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. 2022 May 30;31(7):819–825. doi: 10.1007/s10068-022-01096-x

Rice yogurt with various beans fermented by lactic acid bacteria from kimchi

Yeon Hwa Choi 1, Myung Joo Han 1,✉
PMCID: PMC9203620  PMID: 35720458

Abstract

In this study, the rice yogurt with various beans was developed using a mixture of rice saccharification solution as an artificial sweetener substitute and bean milk as a milk substitute. Rice yogurt was fermented with lactic acid bacteria isolated from kimchi. The lactic acid bacteria count in rice yogurt with various beans had the highest range of 9.37- 9.54 log CFU/g at 12 h fermentation. Also, at 12 h fermentation, pH ranged from 4.05 to 4.20. Rice yogurt with seoritae had the highest brix (15.52°Bx) and DPPH radical scavenging activity (41.86%). In the sensory evaluation, rice yogurt with seoritae received high preference scores in most categories, including flavor, sweet taste, sour taste, mouthfeel and overall preference. These findings suggest that the optimum fermentation time may be 12 h, and rice saccharification solution is an appropriate sugar substitute. Seoritae milk is suitable for the development of rice yogurt with beans.

Keywords: Rice yogurt, Rice saccharification solution, Bean milk, Lactic acid bacteria, Fermentation

Introduction

Rice is one of the most important grains in the world, and it is also an important food resource in Korea (Lee and Shin, 2006). Unlike wet rice flour, the storage and distribution of dry rice flour is convenient and economical. Therefore, it is easy to develop a processed rice flour product. Rice flour contains a large amount of starch, so it is considered suitable as an additive that can increase the viscosity of yogurt (Paik et al., 2004). Fermented cereals have improved nutritional value, sensory qualities, digestibility, and shelf life compared to unfermented cereals (Jo et al., 2021). Thus, rice is one of the best candidate for non-dairy probiotic food (Sen et al., 2020). The resistant starch in rice is a bioactive substance and is classified as an insoluble dietary fiber because it is not digested or absorbed in the body (Oh et al., 2000). It prevents colon cancer and lowers cholesterol levels to prevent cardiovascular disease (Kim et al., 2000).

Soy milk contains many essential amino acids, and the composition of essential amino acids is similar to that of milk. Also, since soy milk does not contain lactose, it can be used as a high-protein milk substitute for infants with milk allergies and does not cause digestive problems in lactose intolerant individuals (Pyun and Hwang, 1996). Soy milk contains many bioactive substances. Among them, isoflavones are composed of daidzein, genistein, glycitein and their glycosides and various derivatives, and have been reported to have a similar structure and activity to estrogen, a female hormone (Shon, 1997). Therefore, soy milk is not only low in cholesterol, it is also a good bioactive substance for preventing adult diseases (Kim et al., 2014).

Yogurt is a nutrient-dense probiotic food that enhance the bioavailability of some of these nutrients (El-Abbadi et al., 2014). Plain or sweetened yogurt is a popular food in many cultures (Craig and Brothers. 2021). LAB-fermented foods could represent a safe, unexpensive, and reliable tool in improving human health (Castellone et al., 2021). Probiotics are living, non-pathogenic microorganisms such as lactic acid bacteria (LAB), and when ingested have positive physiological effects on the host (Schrezenmeir et al., 2001). Some of the important health functions are stimulating the immune system to aid digestion and protect the host from the invasion of bacteria and viruses (Gupta and Garg, 2009). It also prevents colon cancer.

In this study, we isolated LAB strains from kimchi, inoculated in rice yogurt with various kinds of bean milk, and investigated whether rice saccharification solution can replace sugar as a sweetener in rice yogurt. Also, the optimal bean type and fermentation time were determined based on the quality characteristics and sensory evaluation results of rice yogurt with various beans.

Materials and methods

Materials

Rice powder was purchased from Haetssal Maru Co. (Korea). Soybean, yakkong (small black bean) and seoritae (green kernel black bean) were purchased from Yanggok Nongyub (Korea). Barley malt was purchased from Navigol Nongyub (Korea). Water used to make rice saccharification solution was mineral water from DongA-Otsuka Co. (Korea).

LAB strains and culture conditions

LAB strains were isolated from kimchi according to the method of Jang et al. (2013). Briefly, The Chinese cabbage kimchi liquid (1 mL) was diluted in MRS broth sequentially, planted in MRS agar plates, and anaerobically cultured at 37 °C for 48 h. The grown colonies were selected and identified on the basis of the results of gram staining, 16S rDNA sequencing, and API 50 CHL kit. Among identified microbes, Leu. mesenteroides (LM) and Lactiplantibacillus plantarum (LP) with the potent DPPH radical scavenging activity were selected for the fermentation of rice yogurt. For the control group, commercial Leu. mesenteroides KCTC13302 and L. plantarum KCTC33131 were purchased from Korean Collection for Type Culture. These LAB strains were cultured in MRS broth at 30 °C for 24 h prior to inoculation.

Preparation of rice saccharification solution and bean milk

Malt and mineral water were soaked for 2 h and filtered with a 200 mesh sieve. Rice powder was added to soaked malt water (1:3 ratio) and then saccharified at 65 °C for 3 h. After saccharification was over, it was boiled at 100 °C for 3 min and cooled to 40 °C.

To prepare various bean milk, soybean, yakkong and seoritae were used. Various beans were washed and soaked in water for 24 h at 4 °C and then blended with a Halde cutter VCB-61 (Hallde Maskiner, Kista, Sweden). The ground bean mixture was strained through a 200 mesh sieve and then filtered one more time with cotton cloth. Mineral water was added to filtered bean milk until it became 7 Bx. The bean milk was boiled for 3 min and then cooled until it became 40 °C (Chang et al., 2010).

Mixed LAB starter (LM and LP), which was decided on the basis of the ratio of LM and LP found in the well-fermented kimchi (Lee et al., 1992; Lee, 1999), were inoculated to 1 (w/v)% each saccharified rice solution and bean milk at the level of 108 CFU/mL. For control, rice yogurt with soymilk was inoculated with commercial strains. Then they were fermented at 30℃ for 0, 9, 12, 15, and 18 h.

Microbiological analysis and pH

During 18 h fermentation, LAB counts were examined at 0, 9, 12, 15, and 18 h. The serially diluted sample (0.1 mL) was inoculated onto de Man Rogosa Sharpe (MRS) agar (BD, USA) and the plates for LAB were incubated at 30 °C for 48 h. The numbers of LAB strains were counted and presented as log CFU/mL. Five grams of rice yogurts were mixed with 45 mL of distilled water and stirred for 1 min to analyze pH. The pH of samples was measured 3 times with a digital pH meter (Thermo Orion, USA).

Brix and reducing sugar content

The Brix value of samples was measured 3 times by refractometer (Atagoni, Japan). The reducing sugar content was determined by the di-nitrosalicylic acid (DNS) method (Miller, 1959). One gram of sample was diluted in 49 mL of distilled water and stirred for 1 min. The mixture was centrifuged at 3000 × g for 20 min (Vision Sci Co., Korea). One milliliter of the supernatant was mixed with 3 mL of DNS solution in the test tube, then heated for 5 min in boiling water bath, and cooled in ice water to stop the reaction. The absorbance was measured at 550 nm using a spectrophotometer (UV-2101, Shimadzu, Kyoto, Japan). The amount of reducing sugar of each sample was calculated from measured absorbance using the glucose standard curve.

Color

Hunter color meter (Color Techno System Co., Japan) was calibrated with a standard calibration plate of a white surface before color measurement. Hunter L (lightness), a (red + / green -), b (yellow + / blueness −) values of samples were measured 3 times.

DPPH radical scavenging activity

2,2-Diphenyl-1-picrylhydrazyl (DPPH) radical scavenging activity was determined according to the method of Blois (1958) with some modification. Two grams of sample was diluted in 2 mL of 80 (v/v)% ethanol and centrifuged at 3000 × g for 20 min (Vision Sci. Co., Korea). The 0.5 mL aliquot of the supernatant was mixed with 1 mL of 0.4 mM DPPH-ethanol solution. To make DPPH-ethanol solution, DPPH was purchased from Sigma Co. (St Louis, MO, USA). The mixture was strongly shaken and allowed to stand for 30 min at room temperature in the dark. The absorbance was measured at 517 nm using a spectrophotometer (UV-2101, Shimadzu, Kyoto, Japan).

Amylase activity

The amylase activity was determined by using the DNS method (Miller, 1959). After mixing in 5 mL of 1 (w/v)% soluble starch solution, 13 mL of 0.1 M sodium phosphate buffer (pH 7.0) and 1 mL of 1 (w/v)% calcium chloride solution, the mixture was heated at 37℃ for 5 min in a water bath (Shanghai Eyela Co., Japan). One milliliter of the reaction mixture was added to it and heated at 37 °C for 20 min in a water bath. Then 3 mL of DNS solution was added to the mixture and it was boiled for 5 min and cooled for 5 min in ice water to stop the reaction. The absorbance at 550 nm was measured using a spectrophotometer (UV-2101, Shimadzu, Kyoto, Japan). Using the glucose standard curve to obtain enzyme activity, the number of enzymes that produce 1 μmole of glucose equivalent per min was defined as one unit.

Sensory evaluation

This study received the approval of the institutional review board (IRB) of Kyung Hee University (KHSIRB-20–371) to follow bioethics. The sensory evaluation of the rice yogurt with various beans was conducted in the accordance with the rules of IRB. Rice yogurt with various beans was fermented for 12 h at 30 °C, and then the rice yogurt samples were homogenized and kept in a refrigerator at 4 °C for sensory evaluation. The rice yogurt samples were provided in a transparent disposable cup randomly coded with a three-digit number. Water was provided to rinse the mouth before evaluating other samples. Forty-three general panelists were recruited and the test was carried out to evaluate color, flavor, sweet taste, sour taste, mouthfeel test and overall preference using a 7-point hedonic scale (1 = dislike very much; 7 = like very much).

Statistical analysis

All experiments were performed three times. The statistical analysis of the data was conducted with SAS statistical software program (SAS 9.4 version; SAS Institute, Cary, NC USA). The values for each data were indicated as mean ± standard deviation. Analysis of variance (ANOVA) was performed to compare multiple group means, followed by Duncan’s multiple range test to determine statistically significant (p < 0.05) difference.

Results and discussions

Microbiological analysis and pH

The changes in LAB (log CFU/g) of rice yogurts with various beans during 18 h fermentation are shown in Fig. 1A. The initial LAB counts of rice yogurts had a range of 7.29–7.45 log CFU/g. At 9 h fermentation, The LAB counts considerably increased in all rice yogurts and had the range of 9.31–9.47 log CFU/g. At 12 h fermentation, LAB counts in all samples showed the range 9.37–9.54 log CFU/g. Then, rice yogurts with seoritae (9.48 log CFU/g) and yakkong (9.48 log CFU/g) had no significant difference in LAB count until 18 h. Rice yogurt with soybean decreased from 9.54 log CFU/g at 12 h to 9.33 log CFU/g at 18 h.

Fig. 1.

Fig. 1

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LAB counts (A) and pH (B) of rice yogurts with various beans during 18 h fermentation. a,b,cMeans in each fermentation time followed by different superscripts are significantly different at the p < 0.05 level

Kim et al. (2014) reported that the number of lactic acid bacteria in yogurt with rice flour was 8.71 and 8.93 log CFU/mL at 8 and 10 h of fermentation, respectively. Similarly, in this study, most of rice yogurts showed the highest number of lactic acid bacteria counts at 12 h fermentation. According to the Korean Ministry of Food and Drug Safety (2020), the LAB counts of fermented dairy products have to be above 107 CFU/mL. Thus, it is suggested that the LAB counts of rice yogurts with various beans in this study have appropriate numbers during 18 h fermentation. In addition, the isolated LAB (LM and LP) could be used as a suitable starter for rice yogurts.

The changes in pH of rice yogurts with various beans during 18 h fermentation is shown in Fig. 1B. The initial pH of rice yogurt had a range of 6.25–6.45 and significantly declined to 4.05–4.20 at 12 h. After that, the pH slightly decreased to 3.77–3.98 until 18 h fermentation. During 18 h fermentation, the pH of rice yogurts with various beans were shown to decrease as fermentation proceeded in all rice yogurts. Pak et al. (2006) reported that yogurt manufactured from skimmed milk reached pH 4.5 at 6 h fermentation, but the pH yogurt with rice bran added yogurt decreased faster, and as more was added, it decreased faster. This is because the addition of rice promotes the production of lactic acid bacteria, and the milk-only yogurt is buffered by phosphate and citrate in milk. Granata and Morr (1996) reported that a pH value of 4.0–4.4 is required for good quality yogurt. Jang et al. (2002) found that the pH range of lactic acid drinks, which suit Korean tastes, is 3.87 to 4.2. According to the above research results, the pH range (4.05–4.20) of rice yogurts with various beans at 12 h fermentation considered the most appropriate fermentation time.

Brix and reducing sugar content

The changes in Brix of rice yogurts with various beans during 18 h fermentation are shown in Fig. 2A. The initial Brix was 16.77–17.95°Bx and then decreased to 15.11–15.52°Bx at 12 h and 14.77–15.25°Bx at 18 h fermentation. In particular, the Brix of seoritae (15.52°Bx) had the highest value among samples at 12 h. Commercial yogurt in Korea has a range of 16.2–22.2°Bx (Kim et al., 1993). Rice yogurts with various beans is slightly lower than commercial yogurt. However, the use of rice saccharification solution for rice yogurts is considered appropriate as a substitute for sugar.

Fig. 2.

Fig. 2

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Brix (A) and reducing sugar content (B) of rice yogurts with various beans during 18 h fermentation. a,b,cMeans in each fermentation time followed by different superscripts are significantly different at the p < 0.05 level

The changes in reducing sugar content of rice yogurts with various beans during 18 h fermentation is shown in Fig. 2B. The initial sugar content had a range of 4.91–5.27 (w/v)% and as fermentation progressed, it decreased to 4.03–4.63 (w/v)% at 12 h and 3.70–4.39 (w/v)% at 18 h. Kim and Han (2019) reported that the reducing sugar content of soy yogurt without any sugar was 2.78 (w/v)% at 48 h of fermentation. Because of the rice saccharification solution, the reducing sugar content of rice yogurts with various beans was higher than soy yogurt without sugar. This is because of the glucose, maltose and fructose produced by the saccharification of grains such as rice and the action of amylase (Kwon et al., 2013). Similarly, Kim et al. (2015) reported that reducing sugar is reduced during fermentation because reducing sugar is used as a nutrient source from microorganisms such as LAB and at the same time converted into substances such as organic acids, alcohols and carbon dioxide. In general, the greatest reducing power is closely associated with antioxidant capabilities (Yen et al., 2000). The sugar content of plain yogurt on the market in Korea had a range of 4.02–4.32 (w/v)% during 2 weeks of storage (Kim et al., 2008). This is very similar to the range of rice yogurt with various beans [4.03–4.63 (w/v)%) at 12 h fermentation.

Color

The changes of Hunter color L values of rice yogurts with various beans during 18 h fermentation are shown in Fig. 3A. The initial L values, indicating lightness, had a range of 50.96–68.06 and increased to 53.64–70.45 after 18 h fermentation. Rice yogurt with soybean had the highest L value (70.24) among the samples. The L value was relatively high in soybean and C_soybean samples. The changes of Hunter color a values of rice yogurts with various beans during 18 h fermentation are shown in Fig. 3B. The initial a values had a range of − 2.41- − 0.11. After 18 h fermentation, seoritae and yakkong samples increased from − 1.21 and − 0.11 to 7.24 and 10.17. Soybean slightly increased from – 2.43 to − 2.23, and C_soybean showed no significant change.

Fig. 3.

Fig. 3

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Hunter color L (A), a (B) and b (C) of rice yogurts with various beans during 18 h fermentation. a,b,c,dMeans in each fermentation time followed by different superscripts are significantly different at the p < 0.05 level

The changes of Hunter color b values of rice yogurt with various beans during 18 h fermentation are shown in Fig. 3C. The initial b value of soybean sample increased from 11.64 to 13.28 at 18 h fermentation. On the other hand, seoritae and yakkong sample decreased from 8.95 and 6.85 to 7.34 and 4.97, respectively. Rice yogurt with yakkong and seoritae became a darker red color as fermentation progressed, while rice yogurt with soybean became more yellow. Lim (2016) measured the chromaticity of soy yogurt fermented by Lactobacillus delbrueckii subsp. bulgaricus, and reported that the L value was 73.90, a value was 3.09, and b value was 23.44. These are a slightly higher values than rice yogurt with soybean because it was diluted with the addition of rice saccharification solution. Sung and Choi (2014) measured the chromaticity of yogurt with added mulberry powder, which is rich in anthocyanin like black beans, and the L value was 70.61, a value was 6.41, and b value was 3.55. These results are similar to rice yogurt with seoritae and yakkong samples in our study.

DPPH radical scavenging activity and amylase activity

The changes of DPPH radical scavenging activity of rice yogurt with various beans during 18 h fermentation are shown in Fig. 4A. The initial DPPH radical scavenging activity of rice yogurts was 18.23–27.01% and increased to 37.59–41.68% at 12 h fermentation. After that, most of rice yogurts showed a gradual decline. Rice yogurt with seoritae measured the lowest activity (18.23%) at 0 h, measured the highest activity (41.68%) at 12 h, and then decreased until 18 h fermentation. DPPH is a stable free radical with an unmatched valence electron at an atom of nitrogen bridge and DPPH radical scavenging activity is the basis of the well-known DPPH antioxidant assay (Sharma and Bhat, 2009).

Fig. 4.

Fig. 4

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DPPH radical scavenging activity (A) and amylase activity (B) of rice yogurts with various beans during 18 h fermentation. a,b,cMeans in each fermentation time followed by different superscripts are significantly different at the p < 0.05 level

The changes of amylase activity of rice yogurts with various beans during 18 h fermentation are shown in Fig. 4B. The initial activity of amylase was 2.02–3.61 unit/g and increased up to 5.23–7.43 unit/g at 18 h fermentation. At 12 h fermentation, the amylase activity of rice yogurt with soybean had a lower value (5.93) than those with seoritae (7.76), yakkong (7.85), and C_soybean (7.91). Rice yogurt with C_soybean, a commercial lactic acid bacteria starter, showed higher amylase activity than that with soybean fermented by lactic acid bacteria isolated from kimchi. Yang et al. (2013) reported that there was little amylase activity of soy yogurt inoculated with only LP, while soy yogurt fermented with Bacillus subtilis and LP had a value of 8.13 unit/mL. In our study, it is expected that rice yogurt with various beans fermented by mixed LM and LP could also be used as amylolytic lactic acid bacteria.

Sensory evaluation

The sensory evaluation results of rice yogurts with various beans fermented for 12 h are shown in Table 1. The color scores of rice yogurt with various beans were in a range of 4.81–5.26, and there was no significant differences among samples. The flavor of rice yogurt with various beans had a range of 3.95–5.00. Rice yogurt with seoritae (5.00) had the highest flavor score, followed by yakkong (4.44), C_soybean (4.19) and soybean (3.95). Rice yogurt with seoritae (4.84) had a higher sweet taste than yakkong (4.07), soybean (4.04) and C_soybean (3.81). The preference of sour taste of rice yogurt with seoritae (5.02) had significantly higher than those of soybean (4.26), yakkong (4.19), and C_soybean (3.91). Rice yogurt with seoritae (5.21) showed the highest mouthfeel score, followed by yakkong (4.49), soybean (4.02) and C-soybean (3.86). The overall preference of rice yogurt with seoritae (5.19) was significantly higher than those of yakkong (4.37), soybean (4.12), and C_soybean (4.00). Rice yogurt with seoritae obtained excellent preference scores in most of sensory evaluations except color. Therefore, it is considered that rice yogurt with seoritae milk will produce the most superior rice yogurt with bean.

Table 1.

Sensory scores of rice yogurts with various beans fermented for 12 h

Sample2 Sensory scores1
Color Flavor Sweet taste Sour taste Mouthfeel test Overall preference
Soybean 4.81 ± 0.96 3.95 ± 1.17b 4.04 ± 1.25b 4.26 ± 1.26b 4.02 ± 1.12bc 4.12 ± 1.12b
Seoritae 5.19 ± 1.52 5.00 ± 1.45a 4.84 ± 1.60a 5.02 ± 1.52a 5.21 ± 1.25a 5.19 ± 1.53a
Yakkong 5.26 ± 1.18 4.44 ± 1.12ab 4.07 ± 1.26b 4.19 ± 1.48b 4.47 ± 1.33b 4.37 ± 1.57b
C_soybean 4.93 ± 1.33 4.19 ± 1.69b 3.81 ± 1.42b 3.91 ± 1.48b 3.86 ± 1.42c 4.00 ± 1.51b
F value 1.18 (p = 0.3205) 4.58 (p = 0.0041) 4.41 (p = 0.0052) 4.75 (p = 0.0033) 9.46 (p < .0001) 5.88 (p = 0.0008)
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1Sensory scores are indicated as follows: 1 = dislike very much, 7 = like very much

2Rice yogurts with soybean, seoritae, yakkong fermented by LAB (mixed LM and LP) from kimchi, C_soybean is a rice yogurt sample with commercial LAB, KCTC13302 and KCTC33131

a,b,cMeans in a column followed by different superscripts are significantly different at the p < 0.05 level

Based on this study, the optimum fermentation time for rice yogurt with various beans to be a good preference and have excellent quality may be 12 h. Also, rice saccharification solution can replace sugar as sweetener in rice yogurt with various beans. Rice yogurt with seoritae fermented by LM and LP from kimchi as a starter has the highest number of lactic acid bacteria (9.60 log CFU/g) at 15 h fermentation among all samples. At 12 h fermentation, rice yogurt with seoritae had an appropriate pH, and the highest brix and DPPH radical scavenging activity. In the sensory evaluation, it also scored high in preferences for flavor, sweet taste, sour taste, mouthfeel, and overall preference. As a result, rice yogurt with seoritae is expected to be excellent in both quality characteristics and sensory evaluation.

Declarations

Conflict of interest

The authors declare no conflict of interest.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Yeon Hwa Choi, Email: yeonas2@naver.com.

Myung Joo Han, Email: mjhan@khu.ac.kr.

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