycemic effect of water soluble polysaccharide (WSP) extracted from yam (Dioscorea hispida) tuber by three different methods: aqueous extraction, papain assisted extraction, and tempeh inoculums assisted extraction. The two later extraction methods were aimed to remove WSP binding protein to have more pure WSP. The hypoglycemic activities were evaluated by means in vivo test on alloxan induced hyperglycemic rats, glucose response test (GRT), in situ glucose absorption test using everted sac, and short chain fatty acids (SCFAs) analysis. All yam WSP extracts exhibited ability to decrease blood glucose level in hyperglycemia condition as well as inhibited glucose absorption and SCFA formation. The order of hypoglycemic activity was tempeh inoculums assisted- >papain assisted- >aqueous WSP extracts. GRT and in situ glucose absorption test showed that order of inhibition was papain assisted- >tempeh inoculums assisted- >aqueous WSP extracts. Digesta of caecum of yam WSP extracts oral fed rats had more SCFA than control. Tempeh inoculums assisted WSP extract exhibited the most significant hypoglycemic activity.

Keywords: hypoglycemic activity, papain, tempeh inoculums, water soluble polysaccharides, yam (Discorea hispida)

Digital Object Identifier (DOI): doi.org/10.5281/zenodo.1078376

References:

[1] T. Myoda, Y. Matsuda, T. Suzuki, T. Nakagawa, T. Nagai, and T. Nagashima, "Identification of soluble proteins and interaction with mannan in mucilage of Dioscorea opposite Thunb. (Chinese yam tuber)", Food Sci Technol Res, vol. 12, no. 4, pp 299-302, 2006.
[2] C.W. Hou, M.H Lee, H.J. Chen, W.L. Liang, C.H. Han, Y.W. Liu, and Y.H. Lin, "Antioxidant activities of dioscorin, the storage protein of yam (Dioscorea batatas Decne) tuber", J Agric Food Chem, vol. 49, pp 4956-4960, 2001.
[3] Y.W. Liu, H.F. Shang, C.K. Wang, F.L. Hsu, and W.C Hou, "Immunomodulatory activity of dioscorin, the storage protein of yam (Dioscorea alata cv. Tainong no.1) tuber", Food and Chem Toxicol, vol. 45, pp 2312-2318, 2007.
[4] Y.C. Chan, C.K. Hsu, M.F. Wang, J.W. Liao, and T.Y. Su, "Beneficial effect of yam on the amyloid β-protein, monoamine oxidase B and cognitive deficit in mice with accelerated senescence", J Sci Food Agric, vol. 86, pp 1517-1525, 2006
[5] S.T. Chou, B.H. Chiang, Y.C. Chung, P.C. Chen, and C.K. Hsu, "Effects of storage temperatures on the antioxidative activity and composition of yam", Food Chem, vol. 98, pp 618-623, 2006.
[6] L. Braun, "Wild yam Dioscorea sp. Complementary Medicine", vol. 7, no. 2, pp 40-42, 2008.
[7] D.J. Yang and J.T. Lin, "Effects of different storage conditions on steroidal saponins in yam (Dioscorea pseudojaponica Yamamoto) tubers", Food Chem, vol. 110, pp 670-677, 2008.
[8] Y.M. Liu, and K.W. Lin, "Antioxidative ability, dioscorin stability, and the quality of yam chips from various yam species as affected by processing method", J Food Sci, vol. 74, no. 2, pp C118-C125, 2009.
[9] F.H. Hsu, Y.H. Lin, M.H. Lee, C.L. Lin, and W.C. Hou, "Both dioscorin, the tuber storage protein of yam (Dioscorea alata cv. Tainong No. 1), and its peptic hydrolysates exhibited angiotensin converting enzyme inhibitory activities", J Agric Food Chem, vol. 50, no. 21, pp 6109-6113, 2002.
[10] D.T. Zava, C.M. Dollbaum, and M. Blen, M. "Estrogen and progestin bioactivity of foods, herbs, and spices", Proc. Soc. Exp. Biol. Med., vol. 217, pp 369-378, 1998.
[11] Y. Fu, L.A. Ferng, and P. Huang, "Quantitative analysis of allantoin and allantoic acid in yam tuber, mucilage, skin and bulbil of the Dioscorea species", Food Chem, vol. 94, pp 541-549, 2006.
[12] Y. Ohizumi, M. Gaidamashvili, S. Ohwada, K. Matsuda, J. Kominami, N. Sachiko, J. Hirabayashi, T. Naganuma, T. Ogawa, and K. Muramoto, "Mannose-binding lectin from yam (Dioscorea batatas) tubers with insecticidal properties against Helicoverpa armigera (Lepidoptera: Noctuidae)", J Agric Food Chem, vol. 57, pp 2896-2902, 2009.
[13] M. Tsukui, T. Nagashima, H. Sato, and T. Kozima, "Electrophoretic analysis of glycoprotein from yam (Dioscorea opposite Thunb.) mucilage", J Food Preservation Sci, vol. 25, pp 283-286, 1999a.
[14] M. Tsukui, T. Nagashima, H. Sato, T. Kozima, and W. Tanimura, "Characterization of yam (Dioscorea opposita Thunb.) mucilage and polysaccharide with different varieties", J Jpn Soc Food Sci Technol, vol. 46, pp 575-580, 1999b.
[15] Wu RT, "Polysaccharide extract of Dioscorea sp and an orally active pharmaceutical composition comprising the same", Patent US 20050196479A1, 2005.
[16] Y. Uno, S. Hashidume, O. Kurita, T. Fujiwara, and K. Nomura, "Dioscorea opposite Thunb. a mannosiadse belongs to the glycosyl hydrolase family 38", Acta Physiologiae Plantarum, vol. 32, pp 713- 718, 2010.
[17] M.O. Weickert and A.F.H. Pfeiffer, "Metabolic effects of dietary fiber consumptionand prevention of diabetes", J Nutr, vol. 138, pp 439-442, 2008.
[18] J. Lunn and J.L. Buttriss, "Carbohydrates and dietary fibre", Nutrition Bulletin, vol. 32, pp 21-64, 2007.
[19] C.A. Edwards and I.R. Rowland, "Bacterial fermentation in the colon and its measurement. In: Schweizer TF, Edwards CA, eds. Dietary fibrea component of food. Nutritional function in health and disease. London: Springer-Verlag, 119-50, 1992.
[20] P.G. Reeves, F.H. Nilson, and G.C. Fahey, "Purified diet for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of AIN-76 a rodent diet", J Nutr, vol. 123, pp 1939-1951, 1993.
[21] Harijono, T. Estiasih, and W.B. Sunarharum, "Bioactive polysaccharides extraction of gadung and gembili and their capability for diabetic therapy and reducing cholesterol", Report of National Priority Competitive Research Grant Batch I. Research Center, University of Brawijaya, Malang, Indonesia, 2009.
[22] AOAC
[Association of official Analytical Chemist], "Official Methods of Analysis. Association of Official Analytical Chemists.AOAC, Washington DC, USA, 1990.
[23] A. Ruzaidi, A. Maleyki, I. Amin, A.G. Nawalyah, H. Muhajir, M.B.S.M.J. Pauliena, and M.S. Muskinah MS, "Hypoglycaemic properties of Malaysian cocoa (Theobroma Cacao) polyphenols-rich extract", International Food Research Journal, vol. 15, no. 3, pp 305- 312, 2008.
[24] Y. Zhao, Y.O. Son, S.S. Kim, Y.S. Jang, and J.C. Lee, "Antioxidant and anti-hyperglycemic activity of polysaccharide isolated from Dendrobium chrysotoxum Lindl", J of Biochemistry and Molecular Biology, vol. 40, no. 5, pp 670-677, 2007.
[25] J.T. Xie, J.A. Wu, S. Mehendale, H.H. Aung, and C.S. Yuan "Antihyperglycemic effect of the polysaccharides fraction from American ginseng berry extract in ob/ob mice", Phytomedicine, vol. 11, pp 182- 187, 2004.
[26] Harijono, T. Estiasih, W.B. Sunarharum, and I.K. Suwita, "Hypoglycaemic effect of water soluble polysaccharides extracted from gembili (Dioscorea esculenta) by various methods", J Teknol dan Industri Pangan, vol. XXIII, no. 1, pp 1-8, 2012.
[27] C.K. Riley, A.O. Wheatly, and H.N. Asemota, "Physicochemical characterization of starches from Jamaican yams (Dioscorea spp.): potential for pharmaceutical exploitations", Eur J Sci Res, vol. 15, no. 2, pp 207-219, 2006.
[28] D. Sumangat, B.S. Sembiring, and C. Winarti, "Bioconvetion of cashew nut fruits into microbial protein concentrate. Buletin TRO, vol. 14, no. 2, pp 1-8, 2003.
[29] A. Susilowati, Aspiyanto, S. Moerniati, and Y. Maryati, "Potency of amino acids as savory fraction from vegetable broth of mung beans (Phaseolus radiatus l.) through brine fermentation by Rhizopus-C1", Indo J Chem, vol. 9, no. 2, pp 339-346, 2009.
[30] G.A. Youssef, "Physiological studies of cellulase complex enzymes of Aspergillus oryzae and characterization of carboxymethyl cellulase", African J Microbiol Res, vol. 5, no.11, pp 1311-1321, 2011.
[31] G. Chiang, W.Q. Lu, X.S. Piao, J.K. Hu, L.M. Gong, and P.A. Tracker, "Beneficial effects of Rhizopus oligosporus fermentation on reduction of glucosinolates, fibre and phytic acid in rapeseed (Brassica napus) Meal", Asian-Aust J of Anim Sci vol. 23, no. 2, pp 263-271, 2010.
[32] K.O. Shin, J.R. Jeon, J.S. Lee, J.Y. Kim, C.H. Lee, S.D. Kim, Y.S. Yu, and D.H. Nam, "Lactic acid fermentation of Chinese yam (Dioscorea batatas Decne) flour and its pharmacological effect on gastrointestinal function in rat model", Biotechnol and Bioprocess Eng, vol. 11, no. 3, pp 240-244, 2006.
[33] T. Kiho, M. Kochi, S. Usui, K. Hirano, K. Aizawa, and T. Inakum, "Antidiabetic effect of an acidic polysaccharide (TAP) from Tremella aurantia and its degradation product (TAP-H). Biol Pharm Bull, vol. 24, no. 12, pp 1400-1403, 2001.
[34] A. Mortensen, S.E. Kulling, H. Schwartz, I. Rowland, C.E. Ruefer, G. Rimbach, A. Cassidy, P. Magee, J. Millar, W.L. Hall, F.B. Birkved, I.K. Sorensen, AND G. Sontag, "Analytical and compositional aspects of isoflavones in food and their biological effects", Mol Nutr Food Res, vol 53, 2009.
[35] J. Ni├▒o, D.A. Jiménez, O.M. Mosquera, AND Y.M. Correa", "Diosgenin quantification by HPLC in a Dioscorea polygonoidestuber collection from Colombian flora", J Braz Chem Soc, vol 18, no. 5, pp 1073-1076, 2007.
[36] Al-Habori and A. Raman, "Antidiabetic and hypocholesterolaemic effects of fenugreek", Phytother Res, vol. 12, pp 233-242, 1998.
[37] C.L. Lee, H.K. Hung, J.J. Wang, and T.M. Pan, "Improving the ratio of monacolin K to citrinin production of Monascus purpureus NTU 568 under Dioscorea medium through the mediation of pH value and ethanol addition", J Agric Food Chem., vol. 16, pp 6493-6502, 2007.
[38] P. McCue, Y.I. Kwon, and K. Shetty, "Anti-diabetic and antihypertensive potential of sprouted and solid-state bioprocessed soybean", Asia Pac J Clin Nutr, vol. 14, no. 2, pp 145-152, 2005.
[39] S. Chearskul, S. Sangurai, W. Nitiyanant, W. Kriengsinyos, S. Kooptiwut, and T. Harindhanavudhi, "Glycemic and lipid responses to glucomannan in Thais with type 2 diabetes mellitus", J Med Assoc Thai, vol 90, no. 10, pp 2150-2156, 2007.
[40] V. Vuksan, D.J. Jenkins, P. Spadafora, J.L. Sievenpiper, R. Owen, E. Vidgen, F. Brighenti, R. Josse, L.A. Leiter, and C. Bruce-Thompson, "Konjac-mannan (glucomannan) improves glycemia and other associated risk factors for coronary heart disease in type 2 diabetes. A randomized controlled metabolic trial", Diabetes Care, vol. 22, no. 6, pp 913-919, 1999.
[41] M. Madar, M. Nir, N. Trostler, and C. Norenberg, "Effects of cottonseed dietary fiber on metabolic parameters in diabetic rats and non-insulindependent diabetic humans", J Nutr, vol. 118, pp 1143 -1148, 1988.
[42] K. Marsman and M. McBurney, "Dietary fiber and short-chain fatty acids affect cell proliferation and protein synthesis in isolated rat colonocytes", J Nutr, vol.126, pp 1429-1437, 1996.
[43] S. Robert, J.J. Matte, C. Farmer, C.L. Girard, and G.P. Martineau, "High-fibre diets for sows: effects on stereotypes and adjunctive drinking", Appl. Anim. Behav. Sci., vol. 37, pp 297-309, 1993.
[44] J.M. Campbell, G.C. Fahey Jr, and B.R. Wolf, "Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats", J Nutr, vol. 127, pp 130-136, 1997.
[45] A.M. Henningsson, I,M.E. Bjorck, and E.M.G.L. Nyman, "Combinations of indigestible carbohydrates affect short-chain fatty acid formation in the hindgut of rats" J. Nutr, vol.132, pp 3098-3104, 2002.
[46] J.H. Cummings and G.T. Macfarlane, "The control and consequences of bacterial fermentation in the human colon", J. Appl. Bacteriol, Vol. 70, pp 443-459, 1991.
[47] W. Scheppach, "Effects of short chain fatty acids on gut morphology and function" Gut, vol. 35 pp S35-S38, 1994.
[48] S. Albrecht, S.G.J. van Muiswinkel, H.A. Schols, A.G.J. Voragen, and H.Gruppen H, "Introducing capillary electrophoresis with laser-induced fluorescence detection (CE-LIF) for the characterization of konjac glucomannan oligosaccharides and their in vitro fermentation behavior", J. Agric. Food Chem, vol. 57, no. 9, pp 3867-3876, 2009.
[49] H.L. Chen, H.C. Cheng, W.T. Wu, Y.J. Liu, and S.Y. Liu, "Supplementation of konjac glucomannan into a low-fiber chinese diet promoted bowel movement and improved colonic ecology in constipated adults: a placebo-controlled, diet-controlled trial", J Am Coll Nutr, vol. 27, no. 1, pp 102-108, 2008.
[50] G.X. Hu, G.R. Chen, H. Xu, R.S. Ge, and J. Lin, "Activation of the AMP activated protein kinase by short-chain fatty acids is the main mechanism underlying the beneficial effect of a high fiber diet on the metabolic syndrome", Med Hypotheses, vol. 74, no. 1, pp 123-126,