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Fermented soyfoods play an important role in the cuisines of many Asian countries. Fermentation produces changes in the composition of the food itself but the health implications of these changes aren’t precisely understood. Limited evidence suggests fermented soyfoods exert favorable changes on the composition of the intestinal microbiota.
There are numerous ways in which fermentation can potentially enhance the healthfulness of soy, such as by decreasing phytate,1 protease inhibitor2 and oxalate3content, thereby potentially improving protein digestion4 and mineral absorption.5-7 Fermentation may also create antioxidants8-9 and in the case of natto, fermentation causes this food to be an excellent source of vitamin K10,11 and nattokinase, an enzyme which exhibits fibrinolytic activity.12-13 However, the nutritional and physiological relevance of these fermentation-induced changes remains to be established. This lack of clarity is because there is adaptation to the inhibitory effects of phytate on mineral absorption,14 the digestion of protein from unfermented soy is excellent15 and despite containing oxalate (and phytate) the absorption of calcium from fortified soymilk is similar to the absorption of calcium from cow’s milk.16
In addition to the above-cited changes, fermentation causes more of the isoflavones naturally present in the soybean to be in the aglycone rather than glycoside form.17-20 Since isoflavones are absorbed as aglycones, there has been speculation that by bypassing the first step in the absorption of isoflavone glycosides, which is the hydrolysis of the glucose molecule from the isoflavone backbone, the absorption of isoflavones from fermented foods would be greater than from unfermented ones. However, despite years of investigation, no consensus on this issue has emerged,21-26 although it is accepted that aglycones are absorbed more quickly.21-23
Over the past decade or so there has been a surge of interest in understanding the effect of diet on the microbiota and the impact of the microbiota on overall health.27 Some soyfoods may influence the microbiota because the soybean contains large amounts of oligosaccharides (predominately stachyose).28-31 Because these sugars are poorly digested by intestinal enzymes, they travel to the colon where they are able to stimulate the growth of bacteria such as Bifidobacteria which are considered to be advantageous to the host. For this reason soybean oligosaccharides are classified as prebiotics.32-34
Fermented soyfoods may affect the intestinal microflora independent of oligosaccharide content, however. For example, tempeh made from soybeans was shown to stimulate the growth of bacteria of the genus Bifidobacterium, whereas tempeh made from common beans stimulated the growth of Escherichia coli.35 These changes clearly represent potential beneficial effects of soy tempeh. For this in vitro study, tempeh was fermented for 24 hours and then subjected to digestion in conditions simulating the human digestive tract. Human fecal microflora were added at the stage corresponding to the small intestine and the change in the number of microorganisms belonging to the genera Bifidobacterium, Lactobacillus, E. coli and Enterococcus was determined at the end of the digestion process.
More than a decade ago, the effect of natto on the microbiota was evaluated by Japanese researchers.36 Natto is an especially popular food in the Eastern regions of Japan. For this study, seven healthy volunteers 22 to 49 years of age consumed 50 g/day of natto for 14 days. When compared to the baseline values, during natto consumption, the counts of Bacillus subtilis and Bifidobacterium were significantly increased, whereas the counts and the frequency of the occurrence of lecithinase-positive clostridia, including Clostridium perfringens, were significantly decreased. Natto had previously been shown to enhance the growth of Bacillus, Streptococcusand Lactobacillus, and to reduce Escherichia coli, in rat caeca.37
A second human study that utilized a similar experimental design as the previous study, examined the effects of miso soup containing natto on the microbiota.38 The results of the two studies are similar. Over the 14-day experimental period, the numbers of Bacillus and Bifidobacterium were increased whereas numbers of Enterobacteriaceae were decreased and the numbers of Clostridium perfringenstended to decrease. The eight participants in this study consumed 200 ml of miso soup daily containing 50 g of commercially available natto that was boiled for one minute.
Finally, a cross-over study found that fermented soymilk led to desirable changes in the intestinal microflora. Soymilk is typically consumed in the unfermented form but for experimental purposes, Chinese researchers compared the effects of fermented and unfermented soymilk.39 Twenty-eight participants consumed 250 ml twice a day between meals, of either fermented soymilk or regular soymilk for two weeks and then switched to the other drink for two weeks after a two-week washout period. During the consumption of fermented soymilk, the populations of Bifidobacterium spp. and Lactobacillus spp. increased as well as the ratios of Bifidobacterium spp. and Lactobacillus spp. to Clostridium perfringens. The population of coliform organisms also decreased in response to fermented soymilk consumption. A more recent study that also compared fermented with unfermented soymilk also found more favorable changes in the intestinal microflora in response to the former.32 For this study, 10 participants from 21 to 25 years old consumed 100 ml/day of either fermented or unfermented soymilk for two weeks.
Future research is needed to determine how changes in the microflora in response to fermented soyfoods affect overall health.
Popular Fermented Soyfoods in Asia
Traditional Asian soyfoods are typically divided into two general categories, fermented and unfermented. The latter includes tofu, edamame, and soymilk; the former includes tempeh, miso and natto, although tofu can also be consumed in fermented form. Soy sauce, which is fermented, is widely used in Asia but it is a condiment/flavoring agent that provides little nutritional value.
These are among the most widely consumed fermented soyfoods in Asia:
Tempeh is manufactured with dehulled, soaked, and cooked soybeans inoculated with a mold, normally, of the genus Rhizopus. The cultured soybeans are bound together by newly grown thick white mycelia to form a cake. During the growth of mold, the functional properties of foods are formed as follows: protein is hydrolyzed to amino acids and peptides by proteolytic enzymes,1-3 oligosaccharides are hydrolyzed to monosaccharides4 and phytic acid degraded to inorganic phosphates.5-7
Miso is a traditional Japanese seasoning produced by fermenting soybeans with salt and the fungus Aspergillus oryzae, known in Japanese as kōji, and sometimes rice, barley, or other ingredients. The result is a thick paste used for sauces and spreads, pickling vegetables or meats, and mixing with dashi soup stock to serve as miso soup called misoshiru, a Japanese culinary staple.
Natto is a traditional Japanese food made from soybeans fermented with Bacillus subtilis var. natto. Natto is often eaten at breakfast and served with soy sauce, karashi mustard and welsh onion. Natto may be an acquired taste because of its powerful smell, strong flavor, and slimy texture.
1. Wang HLH, C.W. Wheat tempeh. Cereal Chem 1966;43(563-70.
2. Sparringa RA, Owens JD. Protein utilization during soybean tempe fermentation. J Agric Food Chem. 1999;47(10):4375-8.
3. Handoyo T, Morita N. Structural and functional properties of fermented soybean (tempeh) by using Rhizopus oligosporus. Intern J Food Properties. 2006;9(347-55.
4. Rehms H, Barz W. Degradation of stachyose, raffinose, melibiose and sucrose by different tempe-producing Rhizopus fungi. Appl Microbiol Biotechnol. 1995;44(1-2):47-52.
5. Sutardi, Buckle KA. Reduction in phytic acid levels in soybeans during tempeh production, storage and frying. J Food Sci. 1985;50(260-3.
6. Sutardi, Buckle KA. Characterization of extra- and intracellular phytases from Rhizopus oligosporus used in tempeh production. Int J Food Microbiol. 1988;6(1):67-79.
7. Hachmeister KA, Fung DY. Tempeh: a mold-modified indigenous fermented food made from soybeans and/or cereal grains. Crit Rev Microbiol. 1993;19(3):137-88.
History of Fermented Soyfoods
Soyfoods were first consumed in fermented form beginning in China around 2,200 years ago and in Japan approximately 700 years later. Historical records indicate that in China, unfermented soybeans and tofu were consumed beginning approximately 2000 and 1000 years ago, respectively.
Today, in Japan, about half of soy consumed is derived from unfermented foods, primarily tofu, and about half comes from the fermented products, miso and natto.1,2 In contrast, in China,3 Hong Kong4 and Singapore,5 nearly all soy consumed is in unfermented form, mostly as soymilk and various forms of tofu. In Indonesia (the birthplace of tempeh), about 60% of the soy is consumed in fermented form as tempeh, and about 40% as tofu.6 Finally, in Korea, about 70% of the soy is consumed in unfermented form.7
1. Wakai K, Egami I, Kato K, et al. Dietary intake and sources of isoflavones among Japanese. Nutr Cancer. 1999;33(2):139-45.
2. Somekawa Y, Chiguchi M, Ishibashi T, Aso T. Soy intake related to menopausal symptoms, serum lipids, and bone mineral density in postmenopausal Japanese women. Obstet Gynecol. 2001;97(1):109-15.
3. Zhang X, Shu XO, Gao YT, et al. Soy food consumption is associated with lower risk of coronary heart disease in Chinese women. J Nutr. 2003;133(9):2874-8.
4. Ho SC, Woo JL, Leung SS, Sham AL, Lam TH, Janus ED. Intake of soy products is associated with better plasma lipid profiles in the Hong Kong Chinese population. J Nutr. 2000;130(10):2590-3.
5. Seow A, Shi CY, Franke AA, Hankin JH, Lee HP, Yu MC. Isoflavonoid levels in spot urine are associated with frequency of dietary soy intake in a population-based sample of middle-aged and older Chinese in Singapore. Cancer Epidemiol Biomarkers Prev. 1998;7(2):135-40.
6. Purba MB, Lukito W, Wahlqvist ML, et al. Food intake and eating patterns of Indonesian elderly bofore the 1998 economic crisis. Asia Pac J Clin Nutr. 1999;8(200-6.
7. Kim YJ, Park MY, Chang N, Kwon O. Intake and major sources of dietary flavonoid in Korean adults: Korean National Health and Nutrition Examination Survey 2010-2012. Asia Pac J Clin Nutr. 2015;24(3):456-63.
REFERENCES (lead article)
1. Watanabe N, Aoki H, Fujimoto K. Fermentation of soybean by Rhizopus promotes the calcium absorption ratio in rats. J Sci Food Agr. 2008;88(2749-52.
2. Cervantes-Pahm SK, Stein HH. Ileal digestibility of amino acids in conventional, fermented, and enzyme-treated soybean meal and in soy protein isolate, fish meal, and casein fed to weanling pigs. J Anim Sci. 2010;88(8):2674-83.
3. Urua IS, Uyoh EA, Ntui VO, Okpako EC. Effect of processing on proximate composition, anti-nutrient status and amino acid content in three accessions of African locust bean (Parkia biglobosa (jacq.) benth. Int J Food Sci Nutr. 2012.
4. Chitra U, Vimala V, Singh U, Geervani P. Variability in phytic acid content and protein digestibility of grain legumes. Plant Foods Hum Nutr. 1995;47(2):163-72.
5. Heaney RP, Weaver CM, Fitzsimmons ML. Soybean phytate content: effect on calcium absorption. Am J Clin Nutr. 1991;53(3):745-7.
6. Hurrell RF, Reddy MB, Juillerat MA, Cook JD. Degradation of phytic acid in cereal porridges improves iron absorption by human subjects. Am J Clin Nutr. 2003;77(5):1213-9.
7. Weaver CM, Heaney RP, Proulx WR, Hinders SM, Packard PT. Absorbability of calcium from common beans. J Food Sci. 1993;58(1401-3.
8. Esaki H, Kawakishi S, Morimitsu Y, Osawa T. New potent antioxidative o-dihydroxyisoflavones in fermented Japanese soybean products. Biosci Biotechnol Biochem. 1999;63(9):1637-9.
9. Esaki H, Onozaki H, Morimitsu Y, Kawakishi S, Osawa T. Potent antioxidative isoflavones isolated from soybeans fermented with Aspergillus saitoi. Biosci Biotech Biochem. 1998;62(4):740-46.
10. Kamao M, Suhara Y, Tsugawa N, et al. Vitamin K content of foods and dietary vitamin K intake in Japanese young women. J Nutr Sci Vitaminol (Tokyo). 2007;53(6):464-70.
11. Katsuyama H, Ideguchi S, Fukunaga M, Saijoh K, Sunami S. Usual dietary intake of fermented soybeans (Natto) is associated with bone mineral density in premenopausal women. J Nutr Sci Vitaminol (Tokyo). 2002;48(3):207-15.
12. Fujita M, Hong K, Ito Y, Fujii R, Kariya K, Nishimuro S. Thrombolytic effect of nattokinase on a chemically induced thrombosis model in rat. Biol Pharm Bull. 1995;18(10):1387-91.
13. Fujita M, Nomura K, Hong K, Ito Y, Asada A, Nishimuro S. Purification and characterization of a strong fibrinolytic enzyme (nattokinase) in the vegetable cheese natto, a popular soybean fermented food in Japan. Biochem Biophys Res Commun. 1993;197(3):1340-7.
14. Armah SM, Boy E, Chen D, Candal P, Reddy MB. Regular consumption of a high-phytate diet reduces the inhibitory effect of phytate on nonheme-iron absorption in women with suboptimal iron stores. J Nutr. 2015;145(8):1735-9.
15. Rutherfurd SM, Fanning AC, Miller BJ, Moughan PJ. Protein digestibility-corrected amino acid scores and digestible indispensable amino acid scores differentially describe protein quality in growing male rats. J Nutr. 2015;145(2):372-9.
16. Zhao Y, Martin BR, Weaver CM. Calcium bioavailability of calcium carbonate fortified soymilk is equivalent to cow's milk in young women. J Nutr. 2005;135(10):2379-82.
17. Murphy PA, Song T, Buseman G, et al. Isoflavones in retail and institutional soy foods. J Agric Food Chem. 1999;47(7):2697-704.
18. Nakajima N, Nozaki N, Ishihara K, Ishikawa A, Tsuji H. Analysis of isoflavone content in tempeh, a fermented soybean, and preparation of a new isoflavone-enriched tempeh. J Bioscience Bioengineering. 2005;100(685-87.
19. Yen GC, Lai HH. Inhibition of reactive nitrogen species effects in vitro and in vivo by isoflavones and soy-based food extracts. J Agric Food Chem. 2003;51(27):7892-900.
20. Chan SG, Murphy PA, Ho SC, et al. Isoflavonoid content of Hong Kong soy foods. J Agric Food Chem. 2009;57(12):5386-90.
21. Nagino T, Kano M, Masuoka N, et al. Intake of a fermented soymilk beverage containing moderate levels of isoflavone aglycones enhances bioavailability of isoflavones in healthy premenopausal Japanese women: a double-blind, placebo-controlled, single-dose, crossover trial. Bioscience of microbiota, food and health. 2016;35(1):9-17.
22. Izumi T, Piskula MK, Osawa S, et al. Soy isoflavone aglycones are absorbed faster and in higher amounts than their glucosides in humans. J Nutr. 2000;130(7):1695-9.
23. Chang Y, Choue R. Plasma pharmacokinetics and urinary excretion of isoflavones after ingestion of soy products with different aglycone/glucoside ratios in South Korean women. Nutr Res Pract. 2013;7(5):393-9.
24. Yuan B, Zhen H, Jin Y, et al. Absorption and plasma disposition of genistin differ from those of genistein in healthy women. J Agric Food Chem. 2012;60(6):1428-36.
25. Zubik L, Meydani M. Bioavailability of soybean isoflavones from aglycone and glucoside forms in American women. Am J Clin Nutr. 2003;77(6):1459-65.
26. Setchell KD, Brown NM, Desai P, et al. Bioavailability of pure isoflavones in healthy humans and analysis of commercial soy isoflavone supplements. J Nutr. 2001;131(4):1362S-75S.
27. Maukonen J, Saarela M. Human gut microbiota: does diet matter? Proc Nutr Soc. 2015;74(1):23-36.
28. Karr-Lilienthal LK, Grieshop CM, Spears JK, Fahey GC, Jr. Amino acid, carbohydrate, and fat composition of soybean meals prepared at 55 commercial U.S. soybean processing plants. J Agric Food Chem. 2005;53(6):2146-50.
29. Kuo TM, VanMiddlesworth JF, Wolf WJ. Content of raffinose oligosaccharides and sucrose in various plant seeds. J Agric Food Chem. 1988;36(32-6.
30. Grieshop CM, Kadzere CT, Clapper GM, et al. Chemical and nutritional characteristics of United States soybeans and soybean meals. J Agric Food Chem. 2003;51(26):7684-91.
31. de Lourdes MB, P, Silva HCB, G.L. Oligosaccharide content of ten varieties of dark-coated soybeans. J Agr Food Chem. 1984;32(355-7.
32. Inoguchi S, Ohashi Y, Narai-Kanayama A, Aso K, Nakagaki T, Fujisawa T. Effects of non-fermented and fermented soybean milk intake on faecal microbiota and faecal metabolites in humans. Int J Food Sci Nutr. 2012;63(4):402-10.
33. Bang MH, Chio OS, Kim WK. Soyoligosaccharide increases fecal bifidobacteria counts, short-chain fatty acids, and fecal lipid concentrations in young Korean women. J Med Food. 2007;10(2):366-70.
34. Hayakawa K, Mizutani J, Wada K, Masa T, Yoshihara I, Mitsuoka T. Effects of soybean oligosaccharides on human faecal flora. Microbial Ecol Health Dis. 1990;3(292-303.
35. Kuligowski M, Jasinska-Kuligowska I, Nowak J. Evaluation of bean and soy tempeh influence on intestinal bacteria and estimation of antibacterial properties of bean tempeh. Polish journal of microbiology / Polskie Towarzystwo Mikrobiologow = The Polish Society of Microbiologists. 2013;62(2):189-94.
36. Terada A, Yamamoto M, Yoshimura E. Effect of the fermented soybean product "natto" on the composition and metabolic activity of the human fecal flora. Jpn J Food Microbiol. 1999;16(221-30.
37. Watanabe T, Tsuchihashi N, Kanno A, Takai Y. Effects of natto and steamed soybeans on growth and cecal bacterial flora of rats. J Jpn Soc Nutr Food Sci 1995;48(283-9.
38. Fujisawa T, Shinohara K, Kishimoto Y, Terada A. Effect of miso soup containing natto on the composition and metabolic activity of the human faecal flora. Microbial Ecology Health Disease. 2006;18(79-84.
39. Cheng IC, Shang HF, Lin TF, Wang TH, Lin HS, Lin SH. Effect of fermented soy milk on the intestinal bacterial ecosystem. World J Gastroenterol. 2005;11(8):1225-7
Mark Messina, PhD, MS, is the executive director of the Soy Nutrition Institute, and co-owner of Nutrition Matters, Inc., a nutrition consulting company. He is an adjunct professor at Loma Linda University and chairman of The Soy Connection Editorial Board. His research focus is on the health effects of soyfoods and soybean components.
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