The effect of aqueous extracts of some plants on in vitro antioxidant and antidiabetic activity of probiotic yogurt

Abstract

In this study, aqueous extracts of some medicinal and aromatic plants (garlic, Turkish Oregano, rosemary, basil, and peppermint) were used in probiotic yogurt production to increase functionality of probiotic yogurt. The in vitro antidiabetic, antioxidant activity, total phenolic compound content and phenolic compounds of yogurts were evaluated during the 28 day of storage period. Yogurt sample with Turkish Oregano had the highest α-amylase and α-glucosidase inhibitory activity. A strong correlation was found between total phenolic compound content and antioxidant activity (r = 0.84) and between total phenolic compounds content and α-amylase inhibitory activity (r = 0.82). In conclusion, it can be said that the total phenolic compound content and in vitro antioxidant and antidiabetic activities of probiotic yogurt could be increased by adding aqueous extracts of some plants.

Introduction

Nowadays, people have given more importance to their health. As a result of this, their dietary habits have changed and their demand for functional foods has increased. Fortified foods with bioactive components such as probiotics and antioxidants, especially herbal antioxidants, are the most important and widely used functional components (Guarner and Schaafsma 1998). Dairy products are the food products which are fortified several compounds like prebiotics, various cereals, vegetables, fruits and various medicinal and aromatic plants to develop their functionality. Probiotic bacteria are used in traditional yogurt production to enhance its functional properties. In addition probiotics, dairy products have fortified with medicinal and aromatic plants due to their bioactive compounds.

Medicinal and aromatic plants have been used as food additives all over the world, not only to develop the organoleptic properties of food, but also to increase the shelf life (Lai and Roy 2004). In addition, medicinal and aromatic plants have been subject to further researches because of their positive health benefits (Shori and Baba 2011). Medicinal and aromatic plants have valuable nutritional and therapeutic properties due to their antioxidant and phenolic contents (Shori and Baba 2014). Due to the important bioactive components in thyme, peppermint, rosemary and basil structures, they are widely subject to researches. Plants have a vital role in the treatment of Type II diabetes, especially in developing countries (Asgar 2013). Plant-based enzyme inhibitors are also preffered in developed countries because of concern about the critical side effects of synthetic pharmaceutical agents (Asgar 2013). For many years, plants have been the source of potential antidiabetic drugs (Nasser Singab and Youssef 2014). In vivo (Sucharitha and Estari 2013) and in vitro (Value et al. 2013) effect of medicinal and aromatic plants on lowering blood glucose level has determined in several researches. Angel et al. (2013) reported that peppermint juice have positive effect on blood glucose level in diabetic rats. Hanna et al. (2014) reported that use of 5% ginger and 10% thyme in diabetic rats decreased serum glucose and lipid profile levels.

Yogurt is a rich source of antioxidative peptides that can form during fermentation (Muniandy et al. 2016) and in many researches it has reported that yogurt has many antioxidative peptides (Şanlidere Aloĝlu and Öner 2011; Citta et al. 2017). Moreover, antidiabetic, antihypertensive, and antimicrobial peptides have been isolated yogurt in many researches.

Nowadays, dairy products have been successfully used to carry phytochemicals and other nutrients for health benefits (El-Sayed and Youssef 2019). In this study, aqueous extracts of garlic (Allium sativum), Turkish Oregano (Origanum onites), rosemary (Rosmarinus officinalis L.), basil (Ocimum basilicum L.), and peppermint (Mentha piperita L.) were used in probiotic yogurt production to enhance the its functional properties. In this study, it was aimed to determine the effect of aqueous extracts of medicinal and aromatic plants on total phenolic compound content, phenolic compounds, in vitro antioxidant (DPPH radical scavenging activity) and antidiabetic (α-amylase and α-glycosidase inhibitory activity) activities of probiotic yogurts.

Materials and method

Materials

The cow milk was obtained from the Menemen Research and Application Farm of Ege University Faculty of Agriculture, Izmir, Turkey. Yogurt culture containing Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophilus, and the Lactobacillus casei (Lafti L26), and Bifidobacterium longum (Lafti B22) probiotic cultures provided from CSL-Centro Sperimentale del Latte, Italy and DSM, Germany, respectively. Turkish Oregano (Origanum onites L.), rosemary (Rosmarinus officinalis L.), basil (Ocimum basilicum L.), peppermint (Mentha piperita L.) and garlic (Allium sativum) were obtained from the Aegean Agricultural Research Institute, Izmir, Turkey.

Method

Preparation of the aqueous extracts of medicinal and aromatic plants

Firstly, undesired materials from the medicinal and aromatic plants were removed. The plants were washed and boiled for a minute to reduce their microbiological load. Later, the plants were cut to desired sizes and 10 g of each plant was weighed and incubated with 100 mL distilled water in a water bath at 70 °C for a night to obtain the aqueous extracts of the plants.

Yogurt production

For the activation of yogurt and probiotic starter cultures, 13% skim milk powder was used. The starter cultures prepared according to the manufacturer instructions (at 10⁸–10⁹ cfu/mL viability level). The milk used in yogurt production was pasteurized at 85–90 °C for 5 min. After pasteurization, the milk was cooled to 37–40 °C and activated yogurt and probiotic cultures were added to the milk. Mixture was incubated at 37 °C since the pH value reached at 4.6–4.7 level. After fermentation, yogurt was divided into six groups and 1% (v/w) aqueous extracts of medicinal and aromatic plants added each yogurt group. Yogurt samples were stored at 4 °C for 28 days and analyses were carried out on 1st, 14th and 28th day of storage.

Total phenolic compound content

The total phenolic compound content of the yogurt samples was determined using the Folin method described by Satir and Guzel-Seydim (2015). Firstly, yogurt samples (1 mL) were mixed with 1 mL of 95% ethanol and 5 mL of distilled water. Thereafter, 0.5 mL of Folin-Ciocalteu’s reagent (ten fold diluted) was added to the mixture and the mixture was rested for 2 min at room temperature. Then, 1.5 mL of 20% Na₂CO₃ solution was added to the mixture and rested at room temperature at dark for 2 h to complete the reaction. Absorbances were measured at 760 nm using spectrophotometer (Varian Cary 50 Bio UV-Visible, Australia). The total phenolic compound content was calculated as mg gallic acid equivalent (GAE)/100 g sample.

Determination of phenolic compounds

The phenolic compounds of the samples were determined described by Cimo et al. (2013) with some modifications. The analyses were carried out in the Ege University Faculty of Pharmacy Pharmaceutical Sciences Research Laboratory, Izmir, Turkey. 1 g of yogurt sample was mixed with 5 mL of methanol (Sigma-Aldrich, HPLC grade). The mixture was vortexed (IKA MS 3 digital) for 20 min and then, centrifuged at 35,533 g (Beckman Coulter Avanti J-E Centrifuge) for 20 min. Later, the mixture was filtered (Millipore, 0.45 µm) and injected into the HPLC (Thermo Scientific Accela, Waltham, Massachusetts, USA) system consisting of photodiode array (PDA) detector. The ACE 5 C18 column (250 × 4.6 mm I.D.) with a 5 μm packing (Aberdeen, Scotland) used and flow was setted 0.8 mL/min and injection volume was 10 µL. The composition of mobile phase A is acetonitrile (100%) (Sigma, St Louis, USA) and mobile phase B is 0.01% trifluoracetic acid (TFA, Sigma, St Louis, USA) in deionized HPLC-grade water. The samples were eluted initially 10–20% A for 4.5 min. Then with a gradient from 20 to 70% A for 5.5 min and followed by a linear gradient from 30 to 90% B for 2 min. The elute was monitored at 200 and 600 nm for 12 min. The phenolic compounds were compared with peak areas of each standard.

Preparation of the yogurt extracts for biological analyses

To prepare the extracts of yogurt samples, 2.5 mL of sterile distilled water was added to 10 g of yogurt sample and homogenized. Then, the pH values of the samples were adjusted to pH 4 with 0.1 M HCl. Later, the samples were heated in a water bath at 45 ˚C for 10 min and centrifuged at 2655 g for 10 min. In the following stage, the pH value of the supernatant was adjusted to pH 7.0 with 0.1 N NaOH and recentrifuged at 2655 g for 10 min (Shori and Baba 2013). The supernatant was used in determining of DPPH radical scavenging, α-amylase and α-glucosidase inhibitory activity.

Determination of the antioxidant activity using the 1,1-diphenyl-2-picrylhydrazyl (DPPH) radical scavenging method

The antioxidant activities of the samples were determined using the method described by Illupapalayam et al. (2014) after making minor modifications. The antioxidant activity was expressed as radical scavenging activity (RSA). The measurements were carried out at 517 nm using spectrophotometer (Varian Cary 50 Bio UV–Visible, Australia). The RSA (%) values of the samples were calculated using the formula below.

$$\text{RSA}\%=\left[\frac{\left({\text{Absorbance}}_{\text{control}}-{\text{Absorbance}}_{\text{sample}}\right)}{{\text{Absorbance}}_{\text{control}}}\right]\times 100$$

Determination of α-amylase inhibitory activity

The α-amylase inhibitory activity of the yogurt samples was determined described by Apostolidis et al. (2006). A mixture of 500 µL of yogurt extract and 500 µL of 0.02 M sodium phosphate buffer (pH 6.9 with 0.006 M sodium chloride) containing amylase solution (0.5 mg/mL) was incubated at 25 °C for 10 min. After preincubation, 500 µL of 1% starch solution in 0.02 M sodium phosphate buffer (pH 6.9 with 0.006 M sodium chloride) was added to each tube and then, incubated at 25 °C for 10 min. The reaction was stopped using 1 mL dinitro salicylic acid color reagent. Then, the test tubes were incubated in a boiling water bath for 5 min and cooled to room temperature. The reaction mixture was diluted after adding 10 mL distilled water and absorbance was measured at 540 nm. The α-amylase inhibitory activity was given in inhibition percent and calculated below formula:

$$\text{Inhibitory activity}\%=\left[\frac{\left({\text{Absorbance}}_{\text{control}}-{\text{Absorbance}}_{\text{sample}}\right)}{{\text{Absorbance}}_{\text{control}}}\right]\times 100$$

Determination of α-glucosidase inhibitory activity

The α-glucosidase inhibitory activity of the yogurt samples was determined described Apostolidis et al. (2006). 500 µlL ofsample yogurt extract and 1000 µL of 0.1 M phosphate buffer (pH 6.9) containing α-glucosidase solution (1.0 U/mL) was mixed and the mixture was incubated at 25 °C for 10 min. After preincubation, 500 µL of 5 mM p-nitrophenyl-α-D-glucopyranoside solution in 0.1 M phosphate buffer (pH 6.9) was added to the mixture. The reaction mixtures were incubated at 25 °C for 5 min. Absorbance values were recorded at 405 nm before and after incubation. The α-glucosidase inhibitory activity was given in inhibition % and calculated below formula:

$$\text{Inhibitory activity}\%=\left[\frac{\left({\text{Absorbance}}_{\text{control}}-{\text{Absorbance}}_{\text{sample}}\right)}{{\text{Absorbance}}_{\text{control}}}\right]\times 100$$

Statistical analysis

The research was conducted with two repetitions, and all analyses were performed in three parallels. For the statistical evaluation of analysis results, a one-way analysis of variance (ANOVA) in the SPSS version 25.0 (SPSS Inc. Chicago, Illinois) using the DUNCAN test was used. Correlation coefficient was calculated using Pearson Correlation Test. P < 0.05 was considered a statistically significant difference.

Results and discussion

Total phenolic compound content (TPC)

Phenolic compounds are bioactive substances that have important effects on human health. Within this context, the total phenolic compound content was investigated, and the results are given in Fig. 1. During the storage period, the TPC of the aqueous extracts of medicinal and aromatic plants added samples ranged from 34.56 to 79.58 mg gallic acid equivalents (GAE)/100 g, while the phenolic compound content of control sample ranged from 20.16 to 36.06 mg GAE/100 g. Both 1st and 28th day of the storage period, R sample had the highest TPC content. In all samples, a regular increase in the TPC content was observed during the 28 day of storage period. TPC content of the samples significantly changed during the storage period (P < 0.05). However, the control sample did not contain aqueous plant extract, TPC content of this sample was about 20.16 mg GAE/100 g. TPC content of the control yogurt can be associated with the phenolic compounds occurring due to the degradation of milk protein (Damin et al. 2009). Another cause could be the microbial use of phenolic acids such as ferulic and p-coumaric acid during fermentation and post-acidification that causes the production of other phenolic acids such as vanillic acid and p-hydroxybenzoic acid (Blum 1998). The increase in the TPC content of the plant containing yogurts is attributable to the presence of plant specific phytochemical compounds (such as flavonoids and phenolic compounds, etc.) (Amirdivani and Baba 2011). Amirdivani and Baba (2011) stated that the maximum TPC content was determined aqueous extracts of dill, peppermint, basil added and plain yogurt, respectively. Similar to Amirdivani and Baba (2011) research results, in this study, peppermint added sample had more TPC compared to basil added yogurt sample. In the Amirdivani (2015) study, there was not statistically difference between plain and aqueous garlic extract added yogurt.

Fig. 1.

Total phenolic compound content (mg GAE/100 g) of samples during the storage period. C: Control sample (not containing medicinal and aromatic plant), G: garlic containing yogurt, T: Turkish Oregano containing yogurt, R: rosemary containing yogurt, M: peppermint containing yogurt, B: basil containing yogurt

Determination of phenolic compounds

The phenolic compounds of the samples were determined using an RP-HPLC method on 1st and 28th day of the storage. Gallic acid, catechin hydrate, ferulic acid, chlorogenic acid, rutin, quercetin-3-glucoside, ellagic acid, luteolin and apigenin phenolics were determined and results are given in Table 1.

Table 1.

Phenolic compounds and their concentration (µg/mL) in samples during the storage period

Sample/day	Phenolic compounds and their concentrations (µg/mL)
Day 1	Gallic acid	Catechin hydrate	Ferulic acid	Chlorogenic acid	Rutin	Quercetin 3-glucoside	Ellagic acid	Luteolin	Apigenin
C	ND	ND	ND	1.031	ND	ND	0.290	ND	ND
G	ND	ND	ND	0.877	ND	ND	1.351	ND	0.536
T	0.405	0.657	0.180	0.901	ND	ND	1.434	ND	ND
R	0.240	0.952	0.217	1.096	ND	ND	1.375	ND	ND
M	ND	0.511	ND	0.921	0.810	ND	1.274	ND	ND
B	ND	ND	0132	1.197	1.225	ND	0.574	0.378	0.730
Day 28
C	ND	ND	ND	1.320	ND	ND	1.922	0.302	ND
G	0.079	0.542	0.219	26.143	ND	ND	2.270	0.285	5.536
T	0.215	ND	0.620	1.019	ND	0.198	1.306	ND	ND
R	0.198	0.847	0.285	0.851	ND	ND	1.808	0.115	ND
M	0.304	ND	0.087	1.062	5.124	ND	2.678	0.256	ND
B	0.358	ND	ND	1.057	0.678	ND	1.695	ND	ND

C: Control sample (not containing medicinal and aromatic plant), G: garlic containing yogurt, T: Turkish Oregano containing yogurt, R: rosemary containing yogurt, M: peppermint containing yogurt, B: basil containing yogurt, ND: Not determined

Chlorogenic acid and ellagic acid were detected in all samples and their contents were higher than other detected phenolics. The G sample contained chlorogenic acid at 0.877 µg/mL level on the 1st day of the storage but surprisingly its chlorogenic acid content increased by about 30-fold and reached 26.143 µg/mL at the end of the storage. Vallverdú-Queralt et al. (2014) stated that chlorenic acid levels of rosemary, thyme, oregano, cinnamon, cumin and bay were similar. Gallic acid is a commonly found phenolic compound in dairy products while it was not detected in the C, G, M and B samples on the 1st day of the storage. Contrary to this, except for the control sample, all samples contained gallic acid on 28th day of storage. The T sample had the highest gallic acid content on the 1st day of storage (0.405 µg/mL). The quercetin-3-glycosid was detected only T sample on the 28th day of the storage at 0.198 µg/mL level and apigenin was detected only G sample on the 1st and 28th day of the storage. The apigenin content of G sample on the 28th day of the storage (0.536 µg/mL) reached 10 times more on the 28th day of the storage (5.36 µg/mL). The rutin was detected only M and B samples on the 1st and 28th day of the storage. Karadag (2019) studied the phenolic components of some medicinal and aromatic plants. In this study, quercetin was determined in many plant extracts, while rutin was determined only in mint and basil. However, gallic acid was not detected in mint extract, but it was found in basil. It was reported that the most common phenolic acids in medicinal and aromatic plants were protocatheuic acid, caffeic acid, chlorogenic acid, ferulic acid, and flavonoids quercetin and kaempferol (Karadag 2019). The content of phenolic compounds found in plants varies according to the plant type, variety, climate and cultivation style. In the case of using plant extracts in foods such as yogurt, we can mention that the phenolic compound transition will be at different levels from the plants due to the interactions with the protein, fat, sugar and some factors such as the acidity increase during storage. In addition, the phenolic content in yogurt can be explained by the formation and / or breakdown of polymeric phenolics during fermentation by yogurt bacteria. In the present study, it is stated that the phenolic compound and its concentration changed depending on the duration of storage and the medicinal and aromatic plant type.

Antioxidant activity

In the present study, DPPH assay was evaluated for determination of antioxidant activity of the samples. The DPPH radical scavenging activity (RSA) results are shown in Fig. 2. During the storage period, RSA value of the samples varied from 16.40% (C) to 75% (R). During the storage period, the R sample had the highest RSA value while C sample had the lowest RSA value. These results paralled with the TPC content of samples during the storage period.

Fig. 2.

DPPH radical scavenging activity (%) of samples during the storage period. C: Control sample (not containing medicinal and aromatic plant), G: garlic containing yogurt, T: Turkish Oregano containing yogurt, R: rosemary containing yogurt, M: peppermint containing yogurt, B: basil containing yogurt

The antioxidant activity of the samples were increased parallel with TPC content (correlation coefficient = 0.84) and significantly changed during the storage period (P < 0.05). At the end of the storage period, the R sample had the highest antioxidant activity followed by G, B, M, T, C sample, respectively. The medicinal and aromatic plant added samples have higher antioxidant activity due to the phytochemical contents of the plants. Besides this, during the storage period in yogurt samples, proteolysis originating from yogurt starter bacteria and probiotic bacteria was occurred. Due to this proteolysis, antioxidant peptides could be released and showed DPPH radical scavenging activity.

Similar to our study, Amirdivani and Baba (2011) found that all plant containing (peppermint, dill, basil) yogurts had higher antioxidant activity compared with plain yogurts during the storage period (P < 0.05). Gurkan and Hayaloglu (2017) stated that yogurt samples produced with water extract of basil had more DPPH radical inhibition rate compared to control sample. But in their study, contrary to our research, they found decrease in DPPH radical inhibiton rate of yogurt samples during the storage period.

α-glucosidase and α-amylase Inhibitory Activity

Type II diabetes is one of the chronic diseases that is characterized by abnormalities in blood glucose levels, whose frequency is increasing worldwide. The International Diabetes Federation (IDF) reports that in 2035, 592 million people will suffer from Type II diabetes disease. Therefore, effective management strategies of diabetes are of primary importance (Lacroix and Li-Chan 2013).

α-glucosidase and α-amylase are enzymes that trigger Type II diabetes by increasing blood glucose levels by providing rapid breakdown of starch and sugar after a mixed carbohydrate diet (Oboh et al. 2014). Retarding the absorption of glucose via inhibition of these enzymes is an important method in controlling Type II diabetes (Asgar 2013).

Epidemiological studies showed that polyphenols especially flavonoids and foods containing high content of polyphenols may have beneficial effects in preventing diabetes development (Liu et al. 2014). In addition to polyphenols, peptides with antidiabetic properties originating from casein and whey proteins from dairy products including yogurt can be released and showed inhibitory effect on these enzymes. The positive effect of yogurt consumption is explained by its ability to balance postprandial blood sugar, which is defined as the glucose amount in blood (Shori and Baba 2011).

In the present study, α-glucosidase and α-amylase inhibitory activity levels of samples were investigated (Figs. 3, 4). Research results showed that, the α-glucosidase inhibitory activity in the yogurt samples containing the aqueous extracts of medicinal and aromatic plants relatively increased during the storage period except control and B samples and reached maximum values on day 28 of storage. During the 28 day of the storage period, α-glucosidase inhibitory activities of all samples were ranged from 7.6 (C) to 23.08% (T).

Fig. 3.

α-glucosidase inhibitory activity (%) of samples during the storage period. C: Control sample (not containing medicinal and aromatic plant), G: garlic containing yogurt, T: Turkish Oregano containing yogurt, R: rosemary containing yogurt, M: peppermint containing yogurt, B: basil containing yogurt

Fig. 4.

α-amylase inhibitory activity (%) of samples during the storage period. C: Control sample (not containing medicinal and aromatic plant), G: garlic containing yogurt, T: Turkish Oregano containing yogurt, R: rosemary containing yogurt, M: peppermint containing yogurt; B: basil containing yogurt

The control sample had the lowest α-glucosidase inhibitory activity during the storage period. The comparison of the samples both with themselves and each other revealed that there were significant differences (P < 0.05) between their α-glucosidase inhibitory levels on day 28 of storage. The highest α-glucosidase inhibitory activity was obtained in the T and R samples during the storage period parallel with total phenolic compound content. It can be said that Turkish Oregano and rosemary stems from phenols such as thymol and carvacrols, flavonoids, terpenoids and certain polyphenols with a polymerized structure (Kaushik et al. 2010). Ni et al. (2018) found that α-glucosidase inhibitory activities of yogurt produced with aqueous extracts of salal berry and blackcurrant pomace were increased all samples during the storage period.

In the present study, on the 1st day of the storage, the highest α-amylase inhibitory activity was observed in the G sample (28.76%), followed by the R (26.66%) and M (25.8%) samples (Fig. 4). During the storage period, a regular increase was observed in samples, except for the C and G samples. On the 14th and 28th day of the storage, in parallel with α-glucosidase inhibitory activity and TPC content results, the highest α-amylase inhibitory activity values were observed in the T and M samples, respectively. The continuing α-amylase inhibitory activity during storage indicates that the phenolic compounds attach to the active surfaces of enzymes with catalytic activity and, in general terms, carbohydrate-hydrolyzing enzymes are safe and have an inhibitory potential (McCue and Shetty 2004; Lee et al. 2008).

Furthermore, it can be said that cold storage period has also increased the α-amylase inhibitory activity, except for the C and G samples. The decrease in α-amylase inhibitory activity during the storage period may be resulted from degradation of phenolic compounds and/or milk protein-polyphenol interaction (Amirdivani and Baba 2011). As a result of the relationship between phenolic compounds and proteins, insoluble compounds can be formed (Liu et al. 2017), which can adversely affect the in vivo bioavailability of both phenolics and proteins (Liu et al. 2017). However, fermentation process can changed the polyphenol-protein interactions (Oboh et al. 2009). Due to the fermentation, some of the protein-bound polyphenols were transformed into the free soluble polyphenols and help to enhance the antioxidant activities (Oboh et al. 2009). Ni et al. (2018) found that α-amylase inhibitory activities of yogurt produced with aqueous extracts of salal berry and blackcurrant pomace were increased in all samples during the storage period. Shori and Baba (2014) reported that garlic (A. sativum) enriched cow and camel milk yogurt samples showed higher α-amylase inhibition than their respective control samples. Shori and Baba (2013) and Vankudre et al. (2015) reported that α-amylase inhibitory activity is also related to proteolysis and ACE-inhibitory activity. In the present study, it can be said that usage of aqueous extracts of medicinal and aromatic plants in probiotic yogurt help to increase α-amylase inhibitory activity.

Conclusion

In the present study, aqueous extracts of garlic, Turkish Oregano, rosemary, peppermint and basil used in probiotic yogurt production. It is determined that all samples have more total phenolic compound content than control yogurt. The R sample has the highest TPC content during the storage period. Parallel to TPC results, the highest antioxidant activity was detected in R sample. Chlorogenic acid and ellagic acid were detected in all samples and their contents were higher than other detected phenolics. The T sample showed the maximum α-amylase and α-glucosidase inhibitory activity. The maximum strong correlation was found between TPC content and antioxidant, α-amylase inhibitory activity. In conclusion, in this study, it is seen that antioxidant, antidiabetic properties of probiotic yogurt could be improved using some medicinal and aromatic plants and plant added probiotic yogurt can have good potent for treatment of Type II diabet and some degenerative diseases. It can be said that more detailed researches are needed about effect of interaction between milk proteins and plants on some biological activities like antioxidant, antidiabetic and antihypertensive.

Author’s contribution

The design of study was done by Ozer Kinik. The analysis and interpretation of data were performed by Ecem Akan, Oktay Yerlikaya, and Ozge Yildiz Bayram, The manuscript was drafted by Ecem Akan. All authors read and approved the final manuscript.

Funding

This research was funded from Ege University Scientific Research Projects Coordination with 2015-ZRF-17 Project Number.

Availability of data and materials

The results of the study will be sent to the author via e-mail upon request.

Declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Consent for publication

The authors accept that the manuscript will be published by Journal of Food Science and Technology.