The Effect of Thymus serpyllum L. and Its Preparations on Reduction of L. monocytogenes and S. aureus in Kombucha Fresh Cheese
Abstract
:1. Introduction
2. Materials and Methods
2.1. Herb Material
2.1.1. Manufacturing the Dry Extract
2.1.2. Extraction Using Supercritical Fluid
2.1.3. GC–MS and GC-FID Analysis
2.2. Fresh Cheese Sample Production
2.3. Analysis of Physico-Chemical Characteristics
2.4. Microbiological Analysis
2.5. Total Phenols Content
2.6. Analysis of Statistical Parameters
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Schulz-Collins, D.; Senge, B. Acid- and acid/rennet-curd cheeses part A: Quark, cream cheese and related varieties. In Cheese: Chemistry, Physics and Microbiology; Fox, P.F., McSweeney, P.L.H., Cogan, T.M., Guinee, T.P., Eds.; Academic Press: Cambridge, UK, 2004; pp. 301–328. [Google Scholar]
- Coelho, M.; Silva, C.; Ribeiro, S.; Dapkevicius, M.; Rosa, H. Control of Listeria monocytogenes in fresh cheese using protective lactic acid bacteria. Int. J. Food Microbiol. 2014, 191, 53–59. [Google Scholar] [CrossRef] [PubMed]
- Nikoo, M.; Regenstein, J.M.; Gavlighi, H.A. Antioxidant and Antimicrobial Activities of (-)-Epigallocatechin-3-gallate (EGCG) and its Potential to Preserve the Quality and Safety of Foods. Compr. Rev. Food Sci. Food Saf. 2018, 17, 732–753. [Google Scholar] [CrossRef] [PubMed]
- Bjekić, M.; Iličić, M.; Vukić, V.; Vukić, D.; Kanurić, K.; Pavlić, B.; Zeković, Z.; Popović, L.; Torbica, A.; Tomić, J.; et al. Protein characterisation and antioxidant potential of fresh cheese obtained by kombucha inoculum. Mljekarstvo 2021, 71, 215–225. [Google Scholar] [CrossRef]
- Vukić, V.; Iličić, M.; Vukić, D.; Kocić-Tanackov, S.; Pavlić, B.; Bjekić, M.; Kanurić, K.; Degenek, J.; Zeković, Z. The application of kombucha inoculum as an innovative starter culture in fresh cheese production. LWT Food Sci. Technol. 2021, 151, 112142. [Google Scholar] [CrossRef]
- Dufresne, C.; Farnworth, E. Tea, Kombucha, and health: A review. Food Res. Int. 2000, 33, 409–421. [Google Scholar] [CrossRef]
- Teoh, A.L.; Heard, G.; Cox, J. Yeast ecology of Kombucha fermentation. Int. J. Food Microbiol. 2004, 95, 119–126. [Google Scholar] [CrossRef] [PubMed]
- Vukic, V.; Kanuric, K.; Milanovic, S.; Ilicic, M.; Hrnjez, D.; Ranogajec, M. Correlation of the microstructure with viscosity and textural properties during milk fermentation by kombucha inoculum. Acta Period. Technol. 2014, 45, 89–98. [Google Scholar] [CrossRef]
- Milanovic, S.; Ilicic, M.; Durakovic, K.; Vukic, V. Textural characteristics of fermented milk beverages produced by kombucha. Acta Period. Technol. 2009, 40, 63–69. [Google Scholar] [CrossRef]
- Nyiew, K.; Kwong, P.J.; Yow, Y. An overview of antimicrobial properties of kombucha. Compr. Rev. Food Sci. Food Saf. 2022, 21, 1024–1053. [Google Scholar] [CrossRef] [PubMed]
- Gaggìa, F.; Baffoni, L.; Galiano, M.; Nielsen, D.S.; Jakobsen, R.R.; Castro-Mejía, J.L.; Bosi, S.; Truzzi, F.; Musumeci, F.; Dinelli, G.; et al. Kombucha Beverage from Green, Black and Rooibos Teas: A Comparative Study Looking at Microbiology, Chemistry and Antioxidant Activity. Nutrients 2018, 11, 1. [Google Scholar] [CrossRef] [PubMed]
- Morales, D. Biological activities of kombucha beverages: The need of clinical evidence. Trends Food Sci. Technol. 2020, 105, 323–333. [Google Scholar] [CrossRef]
- Caleja, C.; Ribeiro, A.; Barros, L.; Barreira, J.C.; Antonio, A.L.; Oliveira, M.B.P.; Barreiro, M.F.; Ferreira, I.C. Cottage cheeses functionalized with fennel and chamomile extracts: Comparative performance between free and microencapsulated forms. Food Chem. 2016, 199, 720–726. [Google Scholar] [CrossRef] [PubMed]
- Vukić, D.; Pavlić, B.; Vukić, V.; Iličić, M.; Kanurić, K.; Bjekić, M.; Zeković, Z. Antioxidative capacity of fresh kombucha cheese fortified with sage herbal dust and its preparations. J. Food Sci. Technol. 2021, 59, 2274–2283. [Google Scholar] [CrossRef] [PubMed]
- Mrkonjić, Z.; Rakić, D.; Olgun, E.O.; Canli, O.; Kaplan, M.; Teslić, N.; Zeković, Z.; Pavlić, B. Optimization of antioxidants recovery from wild thyme (Thymus serpyllum L.) by ultrasound-assisted extraction: Multi-response approach. J. Appl. Res. Med. Aromat. Plants 2021, 24, 100333. [Google Scholar] [CrossRef]
- Jarić, S.; Mitrović, M.; Pavlović, P. Review of Ethnobotanical, Phytochemical, and Pharmacological Study of Thymus serpyllum L. Evid.-Based Complement. Altern. Med. 2015, 2015, 101978. [Google Scholar] [CrossRef] [PubMed]
- Mihailovic-Stanojevic, N.; Belščak-Cvitanović, A.; Grujić-Milanović, J.; Ivanov, M.; Jovović, D.; Bugarski, D.; Miloradović, Z. Antioxidant and Antihypertensive Activity of Extract from Thymus serpyllum L. in Experimental Hypertension. Plant Foods Hum. Nutr. 2013, 68, 235–240. [Google Scholar] [CrossRef] [PubMed]
- Rasooli, I.; Mirmostafa, S.A. Antibacterial properties of Thymus pubescens and Thymus serpyllum essential oils. Fitoterapia 2002, 73, 244–250. [Google Scholar] [CrossRef] [PubMed]
- Jovanović, A.A.; Đorđević, V.B.; Zdunić, G.M.; Pljevljakušić, D.S.; Šavikin, K.P.; Gođevac, D.M.; Bugarski, B.M. Optimization of the extraction process of polyphenols from Thymus serpyllum L. herb using maceration, heat- and ultrasound-assisted techniques. Sep. Purif. Technol. 2017, 179, 369–380. [Google Scholar] [CrossRef]
- Ančarević, A.; Bugarski, B.; Šavikin, K.; Zdunić, G. Biological activity and ethnomedicinal use of Thymus vulgaris and Thymus serpyllum. Lek. Sirovine 2013, 33, 3–17. Available online: http://TechnoRep.tmf.bg.ac.rs/handle/123456789/2297 (accessed on 18 April 2024.).
- Ducková, V.; Kročko, M.; Kňazovická, V.; Čanigová, M. Evaluation of Yoghurts with Thyme, Thyme Essential Oil and Salt. Acta Univ. Agric. et Silvic. Mendel. Brun. 2018, 66, 365–369. [Google Scholar] [CrossRef]
- Bukvicki, D.; Giweli, A.; Stojkovic, D.; Vujisic, L.; Tesevic, V.; Nikolic, M.; Sokovic, M.; Marin, P.D. Short communication: Cheese supplemented with Thymus algeriensis oil, a potential natural food preservative. J. Dairy Sci. 2018, 101, 3859–3865. [Google Scholar] [CrossRef] [PubMed]
- Gil, K.A.; Jerković, I.; Marijanović, Z.; Manca, M.L.; Caddeo, C.; Tuberoso, C.I.G. Evaluation of an innovative sheep cheese with antioxidant activity enriched with different thyme essential oil lecithin liposomes. LWT Food Sci. Technol. 2022, 154, 112808. [Google Scholar] [CrossRef]
- Ahmed, L.I.; Ibrahim, N.; Abdel-Salam, A.B.; Fahim, K.M. Potential application of ginger, clove and thyme essential oils to improve soft cheese microbial safety and sensory characteristics. Food Biosci. 2021, 42, 101177. [Google Scholar] [CrossRef]
- Bleoancă, I.; Saje, K.; Mihalcea, L.; Oniciuc, E.-A.; Smole-Mozina, S.; Nicolau, A.I.; Borda, D. Contribution of high pressure and thyme extract to control Listeria monocytogenes in fresh cheese—A hurdle approach. Innov. Food Sci. Emerg. Technol. Part A 2016, 38, 7–14. [Google Scholar] [CrossRef]
- Degenek, J.; Kanurić, K.; Iličić, M.; Vukić, D.; Mrkonjić, Z.; Pavlić, B.; Zeković, Z.; Vukić, V. Fortification of fresh kombucha cheese with wild thyme (Thymus serpyllum L.) herbal dust and its influence on antioxidant activity. Food Biosci. 2023, 56, 103161. [Google Scholar] [CrossRef]
- Pavlić, B.; Teslić, N.; Vidaković, A.; Vidović, S.; Velićanski, A.; Versari, A.; Radosavljević, R.; Zeković, Z. Sage processing from by-product to high quality powder: I. Bioactive potential. Ind. Crop. Prod. 2017, 107, 81–89. [Google Scholar] [CrossRef]
- Šojić, B.; Ikonić, P.; Kocić-Tanackov, S.; Peulić, T.; Teslić, N.; Županjac, M.; Lončarević, I.; Zeković, Z.; Popović, M.; Vidaković, S.; et al. Antibacterial Activity of Selected Essential Oils against Foodborne Pathogens and Their Application in Fresh Turkey Sausages. Antibiotics 2023, 12, 182. [Google Scholar] [CrossRef] [PubMed]
- Malbasa, R.; Loncar, E.; Milanovic, S.; Kolarov, L. Use of milk-based kombucha inoculum for milk fermentation. Acta Period. Technol. 2009, 40, 47–52. [Google Scholar] [CrossRef]
- Kanurić, K.G.; Hrnjez, D.V.; Ranogajec, M.I.; Milanović, S.D.; Iličić, M.D.; Vukić, V.R.; Milanović, M.L. The effect of fermentation temperature on the functional dairy product quality. Acta Period. Technol. 2011, 42, 63–70. [Google Scholar] [CrossRef]
- Vukić, V.; Vukić, D.; Pavlić, B.; Iličić, M.; Kocić-Tanackov, S.; Kanurić, K.; Bjekić, M.; Zeković, Z. Antimicrobial potential of kombucha fresh cheese with the addition of sage (Salvia officinalis L.) and its preparations. Food Funct. 2023, 14, 3348–3356. [Google Scholar] [CrossRef] [PubMed]
- Kähkönen, M.P.; Hopia, A.I.; Vuorela, H.J.; Rauha, J.-P.; Pihlaja, K.; Kujala, T.S.; Heinonen, M. Antioxidant Activity of Plant Extracts Containing Phenolic Compounds. J. Agric. Food Chem. 1999, 47, 3954–3962. [Google Scholar] [CrossRef] [PubMed]
- Derringer, G.; Suich, R. Simultaneous Optimization of Several Response Variables. J. Qual. Technol. 1980, 12, 214–219. [Google Scholar] [CrossRef]
- Cardoso, R.R.; Neto, R.O.; Dos Santos D’Almeida, C.T.; Nascimento, T.; Pressete, C.G.; Azevedo, L.; Martino, H.S.D.; Cameron, L.C.; Ferreira, M.S.L.; de Barros, F.A.R. Kombuchas from green and black teas have different phenolic profile, which impacts their antioxidant capacities, antibacterial and antiproliferative activities. Food Res. Int. 2020, 128, 108782. [Google Scholar] [CrossRef] [PubMed]
- Bouarab-Chibane, L.; Forquet, V.; Lantéri, P.; Clément, Y.; Léonard-Akkari, L.; Oulahal, N.; Degraeve, P.; Bordes, C. Antibacterial Properties of Polyphenols: Characterization and QSAR (Quantitative Structure–Activity Relationship) Models. Front. Microbiol. 2019, 10, 829. [Google Scholar] [CrossRef] [PubMed]
- Cueva, C.; Moreno-Arribas, M.V.; Martín-Álvarez, P.J.; Bills, G.; Vicente, M.F.; Basilio, A.; Rivas, C.L.; Requena, T.; Rodríguez, J.M.; Bartolomé, B. Antimicrobial activity of phenolic acids against commensal, probiotic and pathogenic bacteria. Res. Microbiol. 2010, 161, 372–382. [Google Scholar] [CrossRef] [PubMed]
- Velićanski, A.S.; Cvetković, D.D.; Šaponjac, V.T.T.; Vulić, J.J. Antioxidant and Antibacterial Activity of the Beverage Obtained by Fermentation of Sweetened Lemon Balm (Melissa officinalis L.) Tea with Symbiotic Consortium of Bacteria and Yeasts. Food Technol. Biotechnol. 2014, 52, 420–429. [Google Scholar] [CrossRef] [PubMed]
- Özyurt, H. Changes in the content of total polyphenols and the antioxidant activity of different beverages obtained by Kombucha ‘tea fungus’. Int. J. Agric. Environ. Food Sci. 2020, 4, 255–261. [Google Scholar] [CrossRef]
- Nikolić, M.; Glamočlija, J.; Ferreira, I.C.F.R.; Calhelha, R.C.; Fernandes, Â.; Marković, T.; Marković, D.; Giweli, A.; Soković, M. Chemical composition, antimicrobial, antioxidant and antitumor activity of Thymus serpyllum L., Thymus algeriensis Boiss. and Reut and Thymus vulgaris L. essential oils. Ind. Crops Prod. 2014, 52, 183–190. [Google Scholar] [CrossRef]
- Šojić, B.; Tomović, V.; Kocić-Tanackov, S.; Kovačević, D.B.; Putnik, P.; Mrkonjić, Ž.; Đurović, S.; Jokanović, M.; Ivić, M.; Škaljac, S.; et al. Supercritical extracts of wild thyme (Thymus serpyllum L.) by-product as natural antioxidants in ground pork patties. LWT Food Sci. Technol. 2020, 130, 109661. [Google Scholar] [CrossRef]
- Li, L.; Shi, C.; Yin, Z.; Jia, R.; Peng, L.; Kang, S.; Li, Z. Antibacterial activity of α-terpineol may induce morphostructural alterations in Escherichia coli. Braz. J. Microbiol. 2014, 45, 1409–1413. [Google Scholar] [CrossRef] [PubMed]
- Magi, G.; Marini, E.; Facinelli, B. Antimicrobial activity of essential oils and carvacrol, and synergy of carvacrol and erythromycin, against clinical, erythromycin-resistant Group A Streptococci. Front. Microbiol. 2015, 6, 165. [Google Scholar] [CrossRef] [PubMed]
- Marchese, A.; Orhan, I.E.; Daglia, M.; Barbieri, R.; Di Lorenzo, A.; Gortzi, O.; Izadi, M.; Nabavi, S.M. Antibacterial and antifungal activities of thymol: A brief review of the literature. Food Chem. 2016, 210, 402–414. [Google Scholar] [CrossRef] [PubMed]
- Lou, Z.; Wang, H.; Rao, S.; Sun, J.; Ma, C.; Li, J. p-Coumaric acid kills bacteria through dual damage mechanisms. Food Control. 2012, 25, 550–554. [Google Scholar] [CrossRef]
- Nguyen, T.L.A.; Bhattacharya, D. Antimicrobial Activity of Quercetin: An Approach to Its Mechanistic Principle. Molecules 2022, 27, 2494. [Google Scholar] [CrossRef] [PubMed]
- Qian, W.; Liu, M.; Fu, Y.; Zhang, J.; Liu, W.; Li, J.; Li, X.; Li, Y.; Wang, T. Antimicrobial mechanism of luteolin against Staphylococcus aureus and Listeria monocytogenes and its antibiofilm properties. Microb. Pathog. 2020, 142, 104056. [Google Scholar] [CrossRef] [PubMed]
Sample | Form of Wild Thyme | Concentration (g/100 g) |
---|---|---|
Kombucha G | Ground | 2.1 |
Kombucha DE | Dry extract | 0.62 |
Kombucha SFE | Supercritical fluid extract | 0.025 |
Day of Storage | Kombucha C | Kombucha G | Kombucha DE | Kombucha SFE | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
MAB | L. monocytogenes | S. aureus | MAB | L. monocytogenes | S. aureus | MAB | L. monocytogenes | S. aureus | MAB | L. monocytogenes | S. aureus | |
0 | 9.0 *a ± 0.2 | 3.8 a ± 0.1 | 4.1 a ± 0.0 | 9.0 a ± 0.0 | 4.0 a ± 0.1 | 4.0 a ± 0.1 | 8.8 a ± 0.4 | 3.6 a ± 0.0 | 3.7 a ± 0.2 | 8.9 a ± 0.0 | 4.1 a ± 0.2 | 4.2 a ± 0.0 |
10 | 8.7 b ± 0.0 | 3.4 b ± 0.1 | 3.4 b ± 0.0 | 8.8 a ± 0.2 | 3.5 b ± 0.1 | 3.8 a ± 0.1 | 8.9 a ± 0.1 | 3.6 ab ± 0.0 | 3.7 a ± 0.1 | 8.7 b ± 0.1 | 3.7 b ± 0.0 | 3.9 ab ± 0.0 |
20 | 8.4 b ± 0.1 | 3.2 b ± 0.0 | 3.2 c ± 0.0 | 8.8 a ± 0.1 | 3.1 c ± 0.2 | 3.2 b ± 0.0 | 8.7 a ± 0.1 | 3.5 b ± 0.1 | 3.5 a ± 0.0 | 8.8 ab ± 0.0 | 3.5 bc ± 0.1 | 3.5 b ± 0.3 |
30 | 8.6 b ± 0.0 | 3.2 b ± 0.2 | 3.2 c ± 0.0 | 8.6 a ± 0.0 | 2.3 d ± 0.0 | 2.7 c ± 0.2 | 8.7 a ± 0.1 | 2.8 c ± 0.0 | 2.9 b ± 0.1 | 8.8 ab ± 0.0 | 3.3 c ± 0.1 | 3.5 b ± 0.2 |
Sample | TP [g GAE/100 g] | DPPH [mM TE/g] | FRAP [mM Fe2+/g] | ABTS [mM TE/g] |
---|---|---|---|---|
UAE * | 4.39 ± 0.1043 | 0.25 ± 0.0021 | 0.77 ± 0.0210 | 0.52 ± 0.0095 |
Dry extract | 2.05 ± 0.0589 | 0.94 ± 0.0103 | 4.56 ± 0.0492 | 5.53 ± 0.0566 |
Wilks’ Lambda | F | Effect DF | Error DF | p | |
---|---|---|---|---|---|
Thyme addition | 0.00007 | 48053.5796 | 4 | 13 | 0.0000 |
Day of storage | 0.05065 | 6.03434925 | 12 | 34.6862697 | 0.00001 |
Sample * Day of storage | 0.012596 | 12.2108378 | 12 | 34.6862697 | 0.0000 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Vukić, V.; Degenek, J.; Kanurić, K.; Vukić, D.; Pavlić, B.; Iličić, M.; Kocić-Tanackov, S.; Mrkonjić, Ž.; Bulut, S.; Zeković, Z. The Effect of Thymus serpyllum L. and Its Preparations on Reduction of L. monocytogenes and S. aureus in Kombucha Fresh Cheese. Processes 2024, 12, 1187. https://doi.org/10.3390/pr12061187
Vukić V, Degenek J, Kanurić K, Vukić D, Pavlić B, Iličić M, Kocić-Tanackov S, Mrkonjić Ž, Bulut S, Zeković Z. The Effect of Thymus serpyllum L. and Its Preparations on Reduction of L. monocytogenes and S. aureus in Kombucha Fresh Cheese. Processes. 2024; 12(6):1187. https://doi.org/10.3390/pr12061187
Chicago/Turabian StyleVukić, Vladimir, Jovana Degenek, Katarina Kanurić, Dajana Vukić, Branimir Pavlić, Mirela Iličić, Sunčica Kocić-Tanackov, Živan Mrkonjić, Sandra Bulut, and Zoran Zeković. 2024. "The Effect of Thymus serpyllum L. and Its Preparations on Reduction of L. monocytogenes and S. aureus in Kombucha Fresh Cheese" Processes 12, no. 6: 1187. https://doi.org/10.3390/pr12061187
APA StyleVukić, V., Degenek, J., Kanurić, K., Vukić, D., Pavlić, B., Iličić, M., Kocić-Tanackov, S., Mrkonjić, Ž., Bulut, S., & Zeković, Z. (2024). The Effect of Thymus serpyllum L. and Its Preparations on Reduction of L. monocytogenes and S. aureus in Kombucha Fresh Cheese. Processes, 12(6), 1187. https://doi.org/10.3390/pr12061187