Fermented Miso with Adzuki Beans or Black Soybeans Decreases Lipid Peroxidation and Serum Cholesterol in Mice fed a High-Fat Diet

Shan Wu^{1, 2}, Shuo Feng^{1, 2}, ZhaoHong Ci¹, Chengyu Jiang¹, Yang Cui¹, Yuki Sasaki¹, Yukina Ota¹ and Michiyuki Kojima^1,

¹Department of Food Production Science, Obihiro University of Agriculture and Veterinary Medicine, 11, Nishi-2-sen, Inada-machi, Obihiro, Hokkaido 080-8555, Japan

²United Graduate School of Agricultural Sciences, Iwate University, 3-18-8, Ueda, Morioka, Iwate 020-8550, Japan

Cite this paper:
Shan Wu, Shuo Feng, ZhaoHong Ci, Chengyu Jiang, Yang Cui, Yuki Sasaki, Yukina Ota and Michiyuki Kojima. Fermented Miso with Adzuki Beans or Black Soybeans Decreases Lipid Peroxidation and Serum Cholesterol in Mice fed a High-Fat Diet. Journal of Food and Nutrition Research. 2015; 3(3):131-137. doi: 10.12691/jfnr-3-3-1

Abstract

The seed coat extracts of adzuki beans and black soybeans have high antioxidant properties, suggesting health-promoting effects. However, there are few data on the activity of fermented adzuki beans or black soybeans in vivo. This study examined the effects of adzuki beans and black soybeans in mice fed a high-fat diet. Adzuki beans and black soybeans were fermented with soybeans and rice koji for 6 months (miso) and compared with similarly fermented soybeans. Adzuki beans and black soybeans demonstrated higher antioxidant activity compared to soybeans, as evidenced by the 2,2-diphenyl-1-picrylhydrazyl (DPPH) assay. In the in vivo experiments, mice were fed for 5 weeks with a high-fat diet supplemented or not with 10% adzuki bean miso, 10% black soybean miso, or 10% soybean miso. Dietary supplementation with adzuki beans and black soybeans significantly decreased serum aspartate transaminase (58.6% and 62.6%, respectively) and lipid peroxidation in the liver (42.8% and 40.8%, respectively) compared to the soybean control group. Furthermore, mice receiving adzuki beans demonstrated a significant decrease in serum cholesterol (31.0%) and increase in fecal bile acid content (40.0%) compared to the soybean-fed mice. These results indicate that dietary supplementation with adzuki beans and black soybeans characterized with high antioxidant activity may exert health beneficiary effects such as liver protection and reduction of total cholesterol.

Keywords:
fermentation adzuki beans black soybeans antioxidant activity cholesterol

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References:

[1]	Yui, K., Uematsu, H., Muroi, K., Ishii, K., Baba, M., and Osada, K., “Effect of dietary polyphenols from hop (Humulus lupulus L.) pomace on adipose tissue mass, fasting blood glucose, hemoglobin A1c, and plasma monocyte chemotactic protein-1 levels in OLETF rats,” Journal of Oleo Science, 62, 283-292, 2013.
[2]	The advance of carnivorous of Japanese [Growing lifestyle-related diseases risk], Nihon Keizai Shimbun, http://www.nikkei.com/article/DGXNASDG06048_W2A201C1CR8000/ 2012/12/6 (in Japanese).
[3]	Nishi, S., Yamashita, S., Saito, Y., Maeda, R., and Kojima, M., “Smaller increase in serum cholesterol level in rats fed an ethanol extract of adzuki bean seeds,” Nippon Shokuhin Kagaku Kogaku Kaishi, 53, 380-385, 2006 (in Japanese).
[4]	Chijimatsu, T., Umeki, M., Okuda, Y., Yamada, K., Oda, H. and Mochizuki, S., “The fat and protein fractions of freshwater clam (Corbicula fluminea) extract reduce serum cholesterol and enhance bile acid biosynthesis and sterol excretion in hypercholesterolaemic rats fed a high-cholesterol diet.” British Journal of Nutrition, 105, 526-534, 2011.
[5]	Yamashita, S., Nishi, S., Saito, Y., Maeda, R. and Kojima, M., “Antioxidative effect and liver protective action of adzuki polyphenol,” Nippon shokuhin kagaku kogaku kaishi, 53, 386-392, 2006 (in Japanese).
[6]	Nakayama, T., Kodama, M. and Nagata, C., “Generation of hydrogen peroxide and superoxide anion radical from cigarette smoke.” Gan, 75, 95-98, Feb. 1984.
[7]	Halliwel, B. and Gutteridge, J.M.C., Free radicals in biology and medicine. Oxford University Press, 1989, pp. 323-332.
[8]	Yoshikawa, T. and Kondo, M., Cellular Membrane: a key to disease processes, Boca Raton, CRC Press, 1993, pp. 271-284.
[9]	Yoshikawa., T., “Free radicals and their scavengers in Parkinson`s disease,” European Neurology, 33, 60-68, 1993.
[10]	Medvedev, Z.A., “An attempt at a rational classification of theories of ageing,” Biological Reviews, 65, 375-398, Aug. 1990.
[11]	Osawa, T., Yoshida, A., Kawakishi, S., Yamashita, K. and Ochi, H., Protective role of dietary antioxidants in oxidative stress. In: Cutler, R.G.,Packer, L., Bertram, J. and Mori, A. (Eds.) Oxidative Stress and Aging, Birkhauser Verlag, Basel/Switzerland, 1995.
[12]	Nakagawa,K., Ninomiya, M., Okubo,T., Aoi, N., Juneja, L., Kim, M., Yamanaka, K., and Miyazawa, T., “Tea Catechin Supplementation Increases Antioxidant Capacity and Prevents Phospholipid Hydroperoxidation in Plasma of Humans.” Journal of Agricultural and Food Chemistry, 47, 3967-3973, 1999.
[13]	Hatai, A., “Cooking Characteristics of Adzuki Beans, Vigna angularis,” The Japan Society of Cookery Science, 27, 238-242, 1994 (in Japanese).
[14]	Ministry of agriculture, forestry and fisheries, Crop yields of beans (dry grain) and buckwheat (by National Agricultural regions and prefectures)-adzuki beans, 2013 annual production crop statistics (Ordinary crops, feed crops, crafts crops), Statistical information, 2013. http://www.maff.go.jp/j/tokei/index.html
[15]	Wu, X., Beecher, G.R., Holden, J.M., Haytowitz, D.B., Gebhardt, S.E. and Prior, R.L., “Lipophilic and hydrophilic antioxidant capacities of common foods in the United States,” Journal of Agricultural and Food Chemistry, 52, 4026-4037, 2004.
[16]	Sato, S., Hori, Y., Yamate, J., Saito, T., Kurasaki, M. and Hatai, A., “Protective effect of dietary azuki bean (Vigna angularis) seed coats against renal interstitial fibrosis of rats induced by cisplatin.” Nutrition., 21, 504-511, 2005.
[17]	Kojima, M., Yamashita, S., Nishi, S., Saito, Y., Maeda, R., “Antioxidative Effect and Liver Protective Action of Adzuki Polyphenol.” Nippon Shokuhin Kagaku Kogaku Kaishi, 53, 386-392, 2006.
[18]	Nakamura, Y., Yabe, K., Shimada, K., Sasaki, K., Han, K., Okada, T., Sekikawa, M., Ohba, K., Ito, N., Horiuchi, K., Kawakami, S., and Fukushima, M., “Effect of Fermented Bean Paste on Serum Lipids in Rats Fed a Cholesterol-Free Diet,” Bioscience, Biotechnology, and Biochemistry, 73, 2506-2512, Nov. 2009.
[19]	Han, K.H., Fukushima, M., Kato, T., Kojima, M., Ohba, K., Shimada, K., Sekikawa, M. and Nakano, M., “Enzymeresistant fractions of beans lowered serum cholesterol and increased sterol excretions and hepatic mRNA levels in rats.” Lipids, 38,919-924, 2003.
[20]	Han, K.H., Fukushima, M., Shimizu, K., Kojima, M., Ohba, K., Tanaka, A., Shimada, K., Sekikawa, M. and Nakano, M., “Resistant starches of beans reduce the serum cholesterol concentration in rats.” Journal of Nutritional Science and Vitaminology, 49, 281-286, 2003.
[21]	Ikeda, I., Imasato, Y., Sasaki, E., Nakayama, M., Nagao, H., Takeo, T., Yayabe, F. and Sugano, M., “Tea catechins decrease micellar solubility and intestinal absorption of cholesterol in rats.” Biochimica et Biophysica Acta, 1127, 141-146, 1992.
[22]	Tsuda, T., Watanabe, M. and Ohshima, K., “Antioxidative activity of the anthocyanin pigments cyanidin 3-O-β-D-glucoside and cyanidin,” Journal of Agricultural and Food Chemistry, 42, 2407-2410, Nov. 1994.
[23]	Acquaviva, R., Russo, A., Galvano, F., Galvano, G., Barcellona, M.L., Li Volti, G., and Vanella, A., “Cyanidin and cyanidin 3-O-β-D-glucoside aas DNA cleavage protectors and antioxidants,” Cell Biology and Toxicology, 19, 243-252, Aug. 2003.
[24]	Hsu, C.K., Chang, C.H., Wang, C.C., “Black Soybeans Show Acute and Chronic Liver Protective Functions Against Ccl4 Induced Liver Damage.” World Academy of Science, Engineering and Technology, 3, 7, 2015.
[25]	CIE, Colorimetry (Second Edition), Central Bureau of the Commission International de L’Eclairage, Viena, 1986.
[26]	Raki´c, S., Petrovi´c, S., Kuki´c, J., Jadranin, M., Tesevi´c, V., Povrenovi´c, D. and Šiler-Marinković, S., “Influence of thermal treatment on phenolic compounds and antioxidant properties of oak acorn from Serbia.” Food Chemistry, 104, 830-834, 2007.
[27]	Blois, M.S., “Antioxidant determinations by the use of a stable free radical,” Nature, 181, 1199-1200, Apr. 1958.
[28]	Guide for the care and use of laboratory animals. Institute of laboratory animal resources commission on life sciences, National Academy Press, Washington, D.C, 1996.
[29]	National Research Council, Guide for the Care and Use of Laboratory Animals. National Academy Press, Washington, 1996.
[30]	Kosugi, H., Kojima, T., and Kikugawa, K., “Thiobarbituric acid-reactive substances from peroxidized lipids,” Lipids, 24, 873-881, Oct. 1989.
[31]	Gomyo, N., “Miso science and technology,” National Miso Engineering Society, 47, 205, 1999.
[32]	Yoshida, K., Sato, H., Ueshima, H., Ishii, N. and Sato, M., “The Extent and Its Source of Variation for Characteristics Related to Seed Quality of Adzuki Beans: II. Variation of seed coat color among growers lots in Hokkaido area,” Japan Journal of Crop. Science, 60, 234-240, 1991 (in Japanese).
[33]	Yoshida, K., Kameda, K. and Kondo, T., “Studies on anthocyanins of edible legumes,” Urakami Foundation Memories, 5, 85-95, 1996 (in Japanese).
[34]	Takasaki, S., Kouda, I., Ishikawa, M., Okamoto-kainuma, A., Koizumi, Y. and Fukuda, Y., “Properties of the novel products of miso developed using sesame flour,” Journal of Brewing Society of Japan, 105, 749-758, 2010 (in Japanese).
[35]	Friedman, M., “A comparison of alternative tests of significance for the problem of m rankings,” Annals of Mathematical Statistics, 11, 86-92, 1940.
[36]	Gu, Y., Yu, S. and Lambert, J.D., “Dietary cocoa ameliorates obesity-related inflammation in high fat-fed mice,” European Journal of Nutrition, 53, 149-158, Feb. 2014.
[37]	Orihashi, T., “Research about effect of miso on prevention of fatty liver in cow,” Journal of Brewing Society of Japan, 107, 19-24, 2012.
[38]	Kitano-Okada, T., Ito, A., Koide. A., Nakamura, Y., Han, K.H., Shimada, K., Sasaki, K., Ohba, K., Sibayama, S. and Fukushima, M., “Anti-obesity role of adzuki bean extract containing polyphenols: in vivo and in vitro effects,” Journal of the Science of Food and Agriculture, 92, 2644-2651, Oct. 2012
[39]	Yasuda, T., Nakajima, K., Hiwatashi, A., Moroi, C., Sanada, H. and Egashira, Y., “Effect of Rutin in Buckwheat Noodle on Lipid Metabolism in Rats,” Food Science and Technology Research, 19, 1011-1018, 2013.
[40]	Clark, J., Brancati, F. and Diehl, A., “The prevalence and etiology of elevated aminotransferase levels in the United States,” American Journal of Gastroenterology, 98, 960-967, May 2003.
[41]	Byun, J.S., Han, Y.S. and Lee, S.S., “The Effects of Yellow Soybean, Black Soybean, and Sword Bean on Lipid Levels and Oxidative Stress in Ovariectomized Rats,” International Journal for Vitamin and Nutrition Research, 80, 97-106, Apr. 2013.
[42]	Georgetti, S. R., Vicentini, F. T., Yokoyama, C. Y., Borin, M. F., Spadaro, A. C., Fonseca, M. J., “Enhanced in vitro and in vivo antioxidant activity and mobilization of free phenolic compounds of soybean flour fermented with different β-glucosidase-producing fungi,” Journal of Applied Microbiology, 106, 459-466, Feb. 2009.
[43]	Matsuo, M. and Takeuchi, T., “Preparation of low salt miso-like fermented seasonings using soy-oncom and okara-oncom (fermented soybeans and okara with Neurospora intermedia) and their antioxidant activity and antimutagenicity,” Food Science and Technology Research, 9, 237-241, 2003.
[44]	Matsuo, M., “Low-salt O-miso produced from koji fermentation of oncom improves redox state and cholesterolemia in rats more than low-salt soybean-miso,” Journal of Nutritional Science and Vitaminology, 50, 362-366, Oct. 2004.
[45]	Matsuo, M., “Chemical components, palatability, antioxidant activity and antimutagenicity of oncom miso using a mixture of fermented soybeans and okara with Neurospora intermedia,” Journal of Nutritional Science and Vitaminology, 52, 216-222, June 2006.
[46]	Kwak, C.S., Park, S.C. and Song, K.Y., “Doenjang, a fermented soybean paste, decreased visceral fat accumulation and adipocyte size in rats fed with high fat diet more effectively than nonfermented soybeans,” Journal of Medicinal Food, 15, 1-9, Jan. 2012.
[47]	Buhman, K.K., Furumoto, E.J., Donkin, S.S., and Story, J.A., “Dietary Psyllium Increases Fecal Bile Acid Excretion, Total Steroid Excretion and Bile Acid Biosynthesis in Rats.” Journal of Nutrition, 28, 1199-1203, 1998.