As an innovative bio-dairy product, yoghurt was enriched with Spirulina-encapsulated aqueous/hydroalcoholic extracts of pomegranate peel (PP). Some metabolomics, antioxidative, textural and colour properties of bio-yoghurt samples were investigated. The samples with Spirulina (YM) and PP (YPA) had the highest lactic, citric and uric acid. The aroma profile of the samples was affected encapsulation process and storage time. The values on day 1 and day 21 were 17.84–17.04 mg/kg for acetaldehyde, 0.98–0.90 mg/kg for diacetyl and 54.42–46.65 mg/kg for acetoin. The sample with encapsulated PP aqueous extract (YEPA) had the highest TPC (2.97 mg GAE/g), and the sample with PP aqueous extract (YPA) had the highest antioxidant capacity (0.36 mg TE/g). The present study describes that bio-yoghurt enriched with Spirulina-encapsulated PP could be considered a good alternative for consumers demanding functional dairy products and a holistic approach to a circular bioeconomy.

INTRODUCTION

Today, consumers are increasingly aware of the health dimension of food consumption. While consumers are looking for new tastes, smell and aromas in foods, they also draw attention to the content and bioactive properties of foodstuffs (Najgebauer-Lejko et al. 2021). For this purpose, new functional foods are being tested to be developed by combining traditional foods with additives of natural origin. Recently, studies have been conducted in which natural polyphenolic compounds extracted from plants are added to foods as natural additives to prevent or delay food spoilage and for their health benefits (Cutrim and Cortez 2018). By creating a functional new food of plant origin, human needs will be met in terms of essential nutrients and energy, but also foods will be enriched with these active ingredients (Ivanov and Rashevskaya 2011). In studies on the production of functional products with the addition of plant extracts, which are popular in the dairy industry, it has been observed that the antimicrobial, antioxidant, antihypertensive, etc. effects are enhanced, resulting in a protective effect in foods (Granato et al. 2018).

Pomegranate (Punica granatum L.) contains valuable polyphenolic compounds such as ellagitannins, gallagyl-type tannins (punicalagin), hydrolyzable tannins (galloyl glucose and other compounds), derivatives of ellagic acid derivatives (ellagic acid glucoside and ellagic acid) (Robert et al. 2010). These compounds have free radical scavenging activities, and their therapeutic effects have been proven by studies (Panichayupakaranant et al. 2010). For example, punicalagin, which is the most abundant polyphenol in its structure, has been proven to have anticancer and anti-inflammatory effects (Rodríguez et al. 2009). Pomegranate peel (PP) is a by-product of pomegranate fruit processing and is a natural source of antioxidants due to its valuable polyphenolic compounds. Peels are known to contain large amounts of phenolic compounds, flavonoids and antioxidants compared to the whole fruit (Vieira et al. 2009). However, protein-rich Spirulina microalgae is a biotechnologically non-toxic product that is consumed as food throughout the world (Cepoi et al. 2017). Due to the components such as phenol, flavonoid and tannin in their structure, they show antioxidant activity and a free radical-repellent effect. Since the protein content of Spirulina microalgae is similar to that of meat (460–630 g/kg, based on dry matter), it has been considered a rich source of protein (Lupatini et al. 2017). Microalgae and their rheological properties also play a very important role in the foods to which they are added (Suzery et al. 2018). Although there are studies on microencapsulation of valuable components of Spirulina in the literature, studies that use it as a coating material are rare.

Here, a new dairy product with functional properties has been produced using fruit waste (PP) components that have a high potential health effect, but little practical application. For this purpose, Spirulina and PP extracts, two natural products combined with the microencapsulation technique, were used in our previous study (Yağmur et al. 2021). Additionally, the effect of encapsulation was also investigated using unencapsulated PP extracts. For this study, yoghurt was preferred as the dairy product to which encapsulated and unencapsulated extracts would be added. Fermented foods are a very suitable environment for the transport and controlled release of bioactive compounds throughout digestion. Since yoghurt is a widely consumed fermented dairy product, diversifying it was thought that diversifying it would provide significant improvements in health. To minimise the interactions that can occur between milk proteins and phenolic compounds during yoghurt production or storage and not affect antioxidant activity, adding phenolic compounds to the medium as microcapsules are considered an advantage here (Rashidinejad et al. 2013). As a result, their bioavailability and general acceptability will not be affected (Ozdal et al. 2013; Haratifar and Corredig 2014; El-Messery et al. 2019). In addition, the negative effects of added phenolic compounds, if any, will be prevented (Altin et al. 2018).

During the fermentation process, the bioavailability and bioaccessibility of these compounds increase as a result of the release of phenolic compounds attached to some lactic acid bacteria (Young et al. 2015). It is also extremely important that the microorganisms of the starter culture survive until the end of storage, and be abundant and active (Semeniuc et al. 2016). Pomegranate, which has a high active phytochemical content in all parts (153 different identified species), along with its unique antimicrobial and anti-inflammatory properties, and thus has a very high antioxidant effect, has also appeared in studies in different fields (Karimi et al. 2017). For example, Pena et al. (2020), by adding pomegranate juice to fermented milk with probiotics, investigated the viability of the probiotics in the environment and the bioaccessibility of phenolic compounds after simulated digestion. Here, it has been determined that the host microorganism uses phenolic compounds selectively and their benefit to the host is determined (Gibson et al. 2017). Therefore, phenolic compounds have recently been classified as prebiotics. It is known that ellagitannins, ellagic acid and its derivatives, which are abundant in PP, have antioxidant, estrogenic and/or antiestrogenic, and/or anti-inflammatory, and anti-inflammatory activities, as well as positive effects on the development and viability of starter microorganisms (Landete 2011). In fact, in our other study, in which microbiological analysis was performed with the same yoghurt samples, both characteristic microorganisms belonging to yoghurt were active and remained alive until the end of storage (Yağmur et al. 2023). At this point, the nutritional content of Spirulina and the effect of phenolics on PP extracts are considered an advantage.

These natural and colourful yoghurts, which are enriched with bioactive components, have high nutritional value, are functional, have different flavours and will also attract attention with their new sensory properties. In our previous study, it is known that these yoghurts, scored by panellists who were subjected to sensory tests for this purpose, were generally liked (Yağmur et al. 2023). As a result, a new product was developed that had the taste that consumers wanted and could have therapeutic properties. Despite the numerous studies on the addition of Spirulina microalgae to dairy products, in the relevant literature, yoghurt enriched with PP extract was not adequately investigated. This type of bio-yoghurt produced will offer an innovative approach to dairy products with its multiple functional effects. In light of the above-mentioned, bio-yoghurt samples were formulated using Spirulina microalgae, encapsulated and unencapsulated PP extracts. Some metabolomics such as organic acid and aroma compounds, antioxidative, textural and colour properties were investigated during 21-day storage.

MATERIALS AND METHODS

Materials

Spirulina (Blue-Green Algae, E611) was purchased as a powder extract with a pure plant value of 1:20 from Nu-da Gıda Vegetable Oil and Yem Industry Trade Joint Stock Company (Istanbul, Turkiye). Pomegranate fruits required to obtain PP extract were obtained from the local market. Yoghurt culture (Streptococcus thermophilus and Lactobacillus delbrueckii subsp. bulgaricus; FD-DVS YC-350) was purchased from Chr. Hansen's (Hoersholm, Denmark). Raw cow milk was supplied from a commercial dairy plant (Bursa, Turkiye). Skimmed milk powder for the production of yoghurt was obtained from a dairy factory (Pinar Dairy Co., Izmir, Turkiye). Encapsulation of PPs with Spirulina as the coating material was performed in a previous study. The unencapsulated extract obtained in a hydroalcoholic medium was removed from its solvent under N₂ gas before adding it to milk (Yağmur and Şahin 2020).

Production of bio-yoghurt enriched with Spirulina-encapsulated PP extract

The milk was tempered to 45°C, fortified with 3% (w/v) skimmed milk powder and heated to 90°C for 10 min. They were placed in six different sterile containers and when the temperature reached 50°C, Spirulina microalgae, encapsulated and unencapsulated extracts were added to the containers, except for the control group. Six groups of bio-yoghurt were produced; YC (control yoghurt); YM (1% Spirulina microalgae); YPA (1% PP aqueous extract); YEPA (1% encapsulated PP aqueous extract); YPH (1% PP hydroalcoholic extract) and YEPH (1% encapsulated PP hydroalcoholic extract). Then, they were cooled to the recommended incubation temperature (42–45°C). Six different milks inoculated with 3% starter culture were mixed with sterile mixers and placed in the incubator. The samples, which reached pH 4.7, were removed from the incubator and kept at room temperature (20°C) for 30 min, transferred to the refrigerator (+4°C) and stored for 21 days. The physical appearance of the bio-yoghurt samples obtained is shown in Figure 1. Total phenolic content, antioxidant capacity, organic acid, aroma compounds, textural and colour analyses were carried out on the 1st, 7th, 14th and 21st days of storage.

Details are in the caption following the image — **Figure 1**
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YC (control yoghurt); YM (1% *Spirulina* microalgae); YPA (1% pomegranate peel aqueous extract); YEPA (1% encapsulated pomegranate peel aqueous extract); YPH (1% pomegranate peel hydroalcoholic extract) and YEPH (1% encapsulated pomegranate peel hydroalcoholic extract).

Determination of total phenolic substance and antioxidant capacity

All spectroscopic measurements were made with the Cary 50 Conc, Varian model UV–vis spectrophotometer. For this, 1 g of six different yoghurt samples was taken and 5 mL of 80% (v/v) ethyl alcohol-water mixture was added and vortexed for 1 minute. The tubes were then centrifuged at 3000 rpm for 10 minutes and 100 μL was taken from the centrifuge. Total phenolic substance (with the Folin–Ciocalteu method) and antioxidant capacities (with the ABTS method) were determined according to Yağmur and Şahin (2020) procedure. Briefly, distilled water, Lowry C solution and Folin–Ciocalteu reagent were added to the extracts, respectively. The mixture was left in the dark for 30 min and the absorbances were measured at 750 nm. For the ABTS method, ethanol and ABTS solution were added to each extract, and absorbance values at 734 nm were read at the end of the sixth minute. This process was repeated for the blank sample. The total phenolic content and antioxidant capacity of the samples were calculated as gallic acid equivalent (GAE)/g sample and mg Trolox Equivalent (TE)/g sample using the calculated calibration equations.

Determination of organic acid and aroma metabolomics

The extraction of organic acids, including lactic, citric and uric acids, was performed according to AOAC (2005) and Mortera et al. (2018), with some modifications. First, 2 g of the sample was diluted to 40 mL of distilled water. It was shaken at 50 rpm for 1 h in the shaker and centrifuged for 10 min at 4500 rpm and 22°C. The supernatant was filtered using a 0.45 μm hydrophilic PVDF Millipore Millex-HV filter in vials (Sigma-Aldrich, Taufkirchen, Germany). The filtered sample was injected into a Shimadzu Prominence-I LC-2030C 3D Plus liquid chromatography system (Shimadzu Prominence, Japan). Separation was carried out on an AQ-C18 (4.0 × 150 mm, 3 μm) column. It was prepared as a solution system with phosphate buffer (KH₂PO₄/o-H₃PO₄, pH = 2.40) prepared with 0.002 M KH₂PO₄ in isocritical flow for 20 min, and used as a mobile phase with 10 μL injection volume of 10 L and flow rate of 0.6 mL/min. Measurements were made at different wavelengths according to the organic acids. The organic acid values were expressed as mg/kg.

Analysis of aroma compounds including acetaldehyde, diacetyl and acetoin was carried out as described by Kaminarides et al. (2007), with some modifications, using a Headspace Gas Chromatography with Flame Ionisation Detection (HS-GC-FID Agilent 5977A GC, USA) system. The device consists of a 7697A-coded Headspace Sampler and 7890B GC systems. Samples weighing 5 g each were placed in 20 mL GC-Headspace vials and their lids were immediately closed with a clamp. These vials were heated at 80°C for 60 min and pressurised with helium, and the volatile compounds were driven at 110°C on a transfer line and automatically. The GC cycle time was 38 min. The results were expressed in mg/kg.

Texture analysis

Within the scope of texture profile analysis, the index of viscosity, consistency, cohesiveness and firmness analyses were performed according to Joon et al. (2017) and Stable MicroSystems (2019), with some modifications, using the TA.XT-plus Texture Analyzer (Stable Micro Systems) device. In the measurements, the “back extrusion cell” and the “load cell” of 5 kg were used. According to the “Yoghurt Project”, the yoghurt samples were studied at 25 ± 1°C and all measurements were made at a speed of 1 mm/sec and with an immersion distance of 10 mm. During the analysis, measurements were made by immersing the special A/BE-d35, the “back extrusion rig” 35 mm disc probe attached to the system, into the yoghurt samples in 100 mL sterile containers. The numerical values of the index of viscosity, consistency, cohesiveness and firmness were measured using exponent software (version 6.1.23.0).

Colour analysis

In colour measurement, a colour determination device (Hunter-Lab) was used to determine L/a/b values. Yoghurt samples were mixed to make them homogeneous. Hunter Lab was placed in a special sample container and placed in the device; the values of six different yoghurts were read in parallel (Kadakal et al. 2004).

Statistical analysis

To evaluate the results obtained in all analyses, random plot design and variance analysis were applied accordingly to determine the difference between sample types and storage times in bio-yoghurt samples. Basic statistical values were determined in the samples and the sources of variation, which were found to be important according to the results of the analysis of variance, were compared with the Fischer comparison test at P < 0.05 level. As a result, differences caused by the sample type and storage times were revealed (MINITAB 17 Statistical Software).

RESULTS AND DISCUSSION

Total phenolic substance and antioxidant capacity of the samples

Data relating to total phenolic content and antioxidant capacity are presented in Table 1. There were some significant differences (P < 0.05) within the results throughout storage. The values of the total phenolic content of the samples varied between 1.44–5.23 mg GAE/g (Table 1). The total phenolic content was found to be higher in all yoghurt samples containing encapsulated and unencapsulated Spirulina/PP extracts compared to control yoghurt. Valuable phenolic compounds found in PP and Spirulina were considered to be effective in this case. When the change in the total phenolic content of the samples during the storage period was examined, the yoghurt with the highest average value was the YEPA sample (2.97 mg GAE/g), which showed a 56% increase compared to the control yoghurt. The increase in total phenolic substance continued under storage conditions. Phenolic compounds released into the yoghurt environment with the controlled release are higher than on the first day. Some unstable phenolic compounds can change into different types over time. There is also the hypothesis in the literature that phenolic compounds interact with components such as carbohydrates and proteins in the food to which they are added (Vital et al. 2018). In fact, in another study in which pomegranate was included in yoghurt, it was stated that the affinity of pomegranate anthocyanins for milk proteins is high (Trigueros et al. 2014). When these phenolic compounds are in different forms and their interactions in food, fluctuations in total phenolic substances during storage can be explained. Although the value on the first day was 1.93, 2.37 mg GAE/g was found on the last day. Similarly, Mesbah et al. (2022) reported that the concentration of Spirulina platensis powder from 0% to 1.5% resulted in an increase in the total phenolic content of yoghurt samples due to the high amounts of vitamin E, beta-carotene and oligo-elements of microalgae.

Table 1. Total phenolic content and antioxidant capacity of the samples during storage.

Sample type	Total phenolic content (mg GAE/g)				Antioxidant capacity (mg TE/g)
	Storage time (day)				Storage time (day)
	1	7	14	21	1	7	14	21
YC	1.44 ± 0.05^bC	2.01 ± 0.06^bB	2.05 ± 0.02^dAB	2.10 ± 0.01^aA	0.17 ± 0.04^bAB	0.18 ± 0.08^bAB	0.14 ± 0.00^cdB	0.25 ± 0.06^cA
YM	2.01 ± 0.23^abC	2.40 ± 0.13^bB	2.83 ± 0.10^bcA	2.28 ± 0.11^aBC	0.16 ± 0.03^bB	0.17 ± 0.03^bB	0.09 ± 0.00^dB	0.35 ± 0.15^bcA
YPA	2.12 ± 0.50^abA	2.27 ± 0.11^aA	3.31 ± 0.72^bA	3.34 ± 1.77^aA	0.30 ± 0.01^aB	0.31 ± 0.03^aB	0.25 ± 0.02^bC	0.57 ± 0.02^aA
YEPA	2.16 ± 0.93^abB	2.19 ± 0.02^aB	5.23 ± 0.25^aA	2.28 ± 0.10^aB	0.18 ± 0.05^bB	0.19 ± 0.02^bB	0.40 ± 0.02^aA	0.36 ± 0.15^bcA
YPH	2.27 ± 0.05^aB	1.97 ± 0.10^abD	3.09 ± 0.00^bcA	2.14 ± 0.09^aC	0.23 ± 0.08^abB	0.25 ± 0.02^abB	0.22 ± 0.00^bcB	0.42 ± 0.04^abA
YEPH	1.58 ± 0.12^abC	1.98 ± 0.23^bB	2.63 ± 0.00^cA	2.10 ± 0.10^aB	0.16 ± 0.02^bB	0.10 ± 0.00^bB	0.19 ± 0.12^bcB	0.31 ± 0.02^bcA
Minimum	1.44 ± 0.05	1.97 ± 0.10	2.05 ± 0.02	2.10 ± 0.01	0.16 ± 0.03	0.10 ± 0.00	0.09 ± 0.00	0.25 ± 0.06
Maximum	2.27 ± 0.05	2.40 ± 0.13	5.23 ± 0.25	3.34 ± 1.77	0.30 ± 0.01	0.31 ± 0.03	0.40 ± 0.02	0.57 ± 0.02
Average	1.93 ± 0.31	2.14 ± 0.11	3.19 ± 0.18	2.37 ± 0.36	0.20 ± 0.04	0.20 ± 0.03	0.22 ± 0.03	0.38 ± 0.07

a; Small superscripts indicate statistically different groups between samples in a storage period (P < 0.05), A; Capital superscripts indicate statistically different batches of samples at each storage period (P < 0.05). YC, control yoghurt; YEPA, 1% encapsulated pomegranate peel aqueous extract; YEPH, 1% encapsulated pomegranate peel hydroalcoholic extract; YM, 1% Spirulina microalgae; YPA, 1% pomegranate peel aqueous extract; YPH, 1% pomegranate peel hydroalcoholic extract.

The results of the antioxidant capacity analysis (ABTS) were evaluated using the trolox calibration curve (Table 1). It has been observed that the existing antioxidant capacities of samples obtained by adding encapsulated and unencapsulated Spirulina/PP extracts are further increased. In this case, the effect of valuable phenolic compounds found in the structure of PP that show an antioxidant effect is high. Phenolic compounds separated from their natural environment by extraction have a high antioxidant effect on yoghurt, which are added both as extracts and as encapsulates. At the same time, microalgae also show natural antioxidant effects due to the numerous free radicals in their content (Barkallah et al. 2017). A net increase in antioxidant capacity was also observed in yoghurt samples in which Spirulina microalgae were added. Similar results were found in the study by Shin et al. (2008). The addition of Spirulina powder significantly improved the antioxidant activity. Chlorophyll, carotenoid, phycocyanin, vitamin E, oligo-elements and many unknown bioactive compounds in the structure of Spirulina powder have been associated with this increase (Beheshtipour et al. 2012). There was an increase in the antioxidant capacity values of the bio-yoghurt samples during storage. Although the average antioxidant capacity was 0.20 mg TE/g on the 1st day of storage, it increased to 0.38 mg TE/g on the 21st day. The highest average antioxidant capacity value was the YPA sample with 0.36 mg TE/g. Since the number of phenolic compounds recovered by the aqueous extract was higher, a parallel increase in the antioxidant capacity of the yoghurt to which it was added was observed. In relevant research, Al-Hindi and Abd El Ghani (2020) reported that the antioxidant activity of the fermented milk beverage including 300 mg of PP extract per litre was higher than that of the fermented milk beverage including 150 mg of PP extract per litre. El-Said et al. (2014) stated that the use of the increasing concentration of PP extracts (5%, 10%, 15%, 20%, 25%, 30% and 35%) in the production of stirred yoghurt significantly improved the antioxidant activities of the samples by up to 25%. Barkallah et al. (2017) determined that fortification with 0.25% Spirulina powder increased the antioxidant activity of yoghurt. Da Silva et al. (2019) highlighted that the use of Spirulina encapsulated with maltodextrin crosslinked with citric acid enhanced the antioxidant properties of yoghurt throughout storage time.

Organic acid and aroma metabolomics of the samples

Yoghurts are considered a complex matrix that includes hundreds of macro- (proteins, lipids and carbohydrates) and micro-compounds (i.e. amino acids, fatty acids, organic acids, nucleic acids, peptides, minerals and aroma compounds). Degradation of milk components, including lactose, fat and proteins, by S. thermophilus and L. bulgaricus can lead to the formation of metabolomics such as organic acid and aroma compounds. Organic acids, the primary metabolomics of carbohydrate catabolism by yoghurt starters, contribute to the taste and aroma of products, as well as their bio-functional properties. The biofunctional properties of organic acids are the following: (i) protein digestion, (ii) promotion of gastrointestinal peristalsis, (iii) improving mineral absorption, (iv) enhancement of antioxidative attributes and (v) antimicrobial activity (Trigueros et al. 2011; Yilmaz-Ersan et al. 2023). The lactic, citric and uric acid values of the samples during storage with the statistical data are shown in Table 2. Statistical analyses revealed that the encapsulation process and storage time affected organic acid values (P < 0.05). The formation of lactic acid resulting from fermentation depends on the type of bacterial strains used in production. Here, lactic acid is abundant in all samples. This is followed by uric acid detected in excess and citric acid detected in small amounts. The amount of lactic acid in the samples ranged from 657.51 to 838.42 mg/kg (Table 2). The highest values were observed in the sample (YM) in which Spirulina powder was added. Microalgae, which is an important food source for yoghurt bacteria, positively affects the formation of lactic acid (Shin et al. 2008). Citric acid, known to be used during the fermentation process, is the organic acid responsible for the fresh taste (Da Costa et al. 2016). Although the average amount of citric acid in the samples was 114.96 mg/kg on the first day of storage, it was 137.15 mg/kg on the 21st day (Table 2). It was determined that the YM and YPA samples had the highest citric acid values during storage. Among the samples, the YEPA sample (425.47 mg/kg) has the lowest mean uric acid value, while the YPA sample (480.41 mg/kg) has the highest average uric acid value. During storage, the highest uric acid values were determined in the YPA sample.

Table 2. Organic acid values of the samples during storage.

Sample type	Lactic acid (mg/kg)				Citric acid (mg/kg)				Uric acid (mg/kg)
	Storage time (day)				Storage time (day)				Storage time (day)
	1	7	14	21	1	7	14	21	1	7	14	21
YC	693.40 ± 0.14^dB	697.78 ± 10.45^cAB	706.41 ± 0.61^eAB	730.74 ± 21.39^aA	109.75 ± 0.58^cA	138.28 ± 16.96^aA	169.49 ± 42.54^aA	139.55 ± 7.87^aA	450.24 ± 0.85^cA	456.95 ± 8.58^bA	449.44 ± 0.85^bA	412.32 ± 14.84^aB
YM	775.37 ± 0.15^aA	819.76 ± 2.87^aA	836.72 ± 0.01^aA	838.42 ± 165.04^aA	120.70 ± 0.37^aA	130.59 ± 2.17^aA	160.57 ± 2.68^aA	146.06 ± 29.01^aA	470.95 ± 1.29^bA	477.98 ± 9.43^aA	493.19 ± 2.12^aA	450.34 ± 72.35^aA
YPA	719.02 ± 0.62^cA	727.12 ± 6.78^bA	750.11 ± 2.52^cA	754.54 ± 63.79^aA	123.99 ± 0.18^aA	130.43 ± 1.05^aA	158.25 ± 0.87^aA	143.34 ± 34.55^aA	490.60 ± 0.72^aA	481.59 ± 7.14^aA	492.12 ± 7.26^aA	457.35 ± 53.81^aA
YEPA	676.89 ± 0.01^fA	675.83 ± 0.07^dA	760.62 ± 1.42^bA	738.86 ± 92.75^aA	111.94 ± 0.41^bC	130.38 ± 2.17^aB	168.06 ± 2.43^aA	127.01 ± 11.46^aBC	432.70 ± 0.70^eA	429.41 ± 8.94^dA	423.45 ± 2.95^dA	416.32 ± 37.85^aA
YPH	679.72 ± 0.46^eA	676.70 ± 7.64^dA	657.51 ± 0.47^fA	739.11 ± 152.47^aA	111.61 ± 0.16^bA	121.54 ± 0.30^aA	147.64 ± 3.21^aA	142.28 ± 27.62^aA	447.93 ± 0.43^dA	449.11 ± 6.15^bcA	446.30 ± 1.08^bcA	418.67 ± 80.58^aA
YEPH	721.68 ± 0.32^bAB	669.27 ± 8.70^dB	745.64 ± 0.16^dA	726.39 ± 45.14^aAB	111.78 ± 0.21^bB	129.11 ± 3.63^aB	165.22 ± 5.54^aA	124.65 ± 4.38^aB	429.92 ± 0.82^fA	431.11 ± 5.51^cdA	436.50 ± 6.88^cA	407.36 ± 12.52^aB
Minimum	676.89 ± 0.01	669.27 ± 8.70	657.51 ± 0.47	726.39 ± 45.14	109.75 ± 0.58	121.54 ± 0.30	147.64 ± 3.21	124.65 ± 4.38	429.92 ± 0.82	429.41 ± 8.94	423.45 ± 2.95	407.36 ± 12.52
Maximum	775.37 ± 0.15	819.76 ± 2.87	836.72 ± 0.01	838.42 ± 165.04	123.99 ± 0.18	138.28 ± 16.96	169.49 ± 42.54	146.06 ± 29.01	490.60 ± 0.72	481.59 ± 7.14	493.19 ± 2.12	457.35 ± 53.81
Average	711.01 ± 0.28	711.08 ± 6.09	742.84 ± 0.87	754.68 ± 90.10	114.96 ± 0.32	130.06 ± 4.38	161.54 ± 9.55	137.15 ± 19.15	453.72 ± 0.80	454.36 ± 7.63	456.83 ± 3.52	427.06 ± 45.33

]a; Small superscripts indicate statistically different groups between samples in a storage period (P < 0.05), A; Capital superscripts indicate statistically different batches of samples at each storage period (P < 0.05). YC, control yoghurt; YEPA, 1% encapsulated pomegranate peel aqueous extract; YEPH, 1% encapsulated pomegranate peel hydroalcoholic extract; YM, 1% Spirulina microalgae; YPA, 1% pomegranate peel aqueous extract; YPH, 1% pomegranate peel hydroalcoholic extract.

Taste perception, which is strongly based on formed aroma metabolomics, plays a vital role in the acceptability of yoghurt by consumers. Acetaldehyde, diacetyl and acetoin are the most important aroma compounds of yoghurt, generated by microbial metabolism, as well as the catabolism of amino acids and fatty acids. In addition to contributing to flavour, these compounds also demonstrate antimicrobial properties. Acetaldehyde is responsible for the typical flavour of yoghurt, as well as for the fresh, green flavour. It is formed by the activity of threonine aldolase in S. thermophilus and L. bulgaricus from threonine. Diacetyl generated by citrate metabolism is known to have a buttery flavour and in addition, a sweet, buttery, creamy and milky flavour is characterised. Acetoin is generated from diacetyl by the diacetyl reductase enzyme; thus, it is defined as the reduced form of diacetyl. It contains a slightly sweet, mild creamy, buttery flavour (Hegazi and Abo-Elnaga 1990; Beshkova et al. 1998; Tamime and Robinson 1999; Tian et al. 2020; Yilmaz-Ersan et al. 2023). In the present study, acetaldehyde, diacetyl and acetoin analyses were performed on the first and last days of storage. It was revealed that there were significant differences (P < 0.05) among the aroma compounds of the samples (Table 3). The highest formation of volatile aroma compounds was observed in acetoin with an average of 54.42 mg/kg. Toward the end of storage, a significant decrease in acetoin was observed in the YC, YEPA and YPH samples. A similar expected decrease in the amount of acetaldehyde was observed in the YC, YPA and YEPA samples. Although no significant changes in the amounts of diacetyl were observed in YM, YPA, YEPA and YPH samples, the taste and aroma were preserved in terms of diacetyl until the end of storage. The highest average values for the change in all types of the organic component of bio-yoghurt during storage were observed in the YEPA sample (20.08 mg/kg) for acetaldehyde, the YC sample (1.38 mg/kg) for diacetyl and the YPH sample (61.67 mg/kg) for acetoin, respectively. The amount of acetaldehyde, which was 17.84 mg/kg on the first day of storage, decreased to 17.04 mg/kg on the 21st day (Table 3). Another notable result of the study is that the acetaldehyde, acetoin and diacetyl content of the fermented milk beverage, including 150 mg of PP extract per litre was higher than that of the fermented milk beverage, including 300 mg of PP extract per litre.

Table 3. Aroma compounds of the samples on the first and final day of storage.

Sample type	Acetaldehyde (mg/kg)		Diacetyl (mg/kg)		Acetoin (mg/kg)
	Storage time (day)		Storage time (day)		Storage time (day)
	1	21	1	21	1	21
YC	20.07 ± 0.01^bA	16.52 ± 0.01^dB	1.70 ± 0.01^aA	1.05 ± 0.01^aB	69.45 ± 0.01^bA	42.42 ± 0.01^dB
YM	12.20 ± 0.01^fB	14.03 ± 0.01^eA	0.93 ± 0.01^cB	0.99 ± 0.01^bA	36.06 ± 0.01^fB	36.73 ± 0.01^eA
YPA	14.83 ± 0.01^eA	12.69 ± 0.01^fB	0.63 ± 0.01^fB	0.70 ± 0.01^fA	52.55 ± 0.01^dB	57.93 ± 0.01^bA
YEPA	21.66 ± 0.01^aA	18.50 ± 0.01^cB	0.81 ± 0.01^dB	0.82 ± 0.01^eA	37.20 ± 0.01^eA	33.28 ± 0.01^fB
YPH	18.98 ± 0.01^dB	21.09 ± 0.01^aA	0.77 ± 0.01^eB	0.88 ± 0.01^dA	72.70 ± 0.01^aA	50.63 ± 0.01^cB
YEPH	19.30 ± 0.01^cB	19.42 ± 0.01^bA	1.06 ± 0.01^bA	0.94 ± 0.01^cB	58.53 ± 0.01^cB	58.88 ± 0.01^aA
Minimum	12.20 ± 0.01	12.69 ± 0.01	0.63 ± 0.01	0.70 ± 0.01	36.06 ± 0.01	33.28 ± 0.01
Maximum	21.66 ± 0.01	21.09 ± 0.01	1.70 ± 0.01	1.05 ± 0.01	72.70 ± 0.01	58.88 ± 0.01
Average	17.84 ± 0.01	17.04 ± 0.01	0.98 ± 0.01	0.90 ± 0.01	54.42 ± 0.01	46.65 ± 0.01

a; Small superscripts indicate statistically different groups between samples in a storage period (P < 0.05), A; Capital superscripts indicate statistically different batches of samples at each storage period (P < 0.05). YC, control yoghurt; YEPA, 1% encapsulated pomegranate peel aqueous extract; YEPH, 1% encapsulated pomegranate peel hydroalcoholic extract; YM, 1% Spirulina microalgae; YPA, 1% pomegranate peel aqueous extract; YPH, 1% pomegranate peel hydroalcoholic extract.

Textural properties of the samples

Texture parameters are very effective in determining the physical properties and sensory quality of dairy products (Walia et al. 2013). These parameters are determined by the structural arrangement of the casein networks in the yoghurt gel and are also affected by the ingredients added during production and the production conditions. The texture parameters of the samples are illustrated in Table 3. There were significant differences between the textural parameters depending on the encapsulation process and the storage period (P < 0.05). Control yoghurt (YC), which is quite dense, had the highest values of firmness, consistency, cohesiveness and viscosity compared to other types. According to Prasanna et al. (2013), this means that there has been more protein rearrangement in this yoghurt. Textural properties and sensory acceptability are also known to be preserved in yoghurts added to Spirulina (Barkallah et al. 2017). In fact, the results in these yoghurts (the best YM, then YEPA and YEPH) were also good in textural terms. YPH yoghurt with less consistency had the lowest results compared to other types (Table 4). The addition of encapsulated and unencapsulated Spirulina/PP extracts significantly changed the gel firmness of the resulting yoghurts. Similarly to the study by Vital et al. (2015), lower firmness values were measured in all yoghurts except the control yoghurt. Phenolic compounds recovered in the hydroalcoholic environment were thought to interact more in the YPH and YEPA samples, where the highest decrease was observed, and this increased the softness of the yoghurt. The data obtained in the internal cohesiveness and viscosity parameters had negative values only in the vector sense. In the viscosity values changing according to the consistency results, the highest average value belongs to the YC samples (−351.78) control yoghurt, and the lowest average value belongs to the YPH sample (−204.62) (Table 4). As the storage period extended, the firmness, consistency, cohesiveness and viscosity values of all yoghurts increased and reached maximum values. As a result of the interaction of milk proteins with phenolic compounds added to yoghurt, casein networks can be rearranged and gain more stability. Yoghurts with better texture during storage may explain this situation (Vital et al. 2015). In a similar study by Al-Hindi and Abd El Ghani (2020), it was also found that the viscosity of the fermented milk beverage, including 150 mg of PP extract per litre, was higher than that of the fermented milk beverage, including 300 mg of PP extract a litre. Temiz and Ersöz (2023) studied the applicability of maltodextrin encapsulated / unencapsulated PP extract in yoghurts manufactured with cow's milk and soy drink mixtures. They indicated that PP peel extract caused unfavourable textural properties in yoghurts, negatively affecting syneresis and apparent viscosity values. Barkallah et al. (2017) determined that firmness values were significantly lower in yoghurts fortified with 0.5%, 0.75% and 1% of Spirulina powder. In contrast to firmness, the cohesiveness values did not have significant differences between the controls and samples fortified with Spirulina powder. Malik et al. (2013) observed that the higher curd strength in yoghurt with enriched Spirulina (0.1%; 0.2%; 0.3% and 0.5%) was determined with an increased amount of Spirulina.

Table 4. Texture parameters of the samples during storage.

Sample type	Firmness (g)				Consistency (g/sec)
	Storage time (day)				Storage time (day)
	1	7	14	21	1	7	14	21
YC	236.65 ± 0.11^cD	253.19 ± 0.08^cC	310.38 ± 0.01^aB	410.43 ± 0.01^aA	5887.47 ± 0.09^cD	6454.02 ± 0.06^bC	7536.37 ± 0.01^aB	10694.04 ± 0.01^aA
YM	314.07 ± 0.01^aB	327.72 ± 0.01^aA	242.66 ± 0.01^cC	280.59 ± 0.01^cD	6908.37 ± 0.01^bC	7164.48 ± 0.01^aA	6136.05 ± 0.01^cD	6990.35 ± 0.01^bB
YPA	262.89 ± 0.01^bD	268.68 ± 0.01^bB	264.59 ± 0.01^bC	283.11 ± 0.01^bA	6915.45 ± 0.01^aA	6403.00 ± 0.01^cD	6499.08 ± 0.01^bC	6539.22 ± 0.01^cB
YEPA	204.90 ± 0.01^eD	241.36 ± 0.01^dA	241.36 ± 0.01^dB	217.15 ± 0.01^dC	4837.23 ± 0.01^eD	5851.74 ± 0.01^dA	5371.10 ± 0.01^dC	5434.45 ± 0.01^dB
YPH	186.02 ± 0.01^fD	227.45 ± 0.01^eA	207.51 ± 0.01^fB	201.45 ± 0.01^fC	4501.69 ± 0.01^fD	5557.80 ± 0.01^eA	5010.24 ± 0.01^fB	4674.20 ± 0.01^fC
YEPH	209.34 ± 0.01^dC	203.73 ± 0.01^fD	213.90 ± 0.01^eA	210.46 ± 0.01^eB	5039.86 ± 0.01^dC	4950.61 ± 0.01^fD	5099.54 ± 0.01^eB	5146.61 ± 0.01^eA
Minimum	186.02 ± 0.01	203.73 ± 0.01	207.51 ± 0.01	201.46 ± 0.01	4501.69 ± 0.01	4950.61 ± 0.01	5010.24 ± 0.01	4674.20 ± 0.01
Maximum	314.07 ± 0.01	327.72 ± 0.01	310.38 ± 0.01	410.43 ± 0.01	6915.45 ± 0.01	7164.48 ± 0.01	7536.37 ± 0.01	10694.04 ± 0.01
Average	235.65 ± 0.03	253.69 ± 0.02	246.73 ± 0.01	235.65 ± 0.01	5681.17 ± 0.02	6063.61 ± 0.02	5942.06 ± 0.01	4979.81 ± 0.01

Sample type	Cohesiveness (g)				Index of viscosity (g.sec)
	Storage time (day)				Storage time (day)
	1	7	14	21	1	7	14	21
YC	−136.95 ± 0.11^dD	−154.48 ± 0.01^dC	−156.53 ± 0.04^bB	−249.36 ± 0.01^aA	−253.37 ± 0.02^dD	−320.66 ± 0.03^bC	−334.04 ± 0.01^aB	−499.00 ± 0.01^aA
YM	−164.64 ± 0.01^cB	−167.23 ± 0.01^bA	−144.97 ± 0.01^cD	−159.60 ± 0.03^cC	−333.92 ± 0.01^bB	−354.68 ± 0.01^aA	−298.07 ± 0.01^bC	−289.73 ± 0.01^cD
YPA	−172.07 ± 0.01^bC	−160.54 ± 0.01^cD	−205.48 ± 0.01^aA	−183.77 ± 0.01^bB	−339.18 ± 0.01^aB	−293.38 ± 0.01^cD	−293.42 ± 0.01^cC	−356.20 ± 0.01^bA
YEPA	−207.59 ± 0.01^aB	−227.96 ± 0.01^aA	−130.39 ± 0.01^eD	−132.13 ± 0.01^dC	−243.36 ± 0.03^eC	−239.87 ± 0.02^dD	−258.10 ± 0.02^dB	−285.37 ± 0.02^dA
YPH	−127.64 ± 0.01^eA	−124.23 ± 0.01^eB	−110.42 ± 0.01^fC	−105.03 ± 0.01^fD	−202.59 ± 0.01^fC	−238.24 ± 0.01^eA	−202.91 ± 0.01^fB	−174.79 ± 0.03^fD
YEPH	−123.24 ± 0.01^fB	−120.47 ± 0.01^fC	−140.91 ± 0.01^dA	−111.01 ± 0.01^eD	−259.66 ± 0.01^cA	−234.45 ± 0.01^fB	−203.47 ± 0.01^eD	−207.19 ± 0.01^eC
Minimum	−123.24 ± 0.01	−120.47 ± 0.01	−110.42 ± 0.01	−105.03 ± 0.01	−202.59 ± 0.01	−234.45 ± 0.01	−202.91 ± 0.01	−174.79 ± 0.01
Maximum	−207.59 ± 0.01	−227.96 ± 0.01	−205.48 ± 0.01	−249.36 ± 0.01	−339.18 ± 0.01	−354.68 ± 0.01	−334.04 ± 0.01	−499.00 ± 0.01
Average	155.36 ± 0.03	159.15 ± 0.01	148.12 ± 0.02	156.82 ± 0.01	−272.01 ± 0.02	−280.21 ± 0.02	−265.00 ± 0.01	−302.05 ± 0.02

a; Small superscripts indicate statistically different groups between samples in a storage period (P < 0.05), A; Capital superscripts indicate statistically different batches of samples at each storage period (P < 0.05). YC: control yoghurt; YEPA: 1% encapsulated pomegranate peel aqueous extract; YEPH: 1% encapsulated pomegranate peel hydroalcoholic extract; YM: 1% Spirulina microalgae; YPA: 1% pomegranate peel aqueous extract; YPH: 1% pomegranate peel hydroalcoholic extract.

Colour properties of the samples

Colour attributes, which are one of the most important visual features in dairy products, are extremely important in terms of consumer acceptance and purchasing intention (Dönmez et al. 2017). The L*, a* and b* values measured instrumentally during storage day are shown in Table 5. The encapsulation process and storage days were found to result in significant differences (P < 0.05) among the samples. Among the parameters, L* represents brightness, a represents red and green colour intensity, b* represents yellow and blue colour intensity (Şimşek et al. 2010). In general, it was observed that the colour of Spirulina microalgae was dominant in the yoghurt. The yoghurt colours differed according to the added product and were significantly affected by the storage day. This situation was also directly reflected in the colour parameter results. The L*/a*/b* values have gradually decreased. Consequently, the colours of the yoghurt samples tended to be more matt. The YC, YPA and YPH samples were closer to white. When a* values are examined, as expected, results close to green were obtained in the YM, YEPA and YEPH samples. Similar results were obtained for the values b*. A positive colour increase, that is, a movement toward yellow, was observed in YC, YPA and YPH yoghurt samples. While the highest average value in terms of L value was the YC sample (91.93), the average L values of the samples decreased toward the end of storage. As expected, the mean value was highest in the YM sample (−14.27) and lowest in the YPH sample (−1.61) (Table 5). While the average value of b was 8.72 on the first day of storage, it was 8.57 on the last day. Similar findings have been reported by Barkallah et al. (2017), Arslan and Aksay (2021) and Mesbah et al. (2022). They mentioned that control yoghurts have higher L*, a* and b* values than those of yoghurt prepared with Spirulina. They highlighted that the addition of Spirulina powder led to a darker and greenish colour.

Table 5. Colour parameters of the samples during storage.

Sample type	L*				a*				b*
	Storage time (day)				Storage time (day)				Storage time (day)
	1	7	14	21	1	7	14	21	1	7	14	21
YC	92.09 ± 0.01^aA	91.88 ± 0.01^aC	91.99 ± 0.01^aB	91.80 ± 0.02^aD	−2.39 ± 0.00^dB	−2.53 ± 0.01^dA	−2.40 ± 0.01^dB	−2.36 ± 0.00^dC	12.41 ± 0.01^aB	12.55 ± 0.01^aA	12.41 ± 0.05^aB	12.54 ± 0.04^aA
YM	54.63 ± 0.01^fA	53.41 ± 0.01^fB	53.18 ± 0.04^fC	53.46 ± 0.09^fB	−15.73 ± 0.00^aA	−13.87 ± 0.01^aC	−14.10 ± 0.01^aB	−13.39 ± 0.01^aD	5.48 ± 0.01^dA	5.07 ± 0.00^dC	5.06 ± 0.02^dC	5.18 ± 0.01^dB
YPA	86.64 ± 0.01^cA	86.36 ± 0.01^cB	86.23 ± 0.15^cB	86.25 ± 0.03^cB	−1.66 ± 0.02^eC	−1.78 ± 0.01^eB	−1.75 ± 0.01^eB	−1.83 ± 0.01^eA	12.15 ± 0.01^bB	12.27 ± 0.00^bAB	12.23 ± 0.12^bAB	12.39 ± 0.01^bA
YEPA	58.76 ± 0.05^eAB	57.88 ± 0.16^eBC	57.17 ± 0.08^eC	59.08 ± 0.69^eA	−11.27 ± 0.00^bA	−9.97 ± 0.01^bB	−9.91 ± 0.01^bC	−9.24 ± 0.00^bD	4.87 ± 0.01^eB	4.98 ± 0.01^eA	4.55 ± 0.01^fC	4.89 ± 0.01^eB
YPH	87.59 ± 0.01^bA	87.39 ± 0.04^bB	87.28 ± 0.04^bC	87.32 ± 0.04^bBC	−1.55 ± 0.00^fC	−1.63 ± 0.01^{f B}	−1.62 ± 0.00^fB	−1.68 ± 0.00^fA	11.92 ± 0.01^cA	11.77 ± 0.04^cB	11.73 ± 0.01^cB	11.75 ± 0.03^cB
YEPH	63.74 ± 0.32^dA	60.33 ± 0.31^dB	59.44 ± 0.08^dC	60.20 ± 0.06^dB	−6.91 ± 0.05^cA	−6.56 ± 0.04^cB	−6.60 ± 0.01^cB	−6.43 ± 0.02^cC	5.49 ± 0.03^dA	4.71 ± 0.05^fB	4.69 ± 0.02^eB	4.69 ± 0.06^fB
Minimum	54.63 ± 0.01	53.41 ± 0.01	53.18 ± 0.04	53.46 ± 0.09	−1.55 ± 0.00	−1.63 ± 0.01	−1.62 ± 0.00	−1.68 ± 0.00	4.87 ± 0.01	4.71 ± 0.05	4.55 ± 0.01	4.69 ± 0.06
Maximum	92.09 ± 0.01	91.88 ± 0.01	91.99 ± 0.01	91.80 ± 0.02	−15.73 ± 0.00	−13.87 ± 0.01	−14.10 ± 0.01	−13.39 ± 0.01	12.41 ± 0.01	12.55 ± 0.01	12.41 ± 0.05	12.54 ± 0.04
Average	73.91 ± 0.07	72.88 ± 0.09	72.55 ± 0.07	73.04 ± 0.16	−5.43 ± 0.01	−6.06 ± 0.02	−6.06 ± 0.01	−5.82 ± 0.01	8.72 ± 0.01	8.56 ± 0.02	8.45 ± 0.04	8.57 ± 0.03

]a; Small superscripts indicate statistically different groups between samples in a storage period (P < 0.05), A; Capital superscripts indicate statistically different batches of samples at each storage period (P < 0.05). YC, control yoghurt; YEPA, 1% encapsulated pomegranate peel aqueous extract; YEPH, 1% encapsulated pomegranate peel hydroalcoholic extract; YM, 1% Spirulina microalgae; YPA, 1% pomegranate peel aqueous extract; YPH, 1% pomegranate peel hydroalcoholic extract.

CONCLUSIONS

In this study, to bring an innovative approach to bio-yoghurt production, encapsulated and unencapsulated PP extracts in Spirulina were added to milk at a rate of 1% before fermentation. This is also the first and important study that explains very well the value of PP, which is an agricultural by-product, supports the introduction of Spirulina microalgae as a natural coating material in encapsulation technology and increases its use. With these two natural products, a new, economical and functional dairy product that may have various beneficial effects on health has been produced. The combination of encapsulated/non-encapsulated Spirulina/PP extract offers the potential for the development of value-added functional products that can be a source of high antioxidants in the dairy industry, provide a unique taste and aroma and preserve volatile substances from fruits/microalgae. This natural additive, which is not affected much by the storage process, will ensure that the yoghurts produced receive a positive response from the consumer in terms of purchasing intention and can be consumed safely. Recovery of bioactive compounds in PP as extracts and increased use of them as food ingredients due to their health-promoting functional properties contribute to efficient resource use and a circular bioeconomy.

ACKNOWLEDGEMENTS

This study is part of Nuray Yağmur's integrated doctoral thesis in Chemistry at Bursa Uludağ University. It is also TAGEM's Academic Career Project in 2018, supported by the number TAGEM/HSGYAD/A/19/A3/P1/938. Nuray Yağmur, for her support of research activities, thanked her advisor, Prof. Dr. Saliha Şahin and TAGEM for their financial support.

AUTHOR CONTRIBUTIONS

Nuray Yağmur: Formal analysis, Investigation, Methodology, Visualisation, Writing–Review & Editing, Data curation. Saliha Şahin: Conceptualisation, Investigation, Methodology, Visualisation, Data curation, Supervision. Lütfiye Yilmaz Ersan: Data curation.

FUNDING INFORMATION

This study, which is part of author Nuray Yağmur's integrated doctoral thesis at Bursa Uludag University, was supported by TAGEM with registration number TAGEM/HSGYAD/A/19/A3/P1/938.

CONFLICT OF INTEREST

The authors have declared no conflicts of interest for this article.

Open Research

DATA AVAILABILITY STATEMENT

All data generated or analysed during this study are included in the scope of this published article.

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Volume77, Issue3

August 2024

Pages 724-734

Bio-yoghurt enriched with Spirulina-encapsulated pomegranate peel: Impact on some metabolomics, antioxidative, textural and colour properties

Abstract

INTRODUCTION