Impact of Elaeagnus angustifolia flour added to bio-yogurt on probiotic survival and monitoring of in vitro acid tolerance in synthetic gastric fluid

Abstract

The present study aimed to investigate the effect of oleaster flour on Lactobacillus acidophilus, L. delbrueckii subsp. bulgaricus, and Bifidobacterium animalis subsp. lactis in probiotic yogurt during its storage period and whether oleaster flour has a protective effect against gastric fluid for these probiotic bacteria. For that purpose, the effect of oleaster flour at different doses (1%, 2%, and 3% w/v) on the titratable acidity, pH, and microbiological properties was investigated throughout cold storage. In addition, on the first day of storage, in vitro tolerance of probiotics in pH adjusted to (pH 2.0-ph 4.0) simulated gastric fluid was investigated for 1, 60, 120, and 180 min. Yogurt with a higher dosage (2%-3%) of oleaster flour had a higher pH and lower titratable acidity. Moreover, the addition of 3% oleaster flour showed a preservative effect on L. acidophilus, L. delbrueckii subsp. bulgaricus and B. animalis subsp. lactis during storage. On the first day of storage in pH 4.0 for synthetic gastric fluid, in vitro acid tolerance of all probiotics showed stability for 180 minutes. Also, at pH 2.0 SGF, B. animalis subsp. lactis was below the detectable limit in the control and 1% of groups. However, the 2% and 3% groups showed nearly 3 log cfu/g viability at the end of 180 min. These positive effects were related to the buffering effect of the oleaster peel. Thus, these results could prove that oleaster flour can be used for the production of bio-yogurt.

Keywords:
Bio-yogurt; Probiotic survive; Gastric tolerance; Oleaster; Bifidobacterium animalis subsp. lactis; Lactobacillus acidophilus

HIGHLIGHTS

• Oleaster peel may have a buffering effect on milk acidity

• The acid tolerance of probiotics may increase when oleaster fruit is added to the yogurt

• To improve quality, bio-yogurt can be fortified with 2% and 3% of oleaster flour

1 Introduction

The functional food industry needs to discover new areas due to increasing consumer demands for public health. As conscious consumers know, dairy-based functional products improve the function of the immune system and reduce cancer risks (Pandey et al., 2016; Sarkar, 2019; Yildiz & Ozcan, 2019). Particularly, yogurt is a long-time known and consumed milk product thus comprising fermented milk with standard symbiotic starter cultures. In general, yogurt can be separated into two groups: standard culture yogurt and bio-yogurt (probiotic yogurt). Standard culture contains two species of bacteria named Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus. These strains may not play a well role as probiotics in the host (McFarland, 2015; McKinley, 2005; Sarkar, 2019). Meanwhile, bio-yogurt, or probiotic yogurt, is supported with probiotic strains such as Bifidobacterium animalis subsp. lactis, L. acidophilus, L. brevis, etc. (Meybodi et al., 2020). Probiotics are simply defined as live microorganisms that provide health benefits to users when consumed in sufficient numbers (Hill et al., 2014). Therefore, probiotic products need to contain an adequate number of viable probiotic cultures from at least 6 to 9 log CFU per serving at that time of consumption to certify their health effects (Kaur et al., 2022). When bio-yogurt is consumed, probiotic bacteria must first survive the passage through the upper gastrointestinal tract and then linked to provide beneficial effects to the host. It's known that the low pH of gastric juice and the antimicrobial effect of gastric pepsin act as hurdles against the transportation of bacteria into the intestinal tract. Generally, the pH of the stomach varies between 2.5 and 3.5. However, it may range from 1.5 to 6.0 in relation to food intake depending on some factors such as diet (excessive protein intake), anti-acid drug use, age, etc. (Abuhelwa et al., 2017; Huang & Adams, 2004). Foods are the predominant delivery system for probiotic bacteria throughout the gastrointestinal tract. Even if fermented milk is a relatively good protector for ingested bacteria under gastrointestinal tract conditions, some research has shown that so many factors, such as storage conditions, acidity, and oxidative stress, affect the survival of these bacteria. Consequentially, these factors decrease the viability of probiotic bacteria in a short time (Champagne et al., 2018; Thomas, 2016).

Elaeagnus angustifolia L., often known as oleaster, Russian olive, or silver berry, is a member of the Elaeagnacea (Araliaceae) family and has more than 90 species. It is mostly grown in parts of Asia, Europe, and North America. The oleaster (E. angustifolia L.) is defined as a relatively small, reddish brown, elliptical fruit (Hamidpour et al., 2016). Also, these fruits have high nutritional value. Approximately, oleaster contains 27.1% of glucose, 22.3% of fructose, and 12% of protein (Akbolat et al., 2008; Sahan et al., 2015). Previously, the oleaster flour (OF) effect on set-type yogurt physicochemical, textural, and microstructural characteristics was researched by Öztürk et al. (2018). According to Öztürk et al. (2018), yogurt enrichment with OF accelerated the fermentation time, reduced syneresis, enhanced cohesiveness and viscosity index, and improved antioxidant activity. Moreover, researchers didn’t observe any statistical difference between the control and 2% of oleaster samples with regards to flavor or general acceptability in sensory properties. Besides all these positive effects, may oleaster also positively affect the probiotic cultures in bio-yogurt? To the best of our knowledge, there is limited information in the literature about the effect of oleaster flour on probiotic microorganisms. Thus, current research has two aims. The first one was to investigate the effect of oleaster flour on L. acidophilus, L. delbrueckii subsp. bulgaricus, and Bifidobacterium animalis subsp. lactis in probiotic yogurt during its storage period. The second aimed to investigate whether oleaster flour has a protective effect against gastric fluid for these probiotic bacteria.

2 Materials and methods

The oleaster fruits were purchased from a local market. The OF was prepared as described by Öztürk et al. (2018). The unpeeled oleaster fruits were pitted and incubated for 12 h at 30 °C. Afterward, the oleasters were milled with an ultra-centrifugal mill (ZM 200, Retsch, Germany). Commercial UHT sterile whole milk (3% of fat, 3% of protein, and 4.5% of carbohydrates) and commercial freeze-dried yogurt culture (VİVO, Food and Dairy Product Industry and Trade Co. Ltd.) in a direct vat set containing S. thermophilus, L. acidophilus, L. delbrueckii subsp. bulgaricus, and B. animalis subsp. lactis (at least 9 log cfu/g) were purchased from a local market.

2.1 Yogurt production and groups

The standardized whole milk without any treatment was used as a control for experimental yogurt production. In the present study, OF was added to milk at a concentration of 1.0%, 2.0%, and 3.0% (w/v). For each group, heat treatment was used at 90 ± 2 °C for 10 minutes and then cooled to 42 ± 2 °C. The milk was then inoculated with freeze-dried yogurt cultures in the amount recommended by the manufacturer (1 vial/5L) and thoroughly mixed with a sterile spoon. The groups were poured into the sterilized cups (200 ml) and incubated at 42 ± 2 °C. When the pH level hit around 4.6, fermentation was stopped, and samples were closed with a lid and cooled to 4 ± 2 °C in the refrigerator (Figure 1).

Figure 1
Schematic illustration of the preparation of oleaster flour, preparation of yogurt with oleaster flour, and analyses.

2.2 pH and Titratable acidity analyses

Titratable acidity was determined using the titration method (Tyl & Sadler, 2017), and pH values were measured by using a digital pH meter (Hanna Instruments, HI-4221, USA).

2.3 Microbiological analyses

All microbiological analyses were performed using the pour plate method described in the ISO standard (International Organization for Standardization, 2003). Lactobacillus acidophilus and L. delbrueckii subsp. bulgaricus were enumerated using pH-modified MRS agar base (Himedia, Mumbai, India) (pH 5.2, anaerobic, 43 ± 1 °C, 72 h) (Tharmaraj & Shah, 2003). For the enumeration of S. thermophilus, M17 agar base (Himedia, Mumbai, India) (aerobic, 35 ± 1 °C, 48 h) was used (Corry et al., 2003). For enumeration of B. animalis subsp. lactis, modified MRS (mMRS) agar was used as previously described by Allgeyer et al. (2010). To prepare mMRS, 5 mL of a 10% L-cysteine hydrochloride solution (LCH, Merck, Darmstadt, Germany), 10 mL of an 11% lithium chloride (LiCl) solution (Merck, Darmstadt, Germany), and 5 mL of a 0.01% dicloxacillin antibiotic solution (Merck, Darmstadt, Germany) were added per liter of MRS agar base. The plates were incubated under anaerobic conditions at 35±1 °C for 72 hours. Microbiological analyses were measured after 1, 7, 14, 21, and 28^th days of storage at 4 ± 2 °C.

2.4 Monitoring of in vitro gastric tolerance analysis

Synthetic gastric fluid (SGF) was prepared to determine in vitro gastric tolerance to probiotic bacteria in formulated yogurt. Briefly, Pepsin (1:10 000, ICN) (Merck, Darmstadt, Germany) was suspended to the ultimate concentration of 3 g/L in sterile NaCl (0.05%). Then, a prepared solution was filtered and sterilized (0.22-μm SFCA syringe filter). SGF was prepared considering the pH changes in the stomach, which were brought to two different pH values. The solution of pH was adjusted to 2.0 and 4.0 with concentrated HCl (Huang &Adams, 2004). On the first day of storage, one gram of yogurt from each group was transferred into sterile falcon tubes containing 9 mL of gastric juice (adjusted pH 2 and pH 4) at 37 °C. The mixtures were homogenized by using a vortex for 10 s and incubated at 37 °C. Afterward, 1 mL of aliquots was removed from mixtures after 1, 60, 120, and 180 min for determine gastric juice tolerance. Samples were serially diluted with 0.1% peptone water, and then Lactobacillus and B. animalis subsp. lactis counts were determined as previously described.

2.5 Statistical analyses

All data analyses were performed using a computer program (SPSS software version 21). Changes in bacterial count, gastric tolerance analysis, pH, and titratable acidity were analyzed using the one-way Analysis of Variance (ANOVA) method to detect significant differences. Samples were analyzed in triplicate. All data were expressed as mean ± standard deviation of all replicates. The means of the results were compared using Duncan's test, with a 95% confidence interval.

3 Results and discussion

3.1 Titratable acidity and pH

It is known that during the fermentation of yogurt at 42 °C, the microorganisms produce acid and lower the pH, which continues throughout cold storage (Yue et al., 2022). The results of pH and titratable acidity (TA) are demonstrated in Figure 2.

Figure 2
Changes in pH (A) values and titratable acidity (B) of yogurt during storage at 4 ± 2 °C for 28 days. Results are representing mean ± standard deviation (n: 3), with statistical differences p < 0.05. A-D: The means with different superscripts among the sampling days are significantly different, xyz: The means with different superscripts among the groups. Control (C) sample without oleaster flour, 1%OF, 2%OF, 3%OF: 1%, 2%, 3% (w/v) oleaster flour added in milk, respectively.

The pH and acidity values ​​of the yogurt samples on the first day were different than expected. This can be attributed to the starter culture used or the long time the samples come to 4 ± 2 °C storage temperature. By not cooling the samples quickly as well as performing a rapid increase in the number of lactobacilli can lower the pH and increase the acidity (Yue et al., 2022). Microbiological observations in Table 1. agree with this argument.

Table 1
The number of Streptococcus thermophilus, Lactobacillus acidophilus, L. delbrueckii subsp. bulgaricus, and Bifidobacterium animalis subsp. lactis in yogurt samples during cold storage.

Bacteria	Yogurt samples	Storage days
		1	7	14	21	28
S. thermophilus (log cfu/g)	Control	8.69 ± 0.25ax	8.64 ± 0.34ax	8.63 ± 0.34ax	8.59 ± 0.29ax	8.49 ± 0.49ax
	1% OF	8.70 ± 0.29ax	8.67 ± 0.27ax	8.65 ± 0.25ax	8.57 ± 0.18ax	8.52 ± 0.22ax
	2% OF	8.72 ± 0.23ax	8.67 ± 0.18ax	8.62 ± 0.16ax	8.62 ± 0.30ax	8.54 ± 0.25ax
	3% OF	8.68 ± 0.32ax	8.62 ± 0.27ax	8.61 ± 0.22ax	8.59 ± 0.25ax	8.52 ± 0.29ax
L. acidophilus, and L. delbrueckii subsp. bulgaricus (log cfu/g)	Control	8.83 ± 0.26ax	8.74 ± 0.28ax	8.67 ± 0.23ax	8.15 ± 0.23bx	7.81 ± 0.22bx
	1% OF	8.80 ± 0.19ax	8.72 ± 0.16ax	8.68 ± 0.19ax	8.17 ± 0.26bx	7.85 ± 0.17bx
	2% OF	8.77 ± 0.26ax	8.74 ± 0.25ax	8.67 ± 0.25ax	8.20 ± 0.28bx	7.91 ± 0.15bx
	3% OF	8.69 ± 0.23ax	8.66 ± 0.21ax	8.64 ± 0.19ax	8.28 ± 0.25ax	8.31 ± 0.26ay
B. animalis subsp. lactis (log cfu/g)	Control	6.93 ± 0.20ax	6.64 ± 0.49ax	6.60 ± 0.14ax	5.72 ± 0.20by	5.27 ± 0.27bx
	1% OF	6.79 ± 0.24ax	6.73 ± 0.24ax	6.60 ± 0.31ax	6.03 ± 0.32bxy	5.33 ± 0.25cx
	2% OF	6.73 ± 0.24ax	6.61 ± 0.31ax	6.56 ± 0.34ax	5.97 ± 0.28bxy	5.38 ± 0.40cx
	3% OF	6.67 ± 0.16ax	6.61 ± 0.21ax	6.60 ± 0.29ax	6.49 ± 0.31ax	6.26 ± 0.11ay

• OF: Oleaster Flour, Results are expressed as the mean ± standard deviation (n = 3). ^a-c: The mean values with different letters in the same line are significantly different (p< 0.05); ^xy: The mean values with different letters in the same column are significantly different (p< 0.05).

During cold storage, pH decreased, and titratable acidity increased. Except for the control group, there was no difference between the experimental groups in terms of titratable acidity after the 7^th day of storage (p > 0.05), which is consistent with our results (Casarotti & Penna, 2015; Öztürk et al., 2018). It was observed that the group with 3% OF had a higher pH than the control group on the first day of storage. This high pH value persisted until the end of storage except the 21^st day. The decrease in pH was more pronounced in the control group than in the samples supplemented with OF throughout the storage time (p < 0.05). This situation can be attributed to the presence of some buffering compounds in oleaster fruit peel (Casarotti & Penna, 2015; Öztürk et al., 2018). According to Öztürk et al. (2018), peeled OF showed lower pH and higher acidity than unpeeled OF. Different parts of the fruit contain different proportions of organic acid and soluble sugar, which directly impact pH and titratable acidity (Sarvarian et al., 2022). It may be possible that the same phenomenon could be seen in this research.

3.2 Survival of S. thermophilus, L. acidophilus, L. delbrueckii subsp. bulgaricus and B. animalis subsp. lactis during cold storage

Variations in the numbers of fermentation bacteria in bio-yogurt (S. thermophilus, L. acidophilus, L. delbrueckii subsp. bulgaricus, and B. animalis subsp. lactis) during storage are shown in Table 1. During storage, some losses in viability were observed in the S. thermophilus population; these small changes had no microbiological significance, as the changes were less than 0.5 log cfu/g (p > 0.05). This slight decrease observed over the storage period was also observed in other studies (Bedani et al., 2013; Casarotti & Penna, 2015; Zare et al., 2011; Zahid et al., 2022). As known, most lactobacilli are microaerophilic, while bifidobacteria are anaerobic and very sensitive to dissolved oxygen levels. Protecting the number of S. thermophilus in the last days of storage provides a small advantage over other anaerobic bacteria, as it is able to scavenge reactive oxygen species and prevent lipid peroxidation by reducing oxygen levels (Zahid et al., 2022; Michael et al., 2015).

The initial number of L. acidophilus and L. delbrueckii subsp. bulgaricus ranged from 8.69 to 8.83 log cfu/g and was similar to the number of streptococci in fresh yogurt. At the end of storage, the viability of lactobacilli was reduced and ranged from 7.85 to 8.31 log cfu/g. At the same time, the viability of lactobacilli was significantly higher in the samples enriched with 3% OF compared with the control group (p < 0.05). It is noteworthy to know which compounds in the OF have this protective benefit for lactobacilli. Predictably, lactobacilli's survival might have been caused by the high content of dietary fiber, fructose, and glucose in oleaster (Akbolat et al., 2008; Öztürk et al., 2018; Sahan et al., 2015). According to the current study's results, it may be noted that lactobacilli use compounds found in oleaster as an additional growth source. The lactobacilli data are consistent with other studies on bio yogurt fortified with various fruits such as lentils, apples, bananas, or grapes (Casarotti & Penna, 2015; Kycia et al., 2020; Zare et al., 2011; Zahid et al., 2022).

On the first day, relatively few B. animalis subsp. lactis were present in all samples. This may be a result of low pH levels, a short fermentation time, a high amount of milk fat, and dissolved oxygen (Kurtuldu & Ozcan, 2018; Meybodi et al., 2020; Ozcan et al., 2017; Thomas, 2016). When the results for B. animalis subsp. lactis were analyzed, it was found that the duration of storage and the addition of OF significantly affected the viability of the bacteria. The initial number detected varied from 6.67 to 6.93 log cfu/g. Interestingly, this initial number was higher in the non-supplemented group associated with the lactobacilli. This phenomenon can be attributed to the antimicrobial compounds such as organic acids and phenolic acids found in the oleaster (Meybodi et al., 2020). After 28 days of cold storage, the viability of B. animalis subsp. lactis varied between 5.27 and 6.26 log cfu/g. In the control group, there was a loss of about 1.5 log cfu/g of B. animalis subsp. lactis during storage. Several studies have found similar results (Bedani et al., 2013; Kycia et al., 2020; Michael et al., 2015).

The results showed that yogurt fortified with OF increased the survival of B. animalis subsp. lactis during 28 days of cold storage. In general, lactobacilli are able to grow and survive in fermented products with a pH ranging from 3.7 to 4.3 (Nami et al., 2023). On the other hand, bifidobacteria are known to have too low tolerance to acidity (Kycia et al., 2020; Meybodi et al., 2020). Öztürk et al. (2018) found that total soluble solids content increased with increasing concentration of oleaster in yogurt formulation. As the soluble solids content increases, the oxygen damage of bifidobacteria decreases. This could explain the slightly higher B. animalis subsp. lactis count in the group with 3% OF.

3.3 Assessment of In Vitro Gastric Tolerance for B. animalis subsp. lactis, L. acidophilus and L. delbrueckii subsp. bulgaricus

Pepsin's antibacterial properties and the low pH of the stomach are known to efficiently prevent the passage of microorganisms into the intestinal system. One of the main standards used to choose probiotic strains to ensure their ability to survive is an assessment of gastric tolerance. Generally, probiotic strains have been evaluated mostly using in vitro methods, such as carefully monitored incubations in simulated gastric juice (SGJ) (Gaucher et al., 2019; Sanz, 2007). The effect of different pH-adjusted in SGJ on the survival of L. acidophilus, L. delbrueckii subsp. bulgaricus and Bifidobacterium animalis subsp. lactis is presented in Figures 3 and 4, respectively.

Figure 3
The survival of L. acidophilus and L. delbrueckii subsp. bulgaricus of yogurt samples during 180 min in simulated gastric fluid at pH 2.0 and 4.0 on the first day of cold storage.

Figure 4
The survival of Bifidobacterium animalis subsp. lactis of yogurt samples during 180 min in simulated gastric fluid at pH 2.0 and 4.0 on the first day of cold storage.

Probiotic strains showed a progressive decrease at pH 2.0 in viability for 180 minutes. The survival of L. acidophilus, L. delbrueckii subsp. bulgaricus viability was not different between groups neither at pH 2.0 nor 4.0 (p > 0.05). At pH 4.0, the numbers of bacteria in these groups remained the same, but at pH 2.0, there were approximately 4 log cfu/g losses in all groups. The decrease in lactobacillus viability continued over time in all groups. The groups with doses of 2% and 3% OF after 60 minutes were statistically different from the control and 1% OF groups (p < 0.05). After 180 minutes, there was no statistically significant change between the groups (p > 0.05). Generally speaking, bifidobacteria strains proved to be significantly less acid resistant than lactobacilli (Balthazar et al., 2022). In the current research, our results did not find any difference regarding this subject. However, in exceptional cases, differences in acid stress tolerance can result from the use of different bacterial strains and exposure to different extrinsic or intrinsic factors.

Another study, in disagreement with the present study, showed that in plain and fruity yogurt in synthetic gastric juice adjusted to pH 2.0, L. acidophilus counts decreased by about 1.0 and 4.0 log cfu/g after 60 min (Ranadheera et al., 2012). Studies point out that the viability of probiotics in fruit yogurts is limited due to increased acidity (Casarotti & Penna, 2015; Ranadheera et al., 2012; Zare et al., 2011). However, in this study, there was no difference between the yogurts with OF added and the control group (p > 0.05). The presence of oleaster peel may have regulated acidity and then promoted lactobacilli viability.

When the SGF had a pH of 2.0, B. animalis subsp. lactis viability showed a dramatic decrease at pH 2.0 in the control group. After 60 minutes, it was below the detection limit. The group with the addition of 1% OF was also below the detection limit in the analysis after 120 minutes (p < 0.05). As the oleaster addition increased, B. animalis subsp. lactis viability increased, and all minute differences were statistically significant in treated groups (p < 0.05). The researchers likewise investigated the survival of B. animalis subsp. lactis and L. acidophilus in plain and fruity yogurt made from goat's milk in synthetic gastric juice adjusted to pH 2.0 and pH 4.0 (Ranadheera et al., 2012). According to researchers, in plain and fruit yogurt, B. animalis subsp. lactis has been found below the detection limit at pH 2.0 after 30 and 60 min, respectively. Current research results for B. animalis subsp. lactis is consistent with Ranadheera et al. (2012).

Matsumoto et al. (2004) found that strains from B. longum, B. adolescentis, and B. pseudocatenulatum dramatically reduced after an hour of incubation at a pH 3.0 solution. However, the B. animalis strain survived the exposure to pH 3.0-5.0 for 3 h. Moreover, another study showed the viability of L. acidophilus and B. animalis subsp. lactis that remained mostly unaffected by simulated gastric transit at pH 3.0 and pH 4.0 in plain and fruit yogurt (Ranadheera et al., 2012). Similarly, in this study, when the SGF mixture was adjusted to PH 4.0, B. animalis subsp. lactis survived in all groups for 180 minutes (p > 0.05).

4 Conclusion

Although plain and fruit yogurts have a similar shelf life, their physicochemical and microbiological properties are different. Especially tiny changes in acidity can have harmful consequences for probiotics. It is known that fruit acid increases acidity in fruit yogurts and negatively affects some probiotic viability. However, in this study, the presence of some substances from oleaster peel slightly buffered the progression of acidity.

The results of the present investigation showed that even though the survival of B. animalis subsp. lactis, L. acidophilus, and L. delbrueckii subsp. bulgaricus is affected by pH 2.0, these strains may survive well at pH 4.0 in stomach conditions. Also, the amount of surviving probiotic bacteria was significantly higher as the amount of oleaster added to the yogurt increased in gastric fluid conditions adjusted to pH 2.0. So, these results showed that oleaster flour can be applied to produce bio-yogurt.

• Cite as: Güngören, A., Demircioğlu, A., Akkemik, Y., & Güner, A. (2023). Impact of elaeagnus angustifolia flour added to bio-yogurt on probiotic survival and monitoring of in vitro acid tolerance in synthetic gastric fluid. Brazilian Journal of Food Technology, 26, e2023070. https://doi.org/10.1590/1981-6723.07023
• Funding: None.

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Edited by

Associate Editor: Maria Gabriela Bello Koblitz.

Publication Dates

• Publication in this collection
  13 Nov 2023
• Date of issue
  2023

History

• Received
  05 June 2023
• Accepted
  11 Sept 2023