Flavored functional drinking yogurt (Doogh) formulated with Lactobacillus plantarum LS5, cress seed gum, and coriander leaves extract

Abstract The effects of coriander extract (CE) and cress seed gum (CSG) on viability of Lactobacillus plantarum LS5 and physicochemical properties of drinking yogurt (Doogh) were evaluated. The CE contained 18 mg GAE/g and was shown by the DPPH radical assay to have remarkable antioxidant activity. The CE was added at concentrations of 0%, 0.05%, 0.1%, and 0.25%, and the levels of added CSG were 0%, 0.1%, 0.25%, and 0.5%. Doogh samples were analyzed after 1, 2, and 3 weeks of storage at 4°C. By increasing the amounts of CSG, the viscosity of the Doogh samples was increased and phase separation was reduced significantly (p < .05). The results also showed that by increasing the levels of CSG to 0.5%, L. plantarum count increased significantly (p < .05). Doogh sample containing 0.05% CE and 0.5% CSG gained the highest probiotic count, overall acceptability score, and lowest lipid oxidation and phase separation in comparison with the other samples.

seeds when they soak in water and a transparent gel forms around the whole seed. Karazhiyan, Razavi, and Phillips (2011) reported that CSG, as a carbohydrate, contains sugars like l-arabinose, d-xylose, d-galactose, l-rhamnose, d-glucose, d-galacturonic acid, and 4-O-methyl-d-glucuronic acid.
Therefore, in this way, they can improve host health. Probiotics can be defined as living microorganisms that provide health advantages.
As it has been reported, by beneficial effects of probiotics include improvement of the immune system, gastrointestinal complications, and lactose intolerance symptoms, as well as reduction of cholesterol and antitumor effects (El-Abd et al., 2018). Lactobacillus and Bifidobacterium are the main genera of probiotic bacteria. To achieve better effects on host health, combining probiotics and natural prebiotics with Doogh may be helpful. As previously stated, plant extracts contain fibers, vitamins, and minerals that make it a suitable material to promote bacterial growth (El-Abd et al., 2018).
Bioactive constituents, with antioxidant activity, are usually found in high concentrations in medical plants. Coriander (Coriandrum sativum L.) is a good source of natural antioxidants. It is a culinary and medicinal plant from the Umbelliferae family that is approved for food use by the FDA and can be used as an additive in food products and beverage (Mendel & Mandal, 2015). It is commonly utilized for its fresh leaves and the dry powder of its fruits which have organoleptic and flavoring properties (Yildiz, 2016). As has been reported by Burdock and Carabin (2009), this herb had been called the "spice of happiness" by the Egyptians because they considered it an aphrodisiac. As it has been shown by Shahwar et al. (2012), the methanol extract of coriander leaves has remarkable total phenolic contents (30.25 ± 3.42 mg/g) and the fresh leaves con-

| Preparation of cultures
Lactobacillus plantarum LS5 was activated in MRS broth medium and incubated at 37°C/24 hr under anaerobic conditions using an anaerobic atmosphere generation system (GasPak system, anaerobic system, Oxoid).

| Extraction of gum from of cress seed
A sequential process was used to extract gum from cress seeds using the method described by Jouki et al. (2013). Briefly, aqueous CSG was extracted from whole seeds using distilled water (time 15 min, temperature 45°C, and water to seed ratio 30:1). The swelled seeds were stirred with a rod paddle blender at 1,100 to scrape the mucilage layer off the seed surface. The solutions were then filtered with cheese cloth, and the insoluble residue was filtered. The collected gum was dried in an oven (45°C overnight).

| Preparation of coriander extract
Fresh coriander leaves were spread onto drying trays in freezedryer (Biotron) at −55°C for 24 hr. Coriander extract was prepared by mixing 100 g of dried leaves with 300 ml of methanol then stirred at 25°C for 48 hr, and the extracts were filtered by Whatman No. 1 filter paper. To evaporate and remove the solvent from the extract, a rotary under vacuum was employed. The distillation was stopped when the volume of extract remaining was ~1 ml. Solvent was further removed under a purified N 2 stream.

Highlights
• The coriander extract showed remarkable antioxidant activity and had 18 mg GAE/g.
• Probiotic Dooghs containing 0.5% of CSG were stable during storage period.
• Combination of gum and extract at the suitable level prevented phase separation.
• Results indicated the potential of coriander extract for supporting probiotic growth.
The samples were kept under N 2 in sealed vials in a freezer until use (Shahwar et al., 2012).

| Determination of total phenolic content
The total phenolic contents of coriander extract determined by Folin-Ciocalteu method were reported to be gallic acid equivalents (GAE). Extract solution (125 μl) was taken in a volumetric flask, and 500 ml distilled water and 125 μl Folin-Ciocalteu reagent were added and shaken vigorously. Absorbance of the samples in triplicate at 760 nm was measured by using a UV-vis spectrophotometer (Sun et al., 2006). Measurements were carried out in triplicate. Gallic acid was used at various concentrations (0-1,000 mg, 0.1 ml/L), and standard curve was obtained.

| DPPH radical scavenging activity of coriander extract
The DPPH method is used for the determination of free radical scavenging activity, usually expressed as IC 50 (Shahwar et al., 2012). Briefly, 1 ml of DPPH ethanol solution (freshly prepared at a concentration of 0.1 mM) was added to 3 ml of extract solution at various levels (10-100 μg/ml). The resulting mixture was stored in the dark place for 30 min at 20°C, and afterward, absorbance of samples was measured at 517 nm against ethanol. The scavenging activity of DPPH radicals was calculated according to the following equation: The coriander extract concentration providing IC 50 was measured using plotting concentrations against percentage inhibition.
The amount of antioxidant needed to reduce the initial concentration of DPPH by 50% is defined as IC 50 , and lower amounts of IC 50 indicate higher antioxidant activity.

| Preparation of probiotic Doogh
Fresh milk with 2.9% fat, 3.1% protein, 4.7% lactose, and pH 6.7 was pasteurized at 90°C for 15 min. After cooling down of the milk up to the fermentation temperature (42 ± 1°C), it was inoculated with YF-3331 according to the manufacturer's instructions, incubated until its pH reached 4.2, and then cooled to 4°C to stop the fermentation. The yogurt was diluted by drinking water (50% v/v and NaCl 0.7% w/v) to produce Doogh. Then, CSG (0, 0.1, 0.25, and 0.5% w/v) and CE (0, 0.05, 0.1, and 0.25% w/v) were added to the mixture and stirred ( Figure 1). Then, they were filled into 250-ml PET bottles, and to achieve full hydration, the mixture was kept at room temperature overnight. All samples were pasteurized (90°C for 30 min) and cooled down to ambient temperature (Hashemi, Shahidi, Mortazavi, Milani, & Eshaghi, 2015).
Afterward, active probiotic culture (10 9 cfu/ml) was added to the Doogh samples and they were incubated at 37 ± 1°C for 6 hr. Then, Doogh samples were stored for 21 days at 4°C.

| Microbial analysis
Viable counts of L. plantarum in Doogh samples were assessed by plate count method using MRS agar (Merck). The plates were incubated at 37°C for 72 hr in jars under anaerobic conditions (Hashemi et al., 2015). Microbiological colonies from the plates containing 30-300 colony-forming units (cfu) were counted and transformed to log10 cfu/ml.

| pH and titratable acidity
The pH changes of the Doogh samples were regularly measured at 25 ± 1°C using a HANNA pH meter. The titratable acidity (TA) was determined according to the method of Ghasempour, Alizadeh, and Bari (2012). Ten ml of Doogh samples and 10 ml of deionized water were mixed, and 0.5 ml of phenolphthalein was added into the mixture. This mixture was titrated with 0.1 N NaOH. The acidity of the Doogh samples was calculated as percent (%) lactic acid.

| Phase separation
Phase separation of Doogh samples was measured using gravity separation. In order to determine stability of the Doogh samples, they were transferred to 10 ml sterilized and graduated test tubes with cap kept at 4°C. During 21 days of storage, the height of supernatant was measured and its value (divided by the total height of sample in bottle and multiplied by 100) has expressed as the serum separation (Foroughinaia et al., 2007).

| Viscosity measurement
The dynamic viscosity of each Doogh samples was measured using a rotational viscometer (DV-II, Brookfield Engineering Laboratories, Inc.). All measurements were done at room temperature (20°C) using a number 2 (LV2) spindle set at 30 rpm. After primary experiments, the appreciate torque value found between 10% and 100% of the measuring range to obtain reliable results.

| Estimation of peroxide value in Doogh
The lipids were extracted from the Doogh samples according to the Bligh and Dyer's (1959) using chloroform/methanol (1:1 v/v). The peroxide value of the extracts was determined by the (1) Scavenging activity (%) = Abs DPPH − Abs sample Abs DPPH × 100 iodometric titration method described in the IUPAC standard method 2.501 (Paquot, 2013), and results were expressed in meq oxygen/kg lipid.

| Sensory evaluation
Sensory evaluation was carried out by 9 trained panelists (including 5 women and 4 men, food science specialists, age 25-35) were asked to determine the sample scores with a 5-point hedonic scale test.
The scores (1 = dislike very much, 2 = dislike a little, 3 = neither like nor dislike, 4 = like a little, and 5 = like very much) for taste, color, odor, and overall acceptability were given by the expert panelists (Meilgaard, Civille, & Carr, 1999). Doogh samples were taken for the analysis after 1, 7, 14, and 21 days of storage.

| Statistical analysis
The experimental data were statistically analyzed using SPSS statistical software. Duncan's multiple range tests were used to compare the differences among means. Also, the correlation coefficient analysis was done between the different parameters.

| Total phenolic content and antioxidant activity
The phenolic content of the coriander extract was 18.26 mg GAE/g, which agrees with the values found by Sriti, Aids Wannes, Talou, Vilarem, and Marzouk (2011) (1999) showed that antioxidant activity is directly related to total phenolic contents, so the sample having the higher total phenolic content will show the higher antioxidant activity. In addition, a significant correlation between antioxidant activity and total phenolic in some selected herbs was found by Wojdyło, Oszmian, and Czemerys (2007).
In the other words, they reported that phenolic compounds are the dominant antioxidant components.

| pH and acidity measurements
Statistical analysis showed that the effects of CSG gum and CE on the pH ( Figure 2a) and acidity (Figure 2b)

F I G U R E 1 Functional Doogh production process flow chart
The results of this part were consistent with the obtained results of probiotic viability ( Figure 3). As shown in Figure 3, the addition of CE at 0.05% increased probiotic viability, and increase in probiotic counts in the presence of CE might be due to the presence of prebiotic compounds including phenolic compounds. As El-Abd et al. (2018) stated plant extracts contain fibers, vitamins, and minerals that make it a suitable material to promote bacterial growth. Therefore, in this study, reduction in pH and increase in acidity were higher in the samples containing 0.05% CE and high level of CSG because of the bacterial growth and production of lactic acid. Moreover, the acidity slightly decreased at 0.1% and 0.25% of CE compared to 0.25%. This could be related to antimicrobial activity of CE at higher level due to the presence of some phenolic and antibacterial components in CE.

| Viscosity of Doogh
Storage time affected viscosity of Doogh samples, negatively (p ˂ .05). It can be concluded that the addition of CE causes a decrease in viscosity and consistency of the Doogh sample (Figure 4a). As it is shown in Figure 4a, the viscosity of probiotic Doogh was increased significantly (p ˂ .05) as the concentration of CSG increased from 0% to 0.5%. As it has been reported by Koksoy and Kilic (2004) and Paraskevopoulou et al. (2003), the viscosity of dairy drink is changed in the presence of gums. Ziaolhagh and Jalali (2017) reported that xanthan gum increased the viscosity of bio-Doogh, and Paraskevopoulou et al. (2003) showed that it can increase the viscosity of a daily drink made from kefir-milk mixture. The viscosity of the samples decreased significantly (p < .05) during storage time.
This decrease might be due to microbial enzyme action on the casein micelle matrix during the storage period (Kosikowski, 1982).  (Table 1).

| Phase separation
The samples containing coriander extract showed lower rate of peroxide formation, which have higher pH. This may be attributed to the higher rate of lipid auto-oxidation at an acidic pH and thus to the more pro-oxidant environment of pH 3.5 (day 21) in comparison with pH 3.7 (day 1). This result is in agreement with that of Sasanian et al. (2018) on drinking yoghurt. As has been reported by Mei, McClements, and Decker (1999), when the pH decreases to the protein isoelectric point, it may influence positively charged proteins, which can repel positively charged ions (Cu 2+ , Fe 3+ ) that subsequently accelerate lipid oxidation.
The PV of samples treated with CE was significantly lower than that of untreated by CE, indicating that the coriander extract was effective in reducing lipid oxidation in Doogh (Table 1). The results also showed that the highest level of coriander extract (0.25%) had the highest effect in slowing down the primary peroxidation process, compared with other samples (p < .05). As has been previously reported by Shahwar et al. (2012) and Yildiz (2016), coriander extract showed good antioxidant activity. Perumalla and Hettiarachchy (2011) showed that the antioxidant activity of the plant extracts could be related to mechanisms such as inhibition of radical chain initiation, decomposition of peroxides, and interaction with the free radicals as well as binding of metal ion catalysts connection. On day 21 of storage, PV of samples enriched with 0.25% coriander extract was 17% lower than control sample (Table 1).
Meanwhile, PVs of all Doogh samples were lower than 1 meq O 2 /kg of oil until day 21 of storage. In addition, in present study the samples were stored in a dark refrigerator and were protected from light. These conditions most likely contributed to the inhibition of lipid oxidation even at the lowest concentration coriander extract (0.05%).
F I G U R E 4 Effect of coriander extract (CE) and cress seed gum (CSG) concentrations on viscosity (a) and phase separation (b) of probiotic Doogh during 21 days of storage

| Sensory characteristics
As it is shown in Figure 5, the effect of concentrations of CSG and CE on the sensory attributes of the Doogh samples at the first day of storage was significant (p ˂ .05). The sensory evaluation of samples showed that the concentration of CSG and CE had significant (p < .05) effects on the taste, color, odor, and overall acceptability of probiotic Doogh samples (Figure 5a- F I G U R E 5 Effect of coriander extract (CE) and cress seed gum (CSG) concentrations on sensory scores of Doogh samples during 21 days of storage. Taste (a), odor (b), color (c), and overall acceptability (d) the odor and color between control and the sample enriched with 0.05% CE + 0.5%CSG.
The control had the lowest taste and odor scores at the end of storage. As has been reported by Dave and Shah (1997), producing the fermented dairy products only by probiotic bacteria leads to the unfavorable tasted products. So, the gums used in this study could cover the unfavorable sensory attributes in Doogh samples. The higher scores were related to the Doogh sample containing 0.05% CE at the end of storage. Azarikia and Abbasi (2010) showed that the presence of local herbs extracts in Doogh stabilized with tragacanthin could enhance its taste score.
As illustrated in the Figure 5a, the panelists evaluated that Doogh stabilized by 0.5% CSG and 0.05% CE can present the best taste among the other samples. This sample also had a high color and odor score ( Figure 5). The panelists evaluated that the prepared samples with high CSG concentration (have highest viscosity) are ideal for the consumers. Penna, Sivieri, and Oliviera (2001) stated that the sensory acceptability of lactic beverages can be increased by increasing the viscosity.

| CON CLUS ION
The addition of CSG and CE to Doogh significantly affected physicochemical properties including pH, titratable acidity (LA %), viscosity, phase separation, lipid oxidation, and sensorial properties of Doogh.
The results of this study showed that probiotic Doogh samples containing 0.5% CSG and 0.05% CE maintained the quality of Doogh samples by preventing color changes and lipid oxidation and phase separation as well as other quality parameters. Therefore, coriander extract as a natural antioxidant can be added to dairy products to effectively inhibit oxidation during storage.

ACK N OWLED G M ENTS
The authors would like to extend their appreciation for the financial support provided by the Islamic Azad University (Iran, Tehran).

CO N FLI C T O F I NTE R E S T
We declare no potential conflict of interest related to this manuscript.

E TH I C A L A PPROVA L
We declare no ethical issue related with this article.