Investigation of the Viability of Probiotic Microorganisms in a Synbiotic Kefir Beverage Enriched with Pistachio (Pistacia vera) and Hazelnut (Corylus avellana L.) Oils

Document Type : Original Article

Authors

1 Department of Biology, QaS.C., Islamic Azad University, Qaemshahr,Iran

2 Department of Biology, Ro.C., Islamic Azad University, Roudehen, Iran

3 Department of Food Science and Technology, Ro.C., Islamic Azad University, Roudehen, Iran

Abstract

Kefir is a fermented beverage rich in probiotic microorganisms whose viability during storage is limited by environmental stresses, so prebiotic compounds are often needed to improve their survival. This study evaluated the effect of adding pistachio and hazelnut oils, as prebiotic and bioactive compounds, on the viability of the probiotic microorganisms of kefir and on its physicochemical, antioxidant and sensory properties. The oils were extracted by Soxhlet apparatus and characterised, and synbiotic kefir was then prepared with them at single (1.5% and 3%) and combined levels and compared with an oil-free control over 20 days of refrigerated storage. Both oils had low acidity and low peroxide values. Hazelnut oil gave the lower half-maximal inhibitory concentration (IC₅₀) values in the 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid) (ABTS) and 2,2-diphenyl-1-picrylhydrazyl (DPPH) assays, whereas pistachio oil showed the stronger antimicrobial activity, with the lowest minimum inhibitory concentration (MIC) against Listeria monocytogenes. Throughout storage, oil addition significantly maintained a higher pH and a lower titratable acidity than the control (P < 0.05). The combined P2H2 treatment (1.5% pistachio + 1.5% hazelnut oil) retained the highest total phenolic content and antioxidant activity, preserved the highest microbial counts on day 20, and gave the highest cell-surface hydrophobicity, while the milder P1H1 treatment achieved the best overall sensory acceptance. In conclusion, pistachio and hazelnut oils acted as effective prebiotic agents that improved probiotic survival and enhanced the functional value of kefir, offering a practical option for developing more stable probiotic products.

Keywords

References

AOAC. (2000). Official Methods of Analysis (17th ed.). Association of Official Analytical Chemists, Gaithersburg, MD, USA.
Al Juhaimi, F., Özcan, M. M., Ghafoor, K., Babiker, E. E., & Hussain, S. (2018). Comparison of cold-pressing and soxhlet extraction systems for bioactive compounds, antioxidant properties, polyphenols, fatty acids and tocopherols in eight nut oils. Journal of food science and technology, 55, 3163-3173.
Alasalvar, C., & Bolling, B. W. (2015). Review of nut phytochemicals, fat-soluble bioactives, antioxidant components and health effects. British Journal of Nutrition, 113(S2), S68-S78. doi:10.1017/S0007114514003729
Alma, M. H., Nitz, S., Kollmannsberger, H., Digrak, M., Efe, F. T., & Yilmaz, N. (2004). Chemical composition and antimicrobial activity of the essential oils from the gum of Turkish pistachio (Pistacia vera L.). Journal of agricultural and food chemistry, 52(12), 3911-3914.
Altaee, R. T., Aldabbagh, M. G., & Rashan, A. I. (2024). Detection of fatty acids and some secondary metabolites in macadamia and hazelnut fruits and their shells, with studding the physiochemical properties of its extracted oil: a comparative study. Academia Open, 9(2), 10.21070/acopen. 21079.22024. 29637-21010.21070/acopen. 21079.22024. 29637.
Anwar, A. P. M., Maruddin, F., Yuliati, F. N., Wangdi, J. T., & Dagong, M. I. A. (2021). The physiochemical properties of kefir using honey concentrations. Canrea Journal: Food Technology, Nutritions, and Culinary Journal, 8-16.
Arranz, S., Cert, R., Pérez-Jiménez, J., Cert, A., & Saura-Calixto, F. (2008). Comparison between free radical scavenging capacity and oxidative stability of nut oils. Food Chemistry, 110(4), 985-990.
Balik, H. I. (2021). Bioactive compounds and fatty acid composition of new Turkish hazelnut cultivars. International Journal of Fruit Science, 21(1), 106-114.
Barzegar, H., Alizadeh Behbahani, B., & Falah, F. (2021). Safety, probiotic properties, antimicrobial activity, and technological performance of Lactobacillus strains isolated from Iranian raw milk cheeses. Food Science & Nutrition, 9(8), 4094-4107.
Beltrán-Barrientos, L., Hernández-Mendoza, A., Torres-Llanez, M., González-Córdova, A., & Vallejo-Córdoba, B. (2016). Invited review: Fermented milk as antihypertensive functional food. Journal of Dairy Science, 99(6), 4099-4110.
Bisignano, C., Filocamo, A., Faulks, R. M., & Mandalari, G. (2013). In vitro antimicrobial activity of pistachio (Pistacia vera L.) polyphenols. FEMS microbiology letters, 341(1), 62-67.
Borisova, A. (2022). Comparative characteristics of the content of phenolic substances and antioxidant activity of some types of nuts eaten. Chemistry of plant materials, 2, 95-104.
Burt, S. (2004). Essential oils: their antibacterial properties and potential applications in foods—a review. International journal of food microbiology, 94(3), 223-253.
Cavia, M. M., Fernández-Muiño, M. A., Gömez-Alonso, E., Montes-Pérez, M. J., Huidobro, J. F., & Sancho, M. T. (2002). Evolution of fructose and glucose in honey over one year: influence of induced granulation. Food chemistry, 78(2), 157-161.
Chen, C.-Y. O., & Blumberg, J. B. (2008). Phytochemical composition of nuts. Asia Pacific Journal of clinical nutrition, 17.
Cutrim, C. S., Torres, F. R., & Cortez, M. A. S. (2023). Sensorial and instrumental parameters of chocolate-flavored dairy desserts obtained in the retail trade. Ciência Animal Brasileira, 24, e-74566E.
Dris, I., Tabart, J., Brahim, I., Chafaa, S., Mimeche, F., & Kebieche, M. (2024). Antibacterial activity and minimum inhibitory concentration of Cedar atlantica and Pistacia atlantica essential oils against both gram negative and gram positive bacterial strains. Studies in Engineering and Exact Sciences, 5(2), e11825-e11825.
Ekinci, F. Y., Okur, O. D., Ertekin, B., & Guzel‐Seydim, Z. (2008). Effects of probiotic bacteria and oils on fatty acid profiles of cultured cream. European Journal of Lipid Science and Technology, 110(3), 216-224.
El Atki, Y., Aouam, I., El Kamari, F., Taroq, A., Lyoussi, B., Oumokhtar, B., & Abdellaoui, A. (2020). Phytochemistry, antioxidant and antibacterial activities of two Moroccan Teucrium polium L. subspecies: preventive approach against nosocomial infections. Arabian Journal of Chemistry, 13(2), 3866-3874.El-Atki et al. (2020).
Ellahi, H., Sadrabad, E. K., Hekmatimoghaddam, S. H., Jebali, A., Sadeghizadeh-yazdi, J., Rastiani, F., & Mohajeri, F. A. (2019). Antimicrobial activity and chemical composition of Pistachia atlantica gum sub sp. kurdica. Essential oil. Journal of Nutrition and Food Security.
Falah, F., Shirani, K., Vasiee, A., Yazdi, F. T., & Behbahani, B. A. (2021). In vitro screening of phytochemicals, antioxidant, antimicrobial, and cytotoxic activity of Echinops setifer extract. Biocatalysis and Agricultural Biotechnology, 35, 102102.
108
Ghanbari, M., Ghasemi, J. B., & Mortazavian, A. M. (2017). Comparison of three sensory characterization methods based on consumer perception for the development of a novel functional cereal-based dessert. AIMS Agriculture & Food, 2(3).
Ghazanfari, N., Mortazavi, S. A., Yazdi, F. T., & Mohammadi, M. (2020). Microwave-assisted hydrodistillation extraction of essential oil from coriander seeds and evaluation of their composition, antioxidant and antimicrobial activity. Heliyon, 6(9).
Ghirardello, D., Zeppa, G., Rolle, L., Gerbi, V., Contessa, C., Valentini, N., . . . Griseri, G. (2014). Effect of different storage conditions on hazelnut quality. Acta Horticulturae, 1052(1), 315-318.
Givianrad, M., Saber-Tehrani, M., & Mohammadi, S. J. (2013). Chemical composition of oils from wild almond (Prunus scoparia) and wild pistachio (Pistacia atlantica). Grasas y Aceites, 64(1), 77-84.
Gutiérrez-del-Río, I., López-Ibáñez, S., Magadán-Corpas, P., Fernández-Calleja, L., Pérez-Valero, Á., Tuñón-Granda, M., . . . Lombó, F. (2021). Terpenoids and polyphenols as natural antioxidant agents in food preservation. Antioxidants, 10(8), 1264.
Horwitz, W. (Ed.). (2010). Official Methods of Analysis of AOAC International (18th ed.). AOAC International, Gaithersburg, MD, USA.
Hossain, M. A., & Rahman, S. M. (2011). Total phenolics, flavonoids and antioxidant activity of tropical fruit pineapple. Food Research International, 44(3), 672-676.
Johnson, M. E., & Steele, J. L. (2007). Fermented dairy products. In Food Microbiology: Fundamentals and Frontiers, Third Edition (pp. 767-781): American Society of Microbiology.
Karaosmanoglu, H., Soyer, F., Ozen, B., & Tokatli, F. (2010). Antimicrobial and antioxidant activities of Turkish extra virgin olive oils. Journal of agricultural and food chemistry, 58(14), 8238-8245.
Kök-Taş, T., Seydim, A. C., Özer, B., & Guzel-Seydim, Z. B. (2013). Effects of different fermentation parameters on quality characteristics of kefir. Journal of Dairy Science, 96(2), 780-789.
Król, K., Gantner, M., & Piotrowska, A. (2021). The Quality Characteristic and Fatty Acid Profile of Cold-Pressed Hazelnut Oils during Nine Months of Storage. Agronomy, 11(10), 2045. Retrieved from https://www.mdpi.com/2073-4395/11/10/2045
Kwak, H., Park, S., & Kim, D. (1996). Biostabilization of kefir with a nonlactose-fermenting yeast. Journal of Dairy Science, 79(6), 937-942.
Labiad, M. H., Harhar, H., Ghanimi, A., & Tabyaoui, M. (2017). Phytochemical screening and antioxidant activity of Moroccan Thymus satureioïdes extracts. Journal of Materials and Environmental Sciences, 8(6), 2132-2139.
Lethuaut, L., Weel, K. G., Boelrijk, A. E., & Brossard, C. D. (2004). Flavor perception and aroma release from model dairy desserts. Journal of agricultural and food chemistry, 52(11), 3478-3485.
Ling, B., Yang, X., Li, R., & Wang, S. (2016). Physicochemical properties, volatile compounds, and oxidative stability of cold pressed kernel oils from raw and roasted pistachio (Pistacia vera L. Var Kerman). European Journal of Lipid Science and Technology, 118(9), 1368-1379.
Maguire, L., O'sullivan, S., Galvin, K., O'connor, T., & O'brien, N. (2004). Fatty acid profile, tocopherol, squalene and phytosterol content of walnuts, almonds, peanuts, hazelnuts and the macadamia nut. International journal of food sciences and nutrition, 55(3), 171-178.
Man, A., Santacroce, L., Iacob, R., Mare, A., & Man, L. (2019). Erratum: Man, A., et al. Antimicrobial Activity of Six Essential Oils Against a Group of Human Pathogens: A Comparative Study. Pathogens 2019, 8, 15. Pathogens, 8(3), 108.
Markowiak, P., & Śliżewska, K. (2017). Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients, 9(9), 1021.
McGovern, C. J., González-Orozco, B. D., & Jiménez-Flores, R. (2024). Evaluation of kefir grain microbiota, grain viability, and bioactivity from fermenting dairy processing by-products. Journal of Dairy Science, 107(7), 4259-4276.
Miraliakbari, H., & Shahidi, F. (2008). Oxidative stability of tree nut oils. Journal of agricultural and food chemistry, 56(12), 4751-4759.
Mith, H., Dure, R., Delcenserie, V., Zhiri, A., Daube, G., & Clinquart, A. (2014). Antimicrobial activities of commercial essential oils and their components against food‐borne pathogens and food spoilage bacteria. Food science & nutrition, 2(4), 403-416.
Moghanjougi, Z. M., Bari, M. R., Khaledabad, M. A., Almasi, H., & Amiri, S. (2020). Bio-preservation of white brined cheese (Feta) by using probiotic bacteria immobilized in bacterial cellulose: Optimization by response surface method and characterization. Lwt, 117, 108603.
Moghimani, M., Salari, A., Hashemi, M., Soleimanpour, S., Ranjbar, G., & Afshari, A. (2023). Iranian traditional kefir beverage: isolation and identification of beneficial microorganisms and evaluation of antimicrobial activity against food-borne pathogens. Nutrition & Food Science, 53(8), 1257-1267.
Ojeda-Amador, R. M., Salvador, M. D., Fregapane, G., & Gómez-Alonso, S. (2019). Comprehensive study of the phenolic compound profile and antioxidant activity of eight pistachio cultivars and their residual cakes and virgin oils. Journal of agricultural and food chemistry, 67(13), 3583-3594.
109
Oliveira, D., Vidal, L., Ares, G., Walter, E. H., Rosenthal, A., & Deliza, R. (2017). Sensory, microbiological and physicochemical screening of probiotic cultures for the development of non-fermented probiotic milk. LWT-Food Science and Technology, 79, 234-241.
ORHAN, İ. E., Özçelik, B., & ŞENER, B. (2011). Evaluation of antibacterial, antifungal, antiviral, and antioxidant potentials of some edible oils and their fatty acid profiles. Turkish Journal of Biology, 35(2), 251-258.
Özcan, M. M., Ghafoor, K., Al Juhaimi, F., Ahmed, I. A. M., & Babiker, E. E. (2019). Effect of cold-press and soxhlet extraction on fatty acids, tocopherols and sterol contents of the Moringa seed oils. South African Journal of Botany, 124, 333-337.
Pérez-Lamela, C., Franco, I., & Falqué, E. (2021). Impact of High-Pressure Processing on Antioxidant Activity during Storage of Fruits and Fruit Products: A Review. Molecules, 26(17), 5265. Retrieved from https://www.mdpi.com/1420-3049/26/17/5265
Ryan, E., Galvin, K., O'connor, T., Maguire, A., & O'brien, N. (2006). Fatty acid profile, tocopherol, squalene and phytosterol content of brazil, pecan, pine, pistachio and cashew nuts. International journal of food sciences and nutrition, 57(3-4), 219-228.
Sena-Moreno, E., Pardo, J. E., Pardo-Giménez, A., Gómez, R., & Alvarez-Ortí, M. (2016). Differences in oils from nuts extracted by means of two pressure systems. International Journal of Food Properties, 19(12), 2750-2760.
Silveira, S. M. d., Cunha Júnior, A., Scheuermann, G. N., Secchi, F. L., & Vieira, C. R. W. (2012). Chemical composition and antimicrobial activity of essential oils from selected herbs cultivated in the South of
110
Brazil against food spoilage and foodborne pathogens. Ciência Rural, 42, 1300-1306.
Soukoulis, C., Behboudi-Jobbehdar, S., Yonekura, L., Parmenter, C., & Fisk, I. (2014). Impact of milk protein type on the viability and storage stability of microencapsulated Lactobacillus acidophilus NCIMB 701748 using spray drying. Food and bioprocess technology, 7, 1255-1268.
Staffolo, M., Martino, M., & Bevilacqua, A. (2007). Texture and sensory properties of dairy desserts with dietary fibres of different sources. Acta Alimentaria, 36(3), 343-354.
Taribak, C., Casas, L., Mantell, C., Elfadli, Z., Metni, R. E., & Martínez de la Ossa, E. J. (2013). Quality of cosmetic argan oil extracted by supercritical fluid extraction from Argania spinosa L. Journal of Chemistry, 2013(1), 408194.
110
Tsisaryk, O., Musii, L., Dronyk, G., Drach, M., & Slyvka, I. (2022). Development of kefir technology with celery pure. Scientific Messenger of LNU of Veterinary Medicine and Biotechnologies. Series: Food Technologies, 24(98), 57-64.
Turek, K., & Wszołek, M. (2021). Comparative study of walnut and Camelina sativa oil as functional components for the unsaturated fatty acids and conjugated linoleic acid enrichment of kefir. LWT - Food Science and Technology, 147, 111681.
Ullah, H., Hussain, Y., Santarcangelo, C., Baldi, A., Di Minno, A., Khan, H., . . . Daglia, M. (2022). Natural polyphenols for the preservation of meat and dairy products. Molecules, 27(6), 1906.
Yilmaz, B., Elibol, E., Shangpliang, H. N. J., Ozogul, F., & Tamang, J. P. (2022). Microbial communities in home-made and commercial kefir and their hypoglycemic properties. Fermentation, 8(11), 590.
 
 

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