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New Functional Properties of Fermented Rice Bran in Food Processing and Inflammatory Bowel Disease Model Mice
Chapter 16
New Functional Properties of Fermented Rice Bran in Food Processing and Inflammatory Bowel Disease Model Mice Takashi Kuda Department of Food Science and Technology, Tokyo University of Marine Science and Technology, Tokyo, Japan
1. INTRODUCTION The blue shark, Prionace glauca, and salmon shark, Lamna ditropis, frequently land at fisheries ports in the north-eastern coastal region of Japan, Tohoku, particularly in the city of Kesennuma in the Miyagi prefecture. While shark body muscle meat is generally considered of a low value, the fins (especially those containing ceratotrichia) are a valuable commodity, evidenced by an increase in demand for shark fin soup among the Chinese middle class.1 The removal of shark fins and the subsequent discarding of the finless bodies are a significant ecological problem.2 In Japan, almost all meat obtained from the body of blue sharks is used for surimi (fish paste)–based products such as hampen.3 However, the heart of the salmon shark is consumed as part of the sashimi cuisine in Kesennuma and its body muscle meat is traditionally consumed as sashimi and cooked dishes in other areas, particularly in the inland region. Fresh muscle meat from these sharks does not smell of ammonia or other undesirable volatile compounds. However, shark meat can become odorous because of ammonia buildup over time. In elasmobranchs, which includes sharks, ammonia is generated from urea in the muscles as a part of osmotic balance.4 Occasionally, shark meat produces ammonia that smells relatively strong in a refrigerated stock room. In Japan, the water-leaching method is used to elute ammonia and urea from minced fish muscle meat. However, this process may only be used for surimi food products. Volatile basic nitrogen compounds, including ammonia, trimethylamine, and other volatile amines, are responsible for most of the pungent fishy odors emitted from seafood.5 These alkaline products readily dissolve in acidified solutions as opposed to alkaline and neutral solutions. As mentioned above, fresh shark meat should have no undesirable odor when used for sashimi. Therefore, it is commercially advantageous to develop strategies to improve the preference for less fresh fish meat over fresh fish meat. Rice bran (RB) is a major by-product of rice polishing. With the aim of reducing the ammonia content and improving the preference for meat from the blue shark, P. glauca, and salmon shark, L. ditropis, we evaluated the effect of soaking RB in solutions containing 10% sucrose and 5% NaCl in the form of an aqueous extract suspension (AES) of RB or fermented RB (FRB) generated from selected Lactobacillus plantarum and Saccharomyces cerevisiae strains.6,7 Inflammatory bowel disease (IBD) encompasses two forms of intestinal inflammation: ulcerative colitis (UC) and Crohn’s disease (CD). UC is a chronic disease characterized by diffuse inflammation of the rectal and colonic mucosa.8 The incidence rate of UC is high in the United States and Western Europe, reaching 34 and 263 per 100,000 children and adults, respectively, in 2009.9 Similarly, the number of cases in East Asian countries, such as Korea and Japan, has also increased in recent years.10,11 CD has a broad spectrum of clinical manifestations, and the initial presentation is seldom a good predictor of the clinical course. While the pathogenesis of IBD is not completely understood, oxidative stress caused by reactive oxygen species is considered one of the etiological factors involved in several symptoms of IBD.12 Therefore, many studies have reported the antioxidant properties of various foods and extracted compounds and their uses in IBD treatment.13 The beneficial effects and antioxidant properties of some chemical compounds contained in RB for IBD treatment have been reported.14 Recently, the beneficial effect of lactic acid bacteria (LAB) against dextran sodium sulfate (DSS)–induced murine IBD in relation to the superoxide anion radical scavenging capacity was studied.15,16 Some LAB strains suppressed nitric oxide (NO) secretion of murine macrophages, induced by the lipopolysaccharide (LPS) of pathogens.15,17 Dietary Interventions in Gastrointestinal Diseases. https://doi.org/10.1016/B978-0-12-814468-8.00016-8 Copyright © 2019 Elsevier Inc. All rights reserved.
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This chapter presents the new functional effects of FRB fermented using S. cerevisiae and L. plantarum on ammonia content and preference ranking in fresh and less fresh shark meats,6,7 as well as on DSS-induced IBD model mice.18
2. PREPARATION OF FERMENTED RICE BRAN FOR AMMONIA REDUCTION IN SHARK MEAT To use as a starter for fermented fish products, probiotics, and environmental remediation, LAB and yeasts were isolated from marine coast (Satoumi) environments and screened for resistance against acid, salt, and bile.19–32 Among the isolates, Saccharomyces cerevisiae Misaki-1 (Fig. 16.1A and B) isolated from algal beach casts was selected as an ammonialowering yeast by in vitro screening.6 Although there was no ammonia-lowering strain among the Satoumi LAB isolates, Lactobacillus plantarum Sanriku-SU8 (Fig. 16.1C) promoted the ammonia-lowering capacity of S. cerevisiae Misaki-1. Instead of ordinary broth media, Japanese RB, a major by-product of rice polishing, was used. Lightly roasted RB was autoclaved with a 10-fold volume of distilled water (DW) and filtered through a kitchen net. This AES of RB was fermented with a coculture of S. cerevisiae Misaki-1 and L. plantarum Sanriku-SU8 at 30°C for 48 h. During the fermentation, saccharides were converted to lactic acid and ethanol and the pH decreased from 6.5 to 4.3 (Fig. 16.2). Although the RB-AES had a rich RB odor, the FRB-AES had a slightly sweet honey odor.
FIGURE 16.1 Cellular morphology of the Saccharomyces cerevisiae Misaki-1 (A) using a phase-contrast microscope and (B) using an atomic force microscope, SPM-9000, Shimadzu, phase-contrast mode and Lactobacillus plantarum Sanriku-SU8 (C) using a Table Top SEM, TM3030, Hitachi, without treatment.
FIGURE 16.2 (A) Growth of Saccharomyces cerevisiae Misaki-1 and Lactobacillus plantarum Sanriku-SU8 coculture in 10% rice bran (RB) aqueous extract suspension (AES). (B) High performance liquid chromatography (HPLC) chromatogram for saccharides, lactic acid, and ethanol of the fermented RB (FRB) AES. (C) Image of the Misaki-1 and Sanriku-SU8 in FRB-AES observed under TM3030.
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3. EFFECT OF FERMENTED RICE BRAN ON AMMONIA CONTENT AND PREFERENCE RANKING IN SHARK AND OTHER FISH MEAT The soaking brine for the shark meat was made with 200 mL of FRB-AES, 100 g sucrose, 50 g table salt, and 800 mL water. From the results of several soaking experiments, the soaking brine volume to the meat weight ratio was set to 1:1, the temperature 10°C, and the time 48 h.7 In fresh shark meat, ammonia content was low (160–180 mg/kg, Fig. 16.3A and C) and the effects of RB and FRB were not significant. However, meat stored at 10°C for 48 h before the soaking treatment had high ammonia content (340–350 mg/kg, Fig. 16.3B and D) and the effects of RB and FRB were significant. After soaking, the redness of the meat, particularly in the salmon shark meat, decreased (Fig. 16.3E and G). After cooking, browning was observed in only the FRB-treated meat, particularly in blue shark meat (Fig. 16.3F). The browning may be from the Maillard reaction,33 which involves proteolysis and generation of reducing sugars by the yeast and LAB. After light sautéing, the meat slices were ranked from first (the most preferable) to fifth (the least preferable) by total preference. The beneficial effects of the RB and FRB on the preference were not significant in the fresh shark meat (Fig. 16.4 A and C) but significant in the less fresh shark meat (Fig. 16.4B and D). In this experiment, no participants could smell ammonia in any sample. However, comments were made about the reduction in fishy odor and improvements in the taste and texture, from “somewhat dry” to “somewhat moist, tender, and firm,” after soaking with FRB. The improved taste and texture might be caused by S. cerevisiae Misaki-1 protease activity on myofibrillar proteins (Fig. 16.4E and F) and protease activity on water-soluble proteins, which have been shown to correlate with the texture34 and taste,35 respectively. These positive effects of FRB on the meat texture and taste have also been shown previously7 with the chub mackerel fish, pacific cod fish, and chicken breast meat.
4. DIETARY AND LIFESTYLE DISEASE INDICES AND CECAL MICROBIOTA IN HIGH-FAT DIET, DIETARY FIBER-FREE DIET, OR DSS-INDUCED IBD MODELS IN CLOSED COLONY MICE Dietary and lifestyle-related chronic diseases such as obesity, type 2 diabetes, hypertension, and chronic immune IBD are of great concern worldwide.36,37 The relationship between these chronic diseases, gut microbiota, and some functional foods has been studied extensively in recent years.38 To study the beneficial effects of food on these chronic diseases, healthy inbred mice, particularly the BALB/c and C57BL/6 strains, are often used. Although these inbred mice provide
FIGURE 16.3 Effect soaking on ammonia content in fresh and stored blue shark and salmon shark meats. The fresh shark meats were stored at 10°C for 0 (A and C) and 2 (B and D) days. The meat was then soaked in sucrose-salt brine without RB (SS), brine with RB-AES, or brine with FRB-AES at 10°C for 2 days. (E and F) Images of soaked and soaked-cooked blue shark meat, respectively. (G) Images of soaked salmon shark meat. AES, aqueous extract suspension; FRB, fermented rice bran; RB, rice bran.
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FIGURE 16.4 Effect of soaking on preference ranking in fresh and stored blue shark and salmon shark meats. The fresh shark meats were stored at 10°C for 0 (A and C) or 2 (B and D) days. The meat was then soaked in SS, RB-AES, or FRB-AES at 10°C for 2 days. The participants ranked the five treatments from first (the most preferable) to fifth. (E and F) Images of sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) of crude myofibrillar protein of treated blue shark (E) and salmon shark (F) meats. AES, aqueous extract suspension; FRB, fermented rice bran; RB, rice bran.
reliable data with minimal individual variance, they are more susceptible to certain diseases. For example, BALB/c and C57BL/6 mice are more likely to suffer infection and obese–diabetes diseases, respectively.39 However, closed colony mice such as Institute of Cancer Research (ICR; CD-1) mice have reasonable genetic variation, good growth, and increased resistance to pathogenic bacteria.40 Therefore, ICR mice can be considered to exhibit the resistances similar to those of healthy humans. In our recent study41 to examine the relationship between multiple lifestyle-related diseases and IBD, ICR mice were fed normal chow (CE-2), CE-2 with DSS in drinking water, a high-fat diet (Quick Fat), or a fiber-free high-sucrose diet (AIN-76(-)). The ratio of low-density lipoprotein cholesterol to high-density lipoprotein cholesterol (LDL/HDL) was generally higher in the AIN-76(-) and DSS groups. Shortening of the colon, an indicator of IBD, was prominent in the AIN76(-) group (Fig. 16.5A and B). Damage of colon epithelial cells and layers was considerable in the DSS group and also observed in the Quick Fat and AIN-76(-) groups (Fig. 16.5C). Gram staining of cecal contents revealed that sporulation was promoted by DSS (Fig. 16.5D). The 16S rDNA amplicon sequencing of cecal contents showed that the ratio of bacteria from the phylum Firmicutes, particularly in Bifidobacterium, was high in the AIN-76(-) group (Fig. 16.6). In addition to Turicibacter, Bacteroides and Akkermansia muciniphila, which reportedly ameliorate obesity and immune reactions,42 were high in number in the DSS group. Although Allobaculum, previously reported as negative correlation bacteria to high-fat diet,43 was dominant in all diet groups, its operational taxonomic unit (OTU) was different in each group. Similarly, although Lactobacillus was dominant in all diet groups, some Lactobacillus OTUs such as Lactobacillus reuteri were low in the lifestyle disease and IBD model groups. In daily life, several factors affect disease progression. Therefore, consideration of the differences and similarities between the model mice is important for experiments on nutrition, food function, and toxicity.
5. PROTECTIVE EFFECTS OF FRB IN DSS-INDUCED IBD MODEL ICR MICE As mentioned above, RB is a major by-product of rice polishing. The beneficial effects and antioxidant properties of some chemical compounds contained in RB on IBD have been reported.14 RB contains some oligosaccharides and has prebiotic properties.44 Although the mixture of LAB, yeasts, and RB may have synergistic effects, the antioxidant and antiinflammatory activities of the FRB are still unclear.
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FIGURE 16.5 Images of colon and cecum (A), colon length (B), and hematoxylin eosin (HE)–stained colons (C) of mice administered normal chow (CE-2), CE-2, and 4% dextran sodium sulfate (DSS) in drinking water, high-fat diet (Quick Fat), or fiber-free diet (AIN-76 (-)). (D) Images of Gramstained cecal content in test mice.
5.1 Total Phenolic Content and Antioxidant Properties Before fermentation, the concentration of total phenolic compounds in the RB-AES was 71.2 μmol PGEq/mL, slightly decreasing to 62.8 μmol PGEq/mL during fermentation. The concentrations of total phenolic compounds in AES corresponding to 50% scavenging activity against 1,1-diphenyl-2-picrylhydrazyl (DPPH) and superoxide anion radical (O2 − ) were 31 and 16 μmol catechin equivalent/mL, respectively. The antioxidant activities were not affected by fermentation. The antioxidant activities of starter cells are shown in Fig. 16.7. DPPH radical scavenging capacity of L. plantarum Sanriku-SU8 was higher than that of their type strain (Fig. 16.7A). (O2 − ) radical scavenging activity was high in L. plantarum strains (Fig. 16.7B). This scavenging capacity in both L. plantarum and S. cerevisiae was increased by boiling for 20 min. It is concerning that proteins and other components of the cell membrane were denatured by the boiling.22 However, the increase in bile acid–lowering capacity of Satoumi LAB strains via boiling has been reported.26
5.2 Immune Promotion and Antiinflammation Activity in Murine Macrophage RAW264.7 Cells NO is a highly reactive free radical involved in a number of physical and pathological processes and may play an important role in the pathophysiology of various diseases. Its role in macrophage toxicity is well established.45 Furthermore, NO acts as a cytotoxic agent in immunological interactions between invading microorganisms and macrophages.46 Promotion of NO secretion by some functional materials is considered an immunostimulatory activity.17 However, NO production by antigens of pathogens, such as LPS of pathogenic Gram-negative bacterial cells, is regarded as inflammation. NO production was increased in the RB-AES, which increased further, following the treatment with FRB-AES (Fig. 16.8A). The cells, particularly L. plantarum Sanriku-SU8, had increased NO content (Fig. 16.8B). However, LPS-induced NO production was significantly lowered by RB-AES (Fig. 16.8C). This inhibitory property of RB-AES was not affected by fermentation and was not seen in the starter cells (Fig. 16.8D). These in vitro results suggest that FRB intake, rather than RB intake, in vitro promotes immune activity. Furthermore, we hypothesize that FRB and RB will show similar antiinflammatory activity in vitro.
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FIGURE 16.6 Heat map of the relative abundance of identified operational taxonomic units. DSS, dextran sodium sulfate.
FIGURE 16.7 1,1-Diphenyl-2-picrylhydrazyl (DPPH) (A) and superoxide anion (B) radical scavenging activities of cells of Lactobacillus plantarum Sanriku-SU8 and Saccharomyces cerevisiae Misaki-1.
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FIGURE 16.8 Effects of rice bran (RB), fermented RB (FRB), and heated FRB (HFRB) aqueous extract solutions (A and C) and cells of Lactobacillus plantarum Sanriku-SU8 and Saccharomyces cerevisiae Misaki-1 (B and D) on intact (A and B) and Escherichia coli O111 lipopolysaccharide (LPS)induced (C and D) nitric oxide (NO) release of RAW264.7 cells.
5.3 Protective Effects of FRB-AES in DSS-Induced IBD Model ICR Mice To determine the antiinflammatory effects of RB-, FRB-, and heat (boiling for 20 min)-treated RB (HFRB) AES on IBD, 5% (w/v) DSS in drinking water was administered to mice with or without the AES. After 6 days from the start of DSS feeding, the body weights in the DSS + DW and DSS + RB groups were lower than those in the other groups. Diarrhea and bloody bowel discharges were observed in mice from the DSS + DW and DSS + RB groups. The spleen weight of mice fed DSS + DW was twice that of the control (DW) group mice. The spleen enlargement was suppressed by FRBand HFRB-AES’s. The enlargement of the spleen and immune-related organs caused by DSS feeding has been previously reported.17 Colon length was shorter in the mice administered DSS + DW compared with that observed from the DW group mice. As mentioned above, this illustrates the activity index of the inflammation caused by IBD.17 FRB-AES, rather than RBand HFRB-AESs, did not have an extensive reduction in colon length (Fig. 16.9A and B). This result indicates that raw FRB-AES in drinking water significantly prevented IBD induced by DSS. Fig. 16.9C shows typical images of hematoxylin eosin–stained colon tissues. In the DW group, the sections of the crypt structure in the mucosal layer, the submucosa, and muscular layer were normal. In the DSS + DW group, the crypt structure and submucosa were irregular. These irregularities caused by DSS were suppressed by FRB-AES, while still present in RB- and HFRB-AES’s. As mentioned above, there are reports on the in vitro antioxidant activity of RB. Furthermore, the antiinflammatory effects of some chemical compounds, such as phytosteryl ferulates, in DSS-induced colitis have also been reported.14 However, as in the study, the effect of whole RB on IBD is still unclear. Although the antiinflammatory effect of RB in the RAW264.7 cells was not affected by the fermentation (Fig. 16.8C), that of RB-AES was clearly induced by the fermentation. One can hypothesize that part of the protective effect of FRB-AES on the IBD model mice might be caused by the starter cells themselves, which showed some antioxidant activity (Fig. 16.7). Some probiotics are considered to ameliorate IBD.47,48 Although the clear anti-IBD property of FRB-AES was highlighted in this experiment, further research on FRBAES active compounds, as well as the synergistic effect of RB and the L. plantarum and S. cerevisiae cells on IBD and other lifestyle diseases, is needed in the future.
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FIGURE 16.9 Colon lengths (A and B) and images of HE-stained colons (C) of mice administered distilled water (DW) and 5% (w/v) dextran sodium sulfate (DSS) with DW, RB-AES, FRB-AES, or heated FRB (HFRB) AES as drinking water. AES, aqueous extract suspension; FRB, fermented rice bran; HE, hematoxylin eosin; RB, rice bran.
6. CONCLUSION To improve the quality of blue shark and salmon shark meats, we examined how the ammonia content and participantranked preference for the different types of meat were affected by soaking the meat in 10% sugar and 5% salt solution containing RB or FRB generated from RB fermentation with L. plantarum Sanriku-SU8 and S. cerevisiae Misaki-1. Although the effects of this treatment on the meat quality were not clear in the fresh meat, it was more significant in the less fresh meat. Furthermore, FRB-AES soaking raised the preference ranking for chub mackerel, Pacific cod, and chicken breast meats. − RB-AES showed antioxidant (DPPH and O2 radical scavenging) and antiinflammatory effects (inhibition of LPSinduced NO secretion in murine macrophage RAW264.7 cells) in vitro. However, RB-AES did not suppress inflammation in 5% DSS-induced IBD model mice. On the other hand, FRB-AES clearly improved the activity index of inflammation in the IBD model ICR mice, and this anti-IBD effect decreased on heating. These results suggest that FRB-AES is a potential starter for both good taste and functional properties. Further research on FRB-AES active compounds, as well as the synergistic effect of RB and the L. plantarum and S. cerevisiae cells on other processes and functions, is needed in the future.
ACKNOWLEDGMENTS This work was partially supported by a research grant from the Ministry of Agriculture, Forestry, and Fisheries of Japan, Towa Foundation for Food Science and Research, Tokyo, Japan, TERRADA Warehouse, Nutrition Act Co., Tokyo, Japan, and Japan Food Chemical Research Foundation, Tokyo, Japan.
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FURTHER READING 1. Ito R, Shin-Ya M, Kishida T, et al. Interferon gamma islem- causatively involved in experimental inflammatory bowel disease in mice. Clin Exp Immunol 2006;146:330–8.
New Functional Properties of Fermented Rice Bran in Food Processing and Inflammatory Bowel Disease Model Mice Takashi Kuda Department of Food Science and Technology, Tokyo University of Marine Science and Technology, Tokyo, Japan
1. INTRODUCTION The blue shark, Prionace glauca, and salmon shark, Lamna ditropis, frequently land at fisheries ports in the north-eastern coastal region of Japan, Tohoku, particularly in the city of Kesennuma in the Miyagi prefecture. While shark body muscle meat is generally considered of a low value, the fins (especially those containing ceratotrichia) are a valuable commodity, evidenced by an increase in demand for shark fin soup among the Chinese middle class.1 The removal of shark fins and the subsequent discarding of the finless bodies are a significant ecological problem.2 In Japan, almost all meat obtained from the body of blue sharks is used for surimi (fish paste)–based products such as hampen.3 However, the heart of the salmon shark is consumed as part of the sashimi cuisine in Kesennuma and its body muscle meat is traditionally consumed as sashimi and cooked dishes in other areas, particularly in the inland region. Fresh muscle meat from these sharks does not smell of ammonia or other undesirable volatile compounds. However, shark meat can become odorous because of ammonia buildup over time. In elasmobranchs, which includes sharks, ammonia is generated from urea in the muscles as a part of osmotic balance.4 Occasionally, shark meat produces ammonia that smells relatively strong in a refrigerated stock room. In Japan, the water-leaching method is used to elute ammonia and urea from minced fish muscle meat. However, this process may only be used for surimi food products. Volatile basic nitrogen compounds, including ammonia, trimethylamine, and other volatile amines, are responsible for most of the pungent fishy odors emitted from seafood.5 These alkaline products readily dissolve in acidified solutions as opposed to alkaline and neutral solutions. As mentioned above, fresh shark meat should have no undesirable odor when used for sashimi. Therefore, it is commercially advantageous to develop strategies to improve the preference for less fresh fish meat over fresh fish meat. Rice bran (RB) is a major by-product of rice polishing. With the aim of reducing the ammonia content and improving the preference for meat from the blue shark, P. glauca, and salmon shark, L. ditropis, we evaluated the effect of soaking RB in solutions containing 10% sucrose and 5% NaCl in the form of an aqueous extract suspension (AES) of RB or fermented RB (FRB) generated from selected Lactobacillus plantarum and Saccharomyces cerevisiae strains.6,7 Inflammatory bowel disease (IBD) encompasses two forms of intestinal inflammation: ulcerative colitis (UC) and Crohn’s disease (CD). UC is a chronic disease characterized by diffuse inflammation of the rectal and colonic mucosa.8 The incidence rate of UC is high in the United States and Western Europe, reaching 34 and 263 per 100,000 children and adults, respectively, in 2009.9 Similarly, the number of cases in East Asian countries, such as Korea and Japan, has also increased in recent years.10,11 CD has a broad spectrum of clinical manifestations, and the initial presentation is seldom a good predictor of the clinical course. While the pathogenesis of IBD is not completely understood, oxidative stress caused by reactive oxygen species is considered one of the etiological factors involved in several symptoms of IBD.12 Therefore, many studies have reported the antioxidant properties of various foods and extracted compounds and their uses in IBD treatment.13 The beneficial effects and antioxidant properties of some chemical compounds contained in RB for IBD treatment have been reported.14 Recently, the beneficial effect of lactic acid bacteria (LAB) against dextran sodium sulfate (DSS)–induced murine IBD in relation to the superoxide anion radical scavenging capacity was studied.15,16 Some LAB strains suppressed nitric oxide (NO) secretion of murine macrophages, induced by the lipopolysaccharide (LPS) of pathogens.15,17 Dietary Interventions in Gastrointestinal Diseases. https://doi.org/10.1016/B978-0-12-814468-8.00016-8 Copyright © 2019 Elsevier Inc. All rights reserved.
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This chapter presents the new functional effects of FRB fermented using S. cerevisiae and L. plantarum on ammonia content and preference ranking in fresh and less fresh shark meats,6,7 as well as on DSS-induced IBD model mice.18
2. PREPARATION OF FERMENTED RICE BRAN FOR AMMONIA REDUCTION IN SHARK MEAT To use as a starter for fermented fish products, probiotics, and environmental remediation, LAB and yeasts were isolated from marine coast (Satoumi) environments and screened for resistance against acid, salt, and bile.19–32 Among the isolates, Saccharomyces cerevisiae Misaki-1 (Fig. 16.1A and B) isolated from algal beach casts was selected as an ammonialowering yeast by in vitro screening.6 Although there was no ammonia-lowering strain among the Satoumi LAB isolates, Lactobacillus plantarum Sanriku-SU8 (Fig. 16.1C) promoted the ammonia-lowering capacity of S. cerevisiae Misaki-1. Instead of ordinary broth media, Japanese RB, a major by-product of rice polishing, was used. Lightly roasted RB was autoclaved with a 10-fold volume of distilled water (DW) and filtered through a kitchen net. This AES of RB was fermented with a coculture of S. cerevisiae Misaki-1 and L. plantarum Sanriku-SU8 at 30°C for 48 h. During the fermentation, saccharides were converted to lactic acid and ethanol and the pH decreased from 6.5 to 4.3 (Fig. 16.2). Although the RB-AES had a rich RB odor, the FRB-AES had a slightly sweet honey odor.
FIGURE 16.1 Cellular morphology of the Saccharomyces cerevisiae Misaki-1 (A) using a phase-contrast microscope and (B) using an atomic force microscope, SPM-9000, Shimadzu, phase-contrast mode and Lactobacillus plantarum Sanriku-SU8 (C) using a Table Top SEM, TM3030, Hitachi, without treatment.
FIGURE 16.2 (A) Growth of Saccharomyces cerevisiae Misaki-1 and Lactobacillus plantarum Sanriku-SU8 coculture in 10% rice bran (RB) aqueous extract suspension (AES). (B) High performance liquid chromatography (HPLC) chromatogram for saccharides, lactic acid, and ethanol of the fermented RB (FRB) AES. (C) Image of the Misaki-1 and Sanriku-SU8 in FRB-AES observed under TM3030.
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3. EFFECT OF FERMENTED RICE BRAN ON AMMONIA CONTENT AND PREFERENCE RANKING IN SHARK AND OTHER FISH MEAT The soaking brine for the shark meat was made with 200 mL of FRB-AES, 100 g sucrose, 50 g table salt, and 800 mL water. From the results of several soaking experiments, the soaking brine volume to the meat weight ratio was set to 1:1, the temperature 10°C, and the time 48 h.7 In fresh shark meat, ammonia content was low (160–180 mg/kg, Fig. 16.3A and C) and the effects of RB and FRB were not significant. However, meat stored at 10°C for 48 h before the soaking treatment had high ammonia content (340–350 mg/kg, Fig. 16.3B and D) and the effects of RB and FRB were significant. After soaking, the redness of the meat, particularly in the salmon shark meat, decreased (Fig. 16.3E and G). After cooking, browning was observed in only the FRB-treated meat, particularly in blue shark meat (Fig. 16.3F). The browning may be from the Maillard reaction,33 which involves proteolysis and generation of reducing sugars by the yeast and LAB. After light sautéing, the meat slices were ranked from first (the most preferable) to fifth (the least preferable) by total preference. The beneficial effects of the RB and FRB on the preference were not significant in the fresh shark meat (Fig. 16.4 A and C) but significant in the less fresh shark meat (Fig. 16.4B and D). In this experiment, no participants could smell ammonia in any sample. However, comments were made about the reduction in fishy odor and improvements in the taste and texture, from “somewhat dry” to “somewhat moist, tender, and firm,” after soaking with FRB. The improved taste and texture might be caused by S. cerevisiae Misaki-1 protease activity on myofibrillar proteins (Fig. 16.4E and F) and protease activity on water-soluble proteins, which have been shown to correlate with the texture34 and taste,35 respectively. These positive effects of FRB on the meat texture and taste have also been shown previously7 with the chub mackerel fish, pacific cod fish, and chicken breast meat.
4. DIETARY AND LIFESTYLE DISEASE INDICES AND CECAL MICROBIOTA IN HIGH-FAT DIET, DIETARY FIBER-FREE DIET, OR DSS-INDUCED IBD MODELS IN CLOSED COLONY MICE Dietary and lifestyle-related chronic diseases such as obesity, type 2 diabetes, hypertension, and chronic immune IBD are of great concern worldwide.36,37 The relationship between these chronic diseases, gut microbiota, and some functional foods has been studied extensively in recent years.38 To study the beneficial effects of food on these chronic diseases, healthy inbred mice, particularly the BALB/c and C57BL/6 strains, are often used. Although these inbred mice provide
FIGURE 16.3 Effect soaking on ammonia content in fresh and stored blue shark and salmon shark meats. The fresh shark meats were stored at 10°C for 0 (A and C) and 2 (B and D) days. The meat was then soaked in sucrose-salt brine without RB (SS), brine with RB-AES, or brine with FRB-AES at 10°C for 2 days. (E and F) Images of soaked and soaked-cooked blue shark meat, respectively. (G) Images of soaked salmon shark meat. AES, aqueous extract suspension; FRB, fermented rice bran; RB, rice bran.
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FIGURE 16.4 Effect of soaking on preference ranking in fresh and stored blue shark and salmon shark meats. The fresh shark meats were stored at 10°C for 0 (A and C) or 2 (B and D) days. The meat was then soaked in SS, RB-AES, or FRB-AES at 10°C for 2 days. The participants ranked the five treatments from first (the most preferable) to fifth. (E and F) Images of sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) of crude myofibrillar protein of treated blue shark (E) and salmon shark (F) meats. AES, aqueous extract suspension; FRB, fermented rice bran; RB, rice bran.
reliable data with minimal individual variance, they are more susceptible to certain diseases. For example, BALB/c and C57BL/6 mice are more likely to suffer infection and obese–diabetes diseases, respectively.39 However, closed colony mice such as Institute of Cancer Research (ICR; CD-1) mice have reasonable genetic variation, good growth, and increased resistance to pathogenic bacteria.40 Therefore, ICR mice can be considered to exhibit the resistances similar to those of healthy humans. In our recent study41 to examine the relationship between multiple lifestyle-related diseases and IBD, ICR mice were fed normal chow (CE-2), CE-2 with DSS in drinking water, a high-fat diet (Quick Fat), or a fiber-free high-sucrose diet (AIN-76(-)). The ratio of low-density lipoprotein cholesterol to high-density lipoprotein cholesterol (LDL/HDL) was generally higher in the AIN-76(-) and DSS groups. Shortening of the colon, an indicator of IBD, was prominent in the AIN76(-) group (Fig. 16.5A and B). Damage of colon epithelial cells and layers was considerable in the DSS group and also observed in the Quick Fat and AIN-76(-) groups (Fig. 16.5C). Gram staining of cecal contents revealed that sporulation was promoted by DSS (Fig. 16.5D). The 16S rDNA amplicon sequencing of cecal contents showed that the ratio of bacteria from the phylum Firmicutes, particularly in Bifidobacterium, was high in the AIN-76(-) group (Fig. 16.6). In addition to Turicibacter, Bacteroides and Akkermansia muciniphila, which reportedly ameliorate obesity and immune reactions,42 were high in number in the DSS group. Although Allobaculum, previously reported as negative correlation bacteria to high-fat diet,43 was dominant in all diet groups, its operational taxonomic unit (OTU) was different in each group. Similarly, although Lactobacillus was dominant in all diet groups, some Lactobacillus OTUs such as Lactobacillus reuteri were low in the lifestyle disease and IBD model groups. In daily life, several factors affect disease progression. Therefore, consideration of the differences and similarities between the model mice is important for experiments on nutrition, food function, and toxicity.
5. PROTECTIVE EFFECTS OF FRB IN DSS-INDUCED IBD MODEL ICR MICE As mentioned above, RB is a major by-product of rice polishing. The beneficial effects and antioxidant properties of some chemical compounds contained in RB on IBD have been reported.14 RB contains some oligosaccharides and has prebiotic properties.44 Although the mixture of LAB, yeasts, and RB may have synergistic effects, the antioxidant and antiinflammatory activities of the FRB are still unclear.
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FIGURE 16.5 Images of colon and cecum (A), colon length (B), and hematoxylin eosin (HE)–stained colons (C) of mice administered normal chow (CE-2), CE-2, and 4% dextran sodium sulfate (DSS) in drinking water, high-fat diet (Quick Fat), or fiber-free diet (AIN-76 (-)). (D) Images of Gramstained cecal content in test mice.
5.1 Total Phenolic Content and Antioxidant Properties Before fermentation, the concentration of total phenolic compounds in the RB-AES was 71.2 μmol PGEq/mL, slightly decreasing to 62.8 μmol PGEq/mL during fermentation. The concentrations of total phenolic compounds in AES corresponding to 50% scavenging activity against 1,1-diphenyl-2-picrylhydrazyl (DPPH) and superoxide anion radical (O2 − ) were 31 and 16 μmol catechin equivalent/mL, respectively. The antioxidant activities were not affected by fermentation. The antioxidant activities of starter cells are shown in Fig. 16.7. DPPH radical scavenging capacity of L. plantarum Sanriku-SU8 was higher than that of their type strain (Fig. 16.7A). (O2 − ) radical scavenging activity was high in L. plantarum strains (Fig. 16.7B). This scavenging capacity in both L. plantarum and S. cerevisiae was increased by boiling for 20 min. It is concerning that proteins and other components of the cell membrane were denatured by the boiling.22 However, the increase in bile acid–lowering capacity of Satoumi LAB strains via boiling has been reported.26
5.2 Immune Promotion and Antiinflammation Activity in Murine Macrophage RAW264.7 Cells NO is a highly reactive free radical involved in a number of physical and pathological processes and may play an important role in the pathophysiology of various diseases. Its role in macrophage toxicity is well established.45 Furthermore, NO acts as a cytotoxic agent in immunological interactions between invading microorganisms and macrophages.46 Promotion of NO secretion by some functional materials is considered an immunostimulatory activity.17 However, NO production by antigens of pathogens, such as LPS of pathogenic Gram-negative bacterial cells, is regarded as inflammation. NO production was increased in the RB-AES, which increased further, following the treatment with FRB-AES (Fig. 16.8A). The cells, particularly L. plantarum Sanriku-SU8, had increased NO content (Fig. 16.8B). However, LPS-induced NO production was significantly lowered by RB-AES (Fig. 16.8C). This inhibitory property of RB-AES was not affected by fermentation and was not seen in the starter cells (Fig. 16.8D). These in vitro results suggest that FRB intake, rather than RB intake, in vitro promotes immune activity. Furthermore, we hypothesize that FRB and RB will show similar antiinflammatory activity in vitro.
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FIGURE 16.6 Heat map of the relative abundance of identified operational taxonomic units. DSS, dextran sodium sulfate.
FIGURE 16.7 1,1-Diphenyl-2-picrylhydrazyl (DPPH) (A) and superoxide anion (B) radical scavenging activities of cells of Lactobacillus plantarum Sanriku-SU8 and Saccharomyces cerevisiae Misaki-1.
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FIGURE 16.8 Effects of rice bran (RB), fermented RB (FRB), and heated FRB (HFRB) aqueous extract solutions (A and C) and cells of Lactobacillus plantarum Sanriku-SU8 and Saccharomyces cerevisiae Misaki-1 (B and D) on intact (A and B) and Escherichia coli O111 lipopolysaccharide (LPS)induced (C and D) nitric oxide (NO) release of RAW264.7 cells.
5.3 Protective Effects of FRB-AES in DSS-Induced IBD Model ICR Mice To determine the antiinflammatory effects of RB-, FRB-, and heat (boiling for 20 min)-treated RB (HFRB) AES on IBD, 5% (w/v) DSS in drinking water was administered to mice with or without the AES. After 6 days from the start of DSS feeding, the body weights in the DSS + DW and DSS + RB groups were lower than those in the other groups. Diarrhea and bloody bowel discharges were observed in mice from the DSS + DW and DSS + RB groups. The spleen weight of mice fed DSS + DW was twice that of the control (DW) group mice. The spleen enlargement was suppressed by FRBand HFRB-AES’s. The enlargement of the spleen and immune-related organs caused by DSS feeding has been previously reported.17 Colon length was shorter in the mice administered DSS + DW compared with that observed from the DW group mice. As mentioned above, this illustrates the activity index of the inflammation caused by IBD.17 FRB-AES, rather than RBand HFRB-AESs, did not have an extensive reduction in colon length (Fig. 16.9A and B). This result indicates that raw FRB-AES in drinking water significantly prevented IBD induced by DSS. Fig. 16.9C shows typical images of hematoxylin eosin–stained colon tissues. In the DW group, the sections of the crypt structure in the mucosal layer, the submucosa, and muscular layer were normal. In the DSS + DW group, the crypt structure and submucosa were irregular. These irregularities caused by DSS were suppressed by FRB-AES, while still present in RB- and HFRB-AES’s. As mentioned above, there are reports on the in vitro antioxidant activity of RB. Furthermore, the antiinflammatory effects of some chemical compounds, such as phytosteryl ferulates, in DSS-induced colitis have also been reported.14 However, as in the study, the effect of whole RB on IBD is still unclear. Although the antiinflammatory effect of RB in the RAW264.7 cells was not affected by the fermentation (Fig. 16.8C), that of RB-AES was clearly induced by the fermentation. One can hypothesize that part of the protective effect of FRB-AES on the IBD model mice might be caused by the starter cells themselves, which showed some antioxidant activity (Fig. 16.7). Some probiotics are considered to ameliorate IBD.47,48 Although the clear anti-IBD property of FRB-AES was highlighted in this experiment, further research on FRBAES active compounds, as well as the synergistic effect of RB and the L. plantarum and S. cerevisiae cells on IBD and other lifestyle diseases, is needed in the future.
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FIGURE 16.9 Colon lengths (A and B) and images of HE-stained colons (C) of mice administered distilled water (DW) and 5% (w/v) dextran sodium sulfate (DSS) with DW, RB-AES, FRB-AES, or heated FRB (HFRB) AES as drinking water. AES, aqueous extract suspension; FRB, fermented rice bran; HE, hematoxylin eosin; RB, rice bran.
6. CONCLUSION To improve the quality of blue shark and salmon shark meats, we examined how the ammonia content and participantranked preference for the different types of meat were affected by soaking the meat in 10% sugar and 5% salt solution containing RB or FRB generated from RB fermentation with L. plantarum Sanriku-SU8 and S. cerevisiae Misaki-1. Although the effects of this treatment on the meat quality were not clear in the fresh meat, it was more significant in the less fresh meat. Furthermore, FRB-AES soaking raised the preference ranking for chub mackerel, Pacific cod, and chicken breast meats. − RB-AES showed antioxidant (DPPH and O2 radical scavenging) and antiinflammatory effects (inhibition of LPSinduced NO secretion in murine macrophage RAW264.7 cells) in vitro. However, RB-AES did not suppress inflammation in 5% DSS-induced IBD model mice. On the other hand, FRB-AES clearly improved the activity index of inflammation in the IBD model ICR mice, and this anti-IBD effect decreased on heating. These results suggest that FRB-AES is a potential starter for both good taste and functional properties. Further research on FRB-AES active compounds, as well as the synergistic effect of RB and the L. plantarum and S. cerevisiae cells on other processes and functions, is needed in the future.
ACKNOWLEDGMENTS This work was partially supported by a research grant from the Ministry of Agriculture, Forestry, and Fisheries of Japan, Towa Foundation for Food Science and Research, Tokyo, Japan, TERRADA Warehouse, Nutrition Act Co., Tokyo, Japan, and Japan Food Chemical Research Foundation, Tokyo, Japan.
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FURTHER READING 1. Ito R, Shin-Ya M, Kishida T, et al. Interferon gamma islem- causatively involved in experimental inflammatory bowel disease in mice. Clin Exp Immunol 2006;146:330–8.