Antidiabetic Effects of Fermented Soybean Products on Type 2 Diabetes ⁎ Dae Young Kwona, James W
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Available online at www.sciencedirect.com Nutrition Research 30 (2010) 1–13 www.nrjournal.com Antidiabetic effects of fermented soybean products on type 2 diabetes ⁎ Dae Young Kwona, James W. Daily IIIb, Hyun Jin Kima, Sunmin Parkc, aEmerging Innovative Technology Research Division, Korean Food Research Institutes, Sungnam bDaily Manufacturing Inc., Rockwell, NC, USA cDepartment of Food and Nutrition, Obesity/Diabetes Research Institutes, Hoseo University, Asan Received 30 September 2009; revised 12 November 2009; accepted 15 November 2009 Abstract Historically, the incidence of type 2 diabetes has been lower in Asian populations compared with those in Western countries. One possible reason for the lower incidence among Asians is that they consume fermented soybean products, which are unique to the traditional Asian diet. Some have hypothesized that dietary phytoestrogens and soy peptides in fermented soybean foods consumed in traditional Asian diets may help prevent and slow the progression of type 2 diabetes. This review evaluates the existing evidence from animal studies and clinical and epidemiologic investigations on fermented soybeans in the prevention and treatment of type 2 diabetes. Nutritional studies performed in animals and intervention studies with humans suggest that the ingestion of soy protein with isoflavones improves glucose control and reduces insulin resistance. Korean fermented soybean products such as doenjang, kochujang, and chungkookjang contain alterations in the structures and content of isoflavonoids and small bioactive peptides, which are produced during fermentation. Several studies revealed improvements in insulin resistance and insulin secretion with the consumption of these fermented products. Therefore, fermented soybean products may help prevent or attenuate the progression of type 2 diabetes. Although the lack of human intervention trials does not permit definitive conclusions, the evidence does suggest that fermented soy products may be better for preventing or delaying the progression of type 2 diabetes compared with nonfermented soybeans. © 2010 Elsevier Inc. All rights reserved. Keywords: β-Cell function; β-Cell mass; Fermented soybean products; Insulin resistance; Isoflavonoids; Peptides; Type 2 diabetes Abbreviations: IGF-1, insulin-like growth factor 1; IRS-2, insulin receptor substrate 2; OVX, ovariectomy; PPAR, peroxisome- proliferator–activated receptors; SERMs, selective estrogen receptor modulators. 1. Introduction disorder characterized by both insulin deficiency and peripheral insulin resistance [1]. The pancreatic β cell adapts Because type 2 diabetes in Western populations is to increased nutrient availability and insulin resistance by typically accompanied by obesity and hyperinsulinemia, increasing its function and mass [2]. These processes are insulin secretion has received less emphasis than do insulin orchestrated by signals derived from nutrient metabolism, resistance. However, recent studies have revealed the hormones, and cytokines. The failure of β-cell adaptation importance of insulin secretion capacity to prevent type 2 results in type 2 diabetes [3]. Thus, β-cell dysfunction and diabetes. Type 2 diabetes is a heterogeneous metabolic deficient mass pancreatic mass play crucial roles in the development of insulin resistance and subsequent β-cell ⁎ compensation failure and diabetes [4]. Corresponding author. Department of Food and Nutrition, Hoseo β University, Chungnam-Do 336-795, Korea. Tel.: +82 41 540 5633; fax: +82 The primary defect in type 2 diabetes is increased -cell 41 548 0670. apoptosis, which decreases β-cell mass [5]. Therefore, the E-mail address: [email protected] (S. Park). progressive nature of type 2 diabetes is due to β-cell failure. 0271-5317/$ – see front matter © 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.nutres.2009.11.004 2 D.Y. Kwon et al. / Nutrition Research 30 (2010) 1–13 Attenuating insulin resistance, improving β-cell function, and that fermentation changes those bioactive compounds in and increasing β-cell mass are important for preventing and ways that potentiate the antidiabetic properties. delaying the progression of type 2 diabetes. Herein we discuss how fermented soybean products, Soybeans (Glycine max MERILL) have long been isoflavones, and soy peptides improve glucose metabolism, important protein sources, complementing grain proteins, insulin resistance, insulin secretion, and β-cell mass. This in Asian countries. Asians typically consume 9 to 30 g report reviews epidemiologic and experimental evidence soybeans per day, with individual and regional variations describing the effectiveness and possible mechanisms that (Table 1) [6]. In addition to protein, soybeans also contain support and challenge the hypothesis. Some human studies various nutrients and functional components including have been conducted to investigate the antidiabetic effects isoflavonoids [7]. Because isoflavonoids have structural of soybeans and soy isoflavonoids, but a few studies have similarities to endogenous estrogen, they exert estrogenic or investigated fermented soybeans. Thus, this review includes antiestrogenic action with weak binding affinity to the a discussion of soybeans and their compositional changes estrogen receptors, where they act as agonists or competitive that occur during fermentation to support the antidiabetic antagonists [8]. Estrogen is reportedly beneficial for effects and mechanism of action of these fermented preventing and treating type 2 diabetes by attenuating soybean products. insulin resistance, improving insulin secretion, and increas- ing β-cell mass [9]. Therefore, soy isoflavonoids may improve glucose homeostasis through estrogenic action. In 2. Fermented soybean products addition, soy proteins may also improve glucose metabo- Various types of fermented soybean foods are consumed lism. Hence, soybeans may help prevent type 2 diabetes and in Asian countries such as Korea, China, Japan, Indonesia, delay its progression. and Vietnam. The most common Korean fermented soybean Fermentation is one of the major processes used in the foods are chungkookjang, doenjang, kochujang, and soy production of food from soybeans. Fermented bean paste is sauce. Natto and miso are Japanese versions of chungkook- indigenous to the cuisines of East and Southeast Asia. jang and doenjang, respectively. China also has various Korean soy foods are increasingly present on the worldwide fermented soybean products such as doubanjiang, douchi, market, and because kochujang and fermented soybean sweet noodle sauce, tauchu, yellow soybean paste, and pastes (deonjang and chungkookjang) were registered in dajiang. Doenjang, kochujang, and soy sauce are fermented CODEX on July 4, 2009, they are now internationally with varying microorganisms when traditionally made, accepted foods. Most fermented soybean pastes are salty and because fermentation conditions and ambient microbiota savory and some are spicy. They are often used as are different among regional environments (Fig. 1). To make condiments to flavor foods such as stir-fries, stews, and these products by the traditional method, cooked soybeans soups. Differences in their colors and flavors are due to are formed into blocks and fermented outdoors for 20 to 60 different production methods such as the conditions of days by microorganisms naturally present in the environ- fermentation; the addition of wheat flour, pulverized mantou, ment. The fermented blocks are known as meju and are used rice, or sugar; and the presence of different microflora such to prepare the soy pastes and sauce. Meju can be fermented as bacteria or molds used in their production, as well as for less than 5 days by inoculating with microorganisms such whether the soybeans are roasted (as in chunjang) or aged (as as Aspergillus sp; however, when fermented by traditional in tauchu) before being ground. The fermentation of these methods meju is typically fermented primarily by Bacilli soybean products changes the bioactive components, such as species during the early stages of fermentation, followed by isoflavonoids and peptides, in ways which may alter their Aspergillus species, which predominate during the remaining efficacy in the treatment of type 2 diabetes. The intake of fermentation period. Aspergillus oryzae is the major soybeans and fermented soybeans may be associated with microorganism in the final product of meju when it is made the antecedently lower incidence of type 2 diabetes in Asians in the traditional way. Chungkookjang is a short-term [10]. This review is based on the hypothesis that bioactive fermented soybean product similar to Japanese natto, compounds found in soybean have antidiabetic properties whereas doenjang, kochujang, and soy sauce undergo long- term fermentation as do Chinese tauchu and Japanese miso. Table 1 Consumption of soybeans and prevalence of cancer in various countries 3. Changes in soybean components by fermentation Countries Soybean Breast cancer Prostates cancer consumption (g/d) prevalence prevalence 3.1. Nutritional and functional compounds in soybeans Japan 29.5 60 35 Korea 19.9 26 5 Soybean products have been designated as one of world's Hong Kong 10.3 84 29 healthiest foods due to being an excellent source of high- China 9.3 47 28 quality protein as well as providing various health benefits. United States minor 224 157 The protein content of soybean is 32% to 42% (depending on Prevalence is defined as the number of diagnosed cancers per 100 000. the variety and growth