Evaluation of Anti-Hyperglycemic and Anti-Hyperlipidemic Activities of Water Kefir as Probiotic on Streptozotocin-Induced Diabetic Wistar Rats

Abstract

Diabetes mellitus is a predominant chronic disease which causes mortality of millions of people yearly. Its prevalence is on the rise worldwide. Water kefir is fermented food produced by a matrix of polysaccharides containing bacteria and yeasts, with therapeutic properties. Our study aimed to evaluate anti-hyperglycemic and anti-hyperlipidemic activities of water kefir on streptozotocin-induced diabetic Wistar rats. Adult Wistar rats were made diabetic by intraperitoneal injection of streptozotocin, and were given or not kefir in drinking water for 5 weeks. Body weight, glucose and lipid levels were measured. The results demonstrated evident improvement in body weight, glucose, and lipid profiles of treated rats comparing with diabetic or control rats. Water kefir is found to be less cost hypoglycemic and hypolipidimic treatment and less time consuming. Water kefir can potentially be useful food for diabetes to control glucose and lipid levels.

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Alsayadi, M. , Jawfi, Y. , Belarbi, M. , Soualem-Mami, Z. , Merzouk, H. , Sari, D. , Sabri, F. and Ghalim, M. (2014) Evaluation of Anti-Hyperglycemic and Anti-Hyperlipidemic Activities of Water Kefir as Probiotic on Streptozotocin-Induced Diabetic Wistar Rats. Journal of Diabetes Mellitus, 4, 85-95. doi: 10.4236/jdm.2014.42015.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Anderson, l., Dibble, M.V., Turkki, P.R., Mitchell, H.S. and Rynbergen, H.J. (1982) Nutrition in Health and Disease. 17th Edition, J.B. Lippincoott Company, East Washington, Philadelphia.
[2] WHO (1999) Definition, Diagnosis and Classification of Diabetes Mellitus and its Complications Report of a WHO Consultation Part 1: Diagnosis and Classification of Diabetes Mellitus. World Health Organization, Department of Noncommunicable Disease Surveillance, Geneva.
[3] Singh, S.K., Rai, P.K., Jaiswal, D. and Watal, G. (2008) Evidence-Based Critical Evaluation of Glycemic Potential of Cynodon dactylon. Evidence-Based Complementary and Alternative Medicine, 5, 415-420.
http://dx.doi.org/10.1093/ecam/nem044
[4] National Diabetes Data Group (1979) Classification and Diagnosis of Diabetes Mellitus and Other Categories of Glucose Intolerance. Diabetes, 28, 1039-1057.
[5] Shaw, J.E., Sicree, R.A. and Zimmet, P.Z. (2010) Global Estimates of the Prevalence of Diabetes for 2010 and 2030. Diabetes Research and Clinical Practice, 34, 4-14.
[6] Girach, A., Manner, D. and Porta, M. (2006) Diabetic Microvascular Complications: Can Patients at Risk Be Identified? A Review. International Journal of Clinical Practice, 60, 1471-1483.
http://dx.doi.org/10.1111/j.1742-1241.2006.01175.x
[7] Aski Basavaraj, S., Devarnavadagi, B.B., Rudrappa, G. and Kashinath, R.T. (2012) Influence of Anti Diabetic Therapy on Plasma Lipid Profile and its Relation to Erythrocyte Membrane Lipid Levels in Type 2 Diabetic Subjects. Global Journal of Medical Research, 12, 1-9.
[8] Haffner, S.M., Lehto, S., Ronnemaa, T., Pyrala, K. and Laakso, M. (1998) Mortality from Coronary Heart Disease in Subjects with Type 2 Diabetes and in Nondiabetic Subjects with and without Prior Myocardial Infarction. The New England Journal of Medicine, 339, 229-234. http://dx.doi.org/10.1056/NEJM199807233390404
[9] De Ferranti, S. and Mozaffarian, D. (2008) The Perfect Storm: Obesity, Adipocyte Dysfunction, and Metabolic Consequences. Clinical Chemistry, 54, 945-955. http://dx.doi.org/10.1373/clinchem.2007.100156
[10] Betteridge, D.J. (1994) Diabetic Dyslipidemia. American Journal of Medicine, 96, S25-S31.
http://dx.doi.org/10.1016/0002-9343(94)90228-3
[11] Mayes, P.A. and Botham, K.M. (2009) Lipid Transport and Storage. In: Murray, R.K., Bender, D.A, Botham, K.M., Kennelly, P.J., Rodwell, V.W. and Anthony, W.P., Eds., Harper’s Illustrated Biochemistry, 28th Edition, The McGraw-Hill Companies, Inc., New York, 205-218.
[12] Hayden, J.M. and Reaven, P.S. (2000) Cardiovascular Disease in Diabetes Mellitus Type 2: A Potential Role for Novel Cardio-Vascular Risk Factors. Current Opinion in Lipidology, 11, 519-528.
http://dx.doi.org/10.1097/00041433-200010000-00010
[13] Bener, A., Zirie, M. and Al-Rikkabi, R. (2005) Genetics, Obesity and Environmental Risk Factors Associated with Type 2 Diabetes. Croatian Medical Journal, 46, 302-307.
[14] Maher, V.M. and Brown, B.G. (2000) Lipoprotein(a) and Coronary Heart Disease. Current Opinion in Lipidology, 6, 226-235.
[15] Smaoui, M., Hammami, S., Chaaba, R., Attia, N., Ben Hamda, K., Masmoudi, A.S., Mahjoub, S., Bousslama, A., Ben Ferhat, M. and Hammami, M. (2004) Lipids and Lipoprotein(a) Concentrations in Tunisian Type 2 Diabetic Patients Relationship to Glycemic Control and Coronary Heart Disease. Journal of Diabetes and its Complications, 18, 258-263.
http://dx.doi.org/10.1016/S1056-8727(03)00075-8
[16] Schlitt, A., Blankenberg, S., Bickel, C., Meyer, J., Hafner, G., Jiang, X.C. and Rupprecht, H.J. (2005) Prognostic Value of Lipo-Proteins and Their Relation to Inflammatory Markers among Patients with Coronary Artery Disease. International Journal of Cardiology, 102, 477-485. http://dx.doi.org/10.1016/j.ijcard.2004.05.056
[17] Tseng, C.H. (2004) Lipoprotein(a) Is an Independent Risk Factor for Peripheral Arterial Disease in Chinese Type 2 Diabetic Patients in Taiwan. Diabetes Care, 27, 517-521. http://dx.doi.org/10.2337/diacare.27.2.517
[18] Bazzano, L.A., Serdula, M.K. and Liu, S. (2003) Dietary Intake of Fruits and Vegetables and Risk of Cardiovascular Disease. Current Atherosclerosis Reports, 5, 492-499. http://dx.doi.org/10.1007/s11883-003-0040-z
[19] Daar, A.S., Singer, P.A., Persad, D.L., Pramming, S.K., Matthews, D.R., Beaglehole, R., et al. (2007) Grand Challenges in Chronic Non-Communicable Diseases. Nature, 450, 494-496. http://dx.doi.org/10.1038/450494a
[20] Apostolidis, E., Kwon, Y.I. and Shetty, K. (2007) Inhibitory Potential of Herb, Fruit, and Fungal-Enriched Cheese against Key Enzymes Linked to Type 2 Diabetes and Hypertension. Innovative Food Science and Emerging Technologies, 8, 46-54. http://dx.doi.org/10.1016/j.ifset.2006.06.001
[21] Dae, Y.K., Daily, J.W., Hyun, J.K. and Park, S. (2010) Antidiabetic Effects of Fermented Soybean Products on Type 2 Diabetes. Nutrition Research, 30, 1-13. http://dx.doi.org/10.1016/j.nutres.2009.11.004
[22] Kong, K. (2009) Effects of Kefirs on Glycemic, Insulinemic and Satiety Responses. Graduate Theses and Dissertations, Paper 10310, Iowa State University, Ames.
[23] Maeda, H., Zhu, X., and Mitsuoka, T. (2004) Effects of an Exopolysaccharide (Kefiran) from Lactobacillus Kefiranfaciens on Blood Glucose inKKAy Mice and Constipation in SD Rats Induced by a Low-Fiber Diet. Bioscience and Microflora, 23, 149-153.
[24] Honda, K., Moto, M., Uchida, N., He, F. and Hashizume, N. (2011) Anti-Diabetic of Lactic Acid Bacteriain Normal and Type 2 Diabetic Mice. Journal of Clinical Biochemistry and Nutrition, 51, 96-101.
[25] Matsuzaki, T., Yamazaki, R., Hashimoto, S. and Yokokura, T. (1997) Antidiabetic Effects of an Oral Administration of Lactobacillus casei in a Non-Insulin-Dependent Diabetes Mellitus (NIDDM) Model Using KK-Ay Mice. Endocrine Journal, 44, 357-365. http://dx.doi.org/10.1507/endocrj.44.357
[26] Yadav, H., Jain, S. and Sinhá, P.R. (2007) Antidiabetic Effect of Probiotic Dahi Containing Lactobacillus acidophilus and Lactobacillus casei in High Fructose Fed Rats. Nutrition, 23, 62-68. http://dx.doi.org/10.1016/j.nut.2006.09.002
[27] Yadav, H., Jain, S. and Sinha, P.R. (2008) Oral Administration of Dahi Containing Probiotic Lactobacillus acidophilus and Lactobacillus casei Delayed the Progression of Streptozotocin-Induced Diabetes in Rats. The Journal of Dairy Research, 75, 189-195. http://dx.doi.org/10.1017/S0022029908003129
[28] Ma, X., Hua, J. and Li, Z. (2008) Probiotics Improve High Fat Diet-Induced Hepatic Steatosis and Insulin Resistance by Increasing Hepatic NKT Cells. Journal of Hepatology, 49, 821-830. http://dx.doi.org/10.1016/j.jhep.2008.05.025
[29] Lim, S.-I. and Lee, B.-Y. (2010) Anti-Diabetic Effect of Material Fermented Using Rice Bran and Soybean as the Main Ingredient by Bacillus sp. Journal of the Korean Society for Applied Biological Chemistry, 53, 222-229.
http://dx.doi.org/10.3839/jksabc.2010.035
[30] laleye, S.A., igbakin, A.P. and Akinyanju, J.A. (2008) Antidiabetic Effects of Nono (A Nigerian Fermented Milk) on Alloxan-Induced Diabetic Rats. American Journal of Food Technology, 3, 394-398.
[31] Honda, K., Moto, M., Uchida, N., He, F. and Hashizume, N. (2012) Anti-Diabetic Effects of Lactic Acid Bacteria in Normal and Type 2 Diabetic Mice. Journal of Clinical Biochemistry and Nutrition, 2, 96-101.
[32] Vikram, M.V. (2004) Fermented Liquid Milk Products. In: Hui, Y.H., Meunier-Goddik, L., Josephsen, J., Nip, W.-K. and Stanfield, P.S., Eds., Handbook of Food and Beverage Fermentation Technology, Marcel Dekker, Inc., New York, 1-16.
[33] Gilliland, S.E. (1990) Health and Nutritional Benefits from Lactic Acid Bacteria. FEMS Microbiology Reviews, 87, 175-188. http://dx.doi.org/10.1111/j.1574-6968.1990.tb04887.x
[34] Farnworth, E.R. (2005) Kefir—A Complex Probiotic. Food Science and Technology Bulletin: Functional Foods, 2, 1-17.
[35] Farnworth, E.R. and Mainville, I. (2008) Kefir—A Femented Milk Product. In: Farnworth, E.R., Ed., Handbook of Fermented Functional Foods. 2nd Edition, Taylor & Francis Group, LLC, New York, 89-127.
[36] Hallé, C., Leroi, F., Dousset, X. and Pidoux, M. (1994) Les kéfirs: Des associations bactéries lactiques-levures. In: Bactéries Lactiques: Aspects Fondamentaux et Technologiques, Lorica, Uriage, 169-182.
[37] Harta, O., Iconomopoulou, M., Bekatorou, A., Nigam, P., Kontominas, M. and Koutinas, A. (2004) Effect of Various Carbohydrate Substrates on the Production of Kefir Grains for Use as a Novel Baking Starter. Food Chemistry, 88, 237-242. http://dx.doi.org/10.1016/j.foodchem.2003.12.043
[38] Bergmann, R.S., Pereira, M.A. and Veiga, S.M. (2010) Microbial Profile of a Kefir Sample Preparations: Grains in Natural and Lyophilized and Fermented Suspension. Food Science and Technology (Campinas), 30, 1022-1026.
[39] Papapostolou, H., Bosnea, L.A., Koutinas, A.A. and Kanellaki, M. (2008) Fermentation Efficiency of Thermally Dried Kefir. Bioresource Technology, 15, 6949-6956. http://dx.doi.org/10.1016/j.biortech.2008.01.026
[40] Chen, T.-H., Wang, S.-Y., Chen, K.-N., Liu, J.-R. and Chen, M.J. (2009) Microbiological and Chemical Properties of Kefir Manufactured by Entrapped Microorganisms Isolated from Kefir Grains. Journal of Dairy Science, 92, 3002-3013. http://dx.doi.org/10.3168/jds.2008-1669
[41] Magalhães, K.T. and Pereira, G.D. (2010) Microbial Communities and Chemical Changes during Fermentation of Sugary Brazilian Kefir. World Journal of Microbiology and Biotechnology, 26, 1241-1250.
[42] Pidoux, M. (1989) The Microbial Flora of Sugary Kefir Grain (The Gingerbeer Plant): Biosynthesis of the Grain from Lactobacillus hilgardii Producing a Polysaccharide Gel. MIRCEN Journal of Applied Microbiology and Biotechnology, 5, 223-238. http://dx.doi.org/10.1007/BF01741847
[43] Waldherr, F.W., Doll, V.M., Meißner, D. and Vogel, R.F. (2010) Identification and Characterization of a Glucan-Producing Enzyme from Lactobacillus hilgardii TMW 1.828 Involved in Granule Formation of Water Kefir. Food Microbiology, 27, 672-678.
[44] Gulitz, A., Stadie, J., Wenning, M., Ehrmann, M.A. and Vogel, R.F. (2011) The Microbial Diversity of Water Kefir. International Journal of Food Microbiology, 151, 284-288. http://dx.doi.org/10.1016/j.ijfoodmicro.2011.09.016
[45] Miguel, M.G. da C.P., Cardoso, P.G., Magalhães, K.T. and Schwan, R.F. (2011) Profile of Microbial Communities Present in Tibico (Sugary Kefir) Grains from Different Brazilian States. World Journal of Microbiology and Biotechnology, 27, 1875-1884.
[46] Galli, A., Fiori, E., Pagani, M.A. and Ottogalli, G. (1995) Composizionemicrobiologica e chimicadeigranuli di Kefir “di frutta”. Annali di Microbiologia ed Enzimologia, 45, 85-95.
[47] Garrote, G.L., Abraham, A.G. and De Antoni, G.L. (2001) Chemical and Microbiological Characterization of Kefir Grains. Journal of Dairy Research, 68, 639-652. http://dx.doi.org/10.1017/S0022029901005210
[48] Franzetti, L., Galli, A., Pagani, M.A. and de Noni, I. (1998) Microbiological and Chemical Investigations on “Sugar Kefir” Drink. Annali di Microbiologia ed Enzimologia, 48, 67-80.
[49] Reeves, P.G., Nielsen, F.H. and Fahey, G.C. (1993) AIN-93 Purified Diets for Laboratory Rodents: Final Report of the American Institute of Nutrition Ad Hoc Writing Committee on the Reformulation of the AIN-76A Rodent Diet. The Journal of Nutrition, 123, 1939-1951.
[50] SAS (2001) SAS 9.1 Software Package. SAS Institute, Cary.
[51] Latner, A. (1958) Clinical Biochemistry. Saunders, Philadelphia.
[52] Takeshita, F., Kodama, M., Yamamoto, H., Ikarashi, Y., Ueda, S., Teratani, T., Yamamoto, Y., Tamatani, T., Kanegasaki, S., Ochiya, T. and Quinn, G. (2006) Streptozotocin-Induced Partial Beta Cell Depletion in Nude Mice without Hyperglycaemia Induces Pancreatic Morphogenesis in Transplanted Embryonic Stem Cells. Diabetologia, 49, 2948-2958. http://dx.doi.org/10.1007/s00125-006-0432-z
[53] Hayashi, K., Kojima, R. and Ito, M. (2006) Strain Differences in the Diabetogenic Activity of Streptozotocin in Mice. Biological & Pharmaceutical Bulletin, 29, 1110-1119. http://dx.doi.org/10.1248/bpb.29.1110
[54] Chen, V. and Ianuzzo, C.D. (1982) Doasge Effect of Streptozotocin on Rat Tissue Enzyme Activities and Glycogen Concentration. Canadian Journal of Physiology and Pharmacology, 60, 1251-1256. http://dx.doi.org/10.1139/y82-183
[55] Rajkumar, L., Srinivasan, N., Balasubramanian, K. and Govindarajulu, P. (1991) Increased Degradation of Dermal Collagen in Diabetic Rats. Indian Journal of Experimental Biology, 29, 1081-1083.
[56] Murray, R.K., Bender, D.A., Botham, K.M., Kennelly, P.J., Rodwell, V.W. and Anthony, W.P. (2009) Harper’s Illustrated Biochemistry. 28th Edition, The McGraw-Hill Companies, Inc., China.
[57] Judiono, Djokomoeljanto, R. and Hadisaputro, S. (2012) Biomolecular Aspects of Plain Kefir Antidiabetic Potentials. International Journal of Food, Nutrition & Public Health, 5, 7-23.
[58] Kim, D.H., Yang, B.K., Jeong, S.C., Hur, N.J., Das, S., Yun, J., et al. (2001) A Preliminary Study on the Hypoglycemic Effect of the Exo-Polymers Produced by Five Different Medicinal Mushrooms. Journal of Microbiology and Biotechnology, 11, 167-171.
[59] Hwang, H.-J., Kim, S.-W., Lim, J.-M., Joo, J.-H., Kim, H.-O., Kim, H.-M., et al. (2005) Hypoglycemic Effect of Crude Exopolysaccharides Produced by a Medicinal Mushroom Phellinus baumii in Streptozotocin-Induced Diabetic Rats. Life Sciences, 76, 3069-3080. http://dx.doi.org/10.1016/j.lfs.2004.12.019
[60] Peter, M.A. and Kathleen, B.M. (2009) Cholesterol Synthesis, Transport, & Excretion. In: Murray, R.K., Bender, D.A, Botham, K.M., Kennelly, P.J., Rodwell, V.W. and Anthony, W.P., Eds., Harper’s Illustrated Biochemistry, 28th Edition, The McGraw-Hill Companies, Inc., New York, 219-230.
[61] Sharma, S.R., Dwivedi, S.K. and Swarup, D. (1996) Hypoglycemic and Hypolipidaemic Effects of Cinnamomum tomala nees Leaves. Indian Journal of Experimental Biology, 34, 372-374.
[62] Pushparaj, P., Tan, C.H., and Tan, B.K. (2000) Effects of Averrhoa bilimli Leaf Extract on Blood Glucose and Lipids in Streptozotocin Diabetic Rats. Journal of Ethnopharmacolgy, 72, 69-76.
http://dx.doi.org/10.1016/S0378-8741(00)00200-2
[63] Donath, M.Y., Marianne B.-S., Helga, E. and Jan, A.E. (2009) Islet Inflammation Impairs the Pancreatic Beta-Cell in Type 2 Diabetes. Physiology, 24, 325-331. http://dx.doi.org/10.1152/physiol.00032.2009
[64] Hariom, Y., Shalini, J. and Sinha, P.R. (2007) Antidiabetic Effect of Probiotic Dahi Containing Lactobacillus acidophilus and Lactobacillus casei in High Fructose Fed Rats. Nutrition, 23, 62-68.
http://dx.doi.org/10.1016/j.nut.2006.09.002
[65] Wu, C., lin, H., Wu, G., Wang, S. and Tsai, G. (2011) In Vitro Investigation of the Hypoglycemic Activity of Yeasts Using Models of Rat Epididymal Adipocyte and Differentiated Mouse 3T3-L1 Adipocyte. African Journal of Biotechnology, 35, 6773-6783.
[66] Mitra, S.K., Gopumadhavan, S., Muralidhar, T.S., Anturlika, S. and Sujatha, M.B. (1995) Effect of D-400, a Herbomineral Preparation on Lipid Profile, Glycated Hemoglobin and Glucose Tolerance in Streptozotocin Induced Diabetes in Rats. Indian Journal of Experimental Biology, 33, 798-800.
[67] El khamisy, A.E. (2010) Effect of Bifidobacterium and Lactobacillus acidophilus in Diabetic Rats. Proceedings of the 5th Arab and 2nd International Annual Scientific Conference on Recent Trends of Developing Institutional and Academic Performance in Higher Specific Education Institutions in Egypt and Arab World, Mansoura, 14-15 April 2010, 2426-2439.

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