Kombucha Beverage: Comparative Study Based on Bioactive Properties and Antimicrobial Potentials of Different Plant Infusion

Abstract

Kombucha, a fermented beverage, is popular for its prophylactic and therapeutic properties. Kombucha is a traditionally black tea infusion fermented with a symbiotic bacteria and yeast consortium (SCOBY) under aerobic conditions for 7-21 days. However, the beneficial properties of kombucha vary according to the substrate kind, fermentation conditions, and SCOBY consortium. The present study has screened the physicochemical, bioactive, antimicrobial, and sensory properties of beverages produced by fermenting black, green, rosehip, and licorice tea infusions with kombucha starter culture for 21 days. Tea infusions before and after fermentation; pH value, titratable acidity (TA), pellicle weight, color values (L*, a*, b*, ΔE), total phenolic content (TPC), antioxidant capacity against DPPH (2,2-diphenyl-1- picrylhydrazil) radicals, and antimicrobial activity was measured. Antimicrobial activity is applied to various foodborne pathogens such as Escherichia coli (E. coli), Staphylococcus aureus (S. aureus), and C. albicans with based disc diffusion method and spectrophotometric technique. In this study, tea type statistically affected all parameters except pH in kombucha beverages (p<0.05). The highest TPC and antioxidant activity were determined in the green tea kombucha sample. All kombucha beverages, especially those prepared by fermentation of licorice and green tea infusions, showed the highest antimicrobial potential against E. coli and S. aureus, respectively. Consequently, it is vital to prefer kombucha fermented with SCOBY instead of consuming beverages prepared with various plants' infusions to increase many beneficial properties and provide additional benefits.

Keywords

• Antimicrobial activity
• Bioactive potential
• Fermented beverage
• Kombucha
• SCOBY

References

1. AOAC. (2002). Official Methods of Analysis of AOAC International, 17th ed. Methods 976.05, 923.03, 962.09, 920.39. USA: Association of Official Analytical Chemists
2. AOAC. (1975). Association of Official Analytical Chemists. Official Methods of analysis. In Methods in Enzymology (Vol. 299, pp. 152–178). Academic Press. https://doi.org/10.1016/S0076-6879(99)99017-1
3. Azeredo, H. M. C., Barud, H., Farinas, C. S., Vasconcellos, V. M., & Claro, A. M. (2019). Bacterial Cellulose as a Raw Material for Food and Food Packaging Applications. Frontiers in Sustainable Food Systems, 3, 7. https://doi.org/10.3389/FSUFS.2019.00007/BIBTEX
4. Battikh, H., Chaieb, K., Bakhrouf, A., & Ammar, E. (2013). Antibacterial and antifungal activities of black and green kombucha teas. Journal of Food Biochemistry, 37(2), 231–236. https://doi.org/10.1111/j.1745-4514.2011.00629.x
5. Bhattacharya, S., Gachhui, R., & Sil, P. C. (2013). Effect of Kombucha, a fermented black tea in attenuating oxidative stress mediated tissue damage in alloxan induced diabetic rats. Food and Chemical Toxicology, 60, 328–340. https://doi.org/10.1016/J.FCT.2013.07.051
6. Brand-Williams, W., Cuvelier, M. E., & Berset, C. (1995). Use of a free radical method to evaluate antioxidant activity. LWT - Food Science and Technology, 28(1), 25–30. https://doi.org/10.1016/S0023-6438(95)80008-5
7. Cardoso, R. R., Neto, R. O., dos Santos D’Almeida, C. T., do Nascimento, T. P., Pressete, C. G., Azevedo, L., Martino, H. S. D., Cameron, L. C., Ferreira, M. S. L., & Barros, F. A. R. de. (2020). Kombuchas from green and black teas have different phenolic profile, which impacts their antioxidant capacities, antibacterial and antiproliferative activities. Food Research International, 128, 108782. https://doi.org/10.1016/J.FOODRES.2019.108782
8. Chakravorty, S., Bhattacharya, S., Chatzinotas, A., Chakraborty, W., Bhattacharya, D., & Gachhui, R. (2016). Kombucha tea fermentation: Microbial and biochemical dynamics. International Journal of Food Microbiology, 220, 63–72. https://doi.org/10.1016/J.IJFOODMICRO.2015.12.015

9. Chiu, C. T., Lai, C. H., Huang, Y. H., Yang, C. H., & Lin, J. N. (2021). Comparative analysis of gradient diffusion and disk diffusion with agar dilution for susceptibility testing of Elizabethkingia anophelis. Antibiotics, 10(4), 450. https://doi.org/10.3390/antibiotics10040450
10. Chrubasik, C., Roufogalis, B. D., Müller-Ladner, U., & Chrubasik, S. (2008). A systematic review on the Rosa canina effect and efficacy profiles. Phytotherapy Research, 22(6), 725–733. https://doi.org/10.1002/PTR.2400
11. Chu, S. C., & Chen, C. (2006). Effects of origins and fermentation time on the antioxidant activities of kombucha. Food Chemistry, 98(3), 502–507. https://doi.org/10.1016/J.FOODCHEM.2005.05.080
12. Corbo, M. R., Bevilacqua, A., Petruzzi, L., Casanova, F. P., & Sinigaglia, M. (2014). Functional Beverages: The Emerging Side of Functional Foods: Commercial Trends, Research, and Health Implications. Comprehensive Reviews in Food Science and Food Safety, 13(6), 1192–1206. https://doi.org/10.1111/1541-4337.12109
13. Coton, M., Pawtowski, A., Taminiau, B., Burgaud, G., Deniel, F., Coulloumme-Labarthe, L., Fall, A., Daube, G., & Coton, E. (2017). Unraveling microbial ecology of industrial-scale Kombucha fermentations by metabarcoding and culture-based methods. FEMS Microbiology Ecology, 93(5). https://doi.org/10.1093/FEMSEC/FIX048
14. Cottet, C., Ramirez-Tapias, Y. A., Delgado, J. F., la Osa, O. De, Salvay, A. G., & Peltzer, M. A. (2020). Biobased Materials from Microbial Biomass and Its Derivatives. Materials 2020, Vol. 13, Page 1263, 13(6), 1263. https://doi.org/10.3390/MA13061263
15. De Roos, J., & De Vuyst, L. (2018). Acetic acid bacteria in fermented foods and beverages. Current Opinion in Biotechnology, 49, 115–119. https://doi.org/10.1016/j.copbio.2017.08.007
16. Demir, N., Yildiz, O., Alpaslan, M., & Hayaloglu, A. A. (2014). Evaluation of volatiles, phenolic compounds and antioxidant activities of rose hip (Rosa L.) fruits in Turkey. LWT - Food Science and Technology, 57(1), 126–133. https://doi.org/10.1016/j.lwt.2013.12.038
17. Dufresne, C., & Farnworth, E. (2000). Tea, Kombucha, and health: A review. Food Research International, 33(6), 409–421. https://doi.org/10.1016/S0963-9969(00)00067-3
18. Emiljanowicz, K. E., & Malinowska-Pańczyk, E. (2020). Kombucha from alternative raw materials–The review. In Critical Reviews in Food Science and Nutrition (Vol. 60, Issue 19, pp. 3185–3194). Taylor & Francis. https://doi.org/10.1080/10408398.2019.1679714
19. Fujii, S., Morinaga, O., Uto, T., Nomura, S., & Shoyama, Y. (2014). Development of a monoclonal antibody-based immunochemical assay for liquiritin and its application to the quality control of licorice products. Journal of Agricultural and Food Chemistry, 62(15), 3377–3383. https://doi.org/10.1021/JF404731Z/ASSET/IMAGES/JF404731Z.SOCIAL.JPEG_V03
20. Gaggìa, F., Baffoni, L., Galiano, M., Nielsen, D. S., Jakobsen, R. R., Castro-Mejía, J. L., Bosi, S., Truzzi, F., Musumeci, F., Dinelli, G., & Di Gioia, D. (2018). Kombucha Beverage from Green, Black and Rooibos Teas: A Comparative Study Looking at Microbiology, Chemistry and Antioxidant Activity. Nutrients 2019, Vol. 11, Page 1, 11(1), 1. https://doi.org/10.3390/NU11010001
21. Greenwalt, C. J., Ledford, R. A., & Steinkraus, K. H. (1998). Determination and characterization of the antimicrobial activity of the fermented tea Kombucha. LWT - Food Science and Technology, 31(3), 291–296. https://doi.org/10.1006/fstl.1997.0354
22. Jakubczyk, K., Kałduńska, J., Kochman, J., & Janda, K. (2020). Chemical Profile and Antioxidant Activity of the Kombucha Beverage Derived from White, Green, Black and Red Tea. Antioxidants 2020, Vol. 9, Page 447, 9(5), 447. https://doi.org/10.3390/ANTIOX9050447
23. Jayabalan, R., Marimuthu, S., & Swaminathan, K. (2007a). Changes in content of organic acids and tea polyphenols during kombucha tea fermentation. Food Chemistry, 102(1), 392–398. https://doi.org/10.1016/J.FOODCHEM.2006.05.032
24. Jayabalan, R., Marimuthu, S., & Swaminathan, K. (2007b). Changes in content of organic acids and tea polyphenols during kombucha tea fermentation. Food Chemistry, 102(1), 392–398. https://doi.org/10.1016/j.foodchem.2006.05.032
25. Jayabalan, Rasu, Chen, P.-N., Hsieh, Y.-S., Prabhakaran, K., Pitchai, P., Marimuthu, S., Thangaraj, P., Swaminathan, K., & Eok Yun, S. (2011). Effect of solvent fractions of kombucha tea on viability and invasiveness of cancer cells-Characterization of dimethyl 2-(2-hydroxy-2-methoxypropylidine) malonate and vitexin. Indian Journal of Biotechnology, 10, 75–82.
26. Jayabalan, Rasu, Malbaša, R. V., Lončar, E. S., Vitas, J. S., & Sathishkumar, M. (2014). A review on kombucha tea-microbiology, composition, fermentation, beneficial effects, toxicity, and tea fungus. In Comprehensive Reviews in Food Science and Food Safety (Vol. 13, Issue 4, pp. 538–550). John Wiley & Sons, Ltd. https://doi.org/10.1111/1541-4337.12073
27. Kamal, D. A. M., Salamt, N., Zaid, S. S. M., & Mokhtar, M. H. (2021). Beneficial effects of green tea catechins on female reproductive disorders: A review. Molecules, 26(9), 2675. https://doi.org/10.3390/molecules26092675
28. Khan, N., & Mukhtar, H. (2019). Tea polyphenols in promotion of human health. In Nutrients (Vol. 11, Issue 1, p. 39). Multidisciplinary Digital Publishing Institute. https://doi.org/10.3390/nu11010039
29. Kim, J., & Adhikari, K. (2020). Current trends in kombucha: Marketing perspectives and the need for improved sensory research. In Beverages (Vol. 6, Issue 1, pp. 1–19). Multidisciplinary Digital Publishing Institute. https://doi.org/10.3390/beverages6010015
30. Liu, C. H., Hsu, W. H., Lee, F. L., & Liao, C. C. (1996). The isolation and identification of microbes from a fermented tea beverage, Haipao, and their interactions during Haipao fermentation. Food Microbiology, 13(6), 407–415. https://doi.org/10.1006/FMIC.1996.0047
31. Marsh, A. J., O’Sullivan, O., Hill, C., Ross, R. P., & Cotter, P. D. (2014). Sequence-based analysis of the bacterial and fungal compositions of multiple kombucha (tea fungus) samples. Food Microbiology, 38, 171–178. https://doi.org/10.1016/j.fm.2013.09.003
32. Massoud, R., Jafari-Dastjerdeh, R., Naghavi, N., & Khosravi-Darani, K. (2022). All aspects of antioxidant properties of kombucha drink. In Biointerface Research in Applied Chemistry (Vol. 12, Issue 3, pp. 4018–4027). https://doi.org/10.33263/BRIAC123.40184027
33. Maughan, C., Tansawat, R., Cornforth, D., Ward, R., & Martini, S. (2012). Development of a beef flavor lexicon and its application to compare the flavor profile and consumer acceptance of rib steaks from grass- or grain-fed cattle. Meat Science, 90(1), 116–121. https://doi.org/10.1016/J.MEATSCI.2011.06.006
34. May, A., Narayanan, S., Alcock, J., Varsani, A., Maley, C., & Aktipis, A. (2019). Kombucha: A novel model system for cooperation and conflict in a complex multi-species microbial ecosystem. PeerJ, 2019(9), e7565. https://doi.org/10.7717/peerj.7565
35. Medveckiene, B., Kulaitiene, J., Jariene, E., Vaitkevičiene, N., & Hallman, E. (2020). Carotenoids, polyphenols, and ascorbic acid in organic rosehips (Rosa spp.) cultivated in Lithuania. Applied Sciences (Switzerland), 10(15), 5337. https://doi.org/10.3390/APP10155337
36. Miranda, B., Lawton, N. M., Tachibana, S. R., Swartz, N. A., & Hall, W. P. (2016). Titration and HPLC Characterization of Kombucha Fermentation: A Laboratory Experiment in Food Analysis. Journal of Chemical Education, 93(10), 1770–1775. https://doi.org/10.1021/ACS.JCHEMED.6B00329/ASSET/IMAGES/ACS.JCHEMED.6B00329.SOCIAL.JPEG_V03
37. Mukadam, T. A., Punjabi, K., Deshpande, S. D., Vaidya, S. P., & Chowdhary, A. S. (2016). Isolation and Characterization of Bacteria and Yeast from Kombucha Tea. International Journal of Current Microbiology and Applied Sciences, 5(6), 32–41. https://doi.org/10.20546/ijcmas.2016.506.004
38. Oh, J., Jo, H., Cho, A. R., Kim, S. J., & Han, J. (2013). Antioxidant and antimicrobial activities of various leafy herbal teas. Food Control, 31(2), 403–409. https://doi.org/10.1016/J.FOODCONT.2012.10.021
39. Poveda-Castillo, G. D. C., Rodrigo, D., Martínez, A., & Pina-Pérez, M. C. (2018). Bioactivity of Fucoidan as an antimicrobial agent in a new functional beverage. Beverages, 4(3), 64. https://doi.org/10.3390/beverages4030064
40. Ramaswamy, H. S., & Richards, J. F. (1980). A Reflectance Method to Study the Green-Yellow Changes in Fruits and Vegetables. Canadian Institute of Food Science and Technology Journal, 13(3), 107–111. https://doi.org/10.1016/s0315-5463(80)73346-1
41. Ramírez Tapias, Y. A., Peltzer, M. A., Delgado, J. F., & Salvay, A. G. (2020). Kombucha Tea By-product as Source of Novel Materials: Formulation and Characterization of Films. Food and Bioprocess Technology, 13(7), 1166–1180. https://doi.org/10.1007/S11947-020-02471-4/FIGURES/8
42. Record, I. R., & Lane, J. M. (2001). Simulated intestinal digestion of green and black teas. Food Chemistry, 73(4), 481–486. https://doi.org/10.1016/S0308-8146(01)00131-5
43. Rojo-Poveda, O., Barbosa-Pereira, L., Mateus-Reguengo, L., Bertolino, M., Stévigny, C., & Zeppa, G. (2019). Effects of particle size and extraction methods on cocoa bean shell functional beverage. Nutrients, 11(4), 867. https://doi.org/10.3390/nu11040867
44. Sethi, S., Tyagi, S. K., & Anurag, R. K. (2016). Plant-based milk alternatives an emerging segment of functional beverages: a review. Journal of Food Science and Technology, 53(9), 3408–3423. https://doi.org/10.1007/S13197-016-2328-3/FIGURES/4
45. Sharma, O. P., & Bhat, T. K. (2009). DPPH antioxidant assay revisited. Food Chemistry, 113(4), 1202–1205. https://doi.org/10.1016/j.foodchem.2008.08.008
46. Silva, K. A., Uekane, T. M., Miranda, J. F. de, Ruiz, L. F., Motta, J. C. B. da, Silva, C. B., Pitangui, N. de S., Gonzalez, A. G. M., Fernandes, F. F., & Lima, A. R. (2021). Kombucha beverage from non-conventional edible plant infusion and green tea: Characterization, toxicity, antioxidant activities and antimicrobial properties. Biocatalysis and Agricultural Biotechnology, 34, 102032. https://doi.org/10.1016/J.BCAB.2021.102032
47. Sreeramulu, G., Zhu, Y., & Knol, W. (2001). Characterization of antimicrobial activity in Kombucha fermentation. Acta Biotechnologica, 21(1), 49–56. https://doi.org/10.1002/1521-3846(200102)21:1<49::AID-ABIO49>3.0.CO;2-G
48. Sun-Waterhouse, D. (2011). The development of fruit-based functional foods targeting the health and wellness market: A review. International Journal of Food Science and Technology, 46(5), 899–920. https://doi.org/10.1111/j.1365-2621.2010.02499.x
49. Sun, T. Y., Li, J. S., & Chen, C. (2015). Effects of blending wheatgrass juice on enhancing phenolic compounds and antioxidant activities of traditional kombucha beverage. Journal of Food and Drug Analysis, 23(4), 709–718. https://doi.org/10.1016/J.JFDA.2015.01.009
50. Torán-Pereg, P., del Noval, B., Valenzuela, S., Martinez, J., Prado, D., Perisé, R., & Arboleya, J. C. (2021). Microbiological and sensory characterization of kombucha SCOBY for culinary applications. International Journal of Gastronomy and Food Science, 23, 100314. https://doi.org/10.1016/j.ijgfs.2021.100314
51. Velićanski, A. S., Cvetković, D. D., Markov, S. L., Tumbas Šaponjac, V. T., & Vulić, J. J. (2014). Antioxidant and Antibacterial Activity of the Beverage Obtained by Fermentation of Sweetened Lemon Balm (Melissa offi cinalis L.) Tea with Symbiotic Consortium of Bacteria and Yeasts. Food Technology and Biotechnology, 52(4), 420–429. https://doi.org/10.17113/FTB.52.04.14.3611
52. Villarreal-Soto, S. A., Beaufort, S., Bouajila, J., Souchard, J. P., Renard, T., Rollan, S., & Taillandier, P. (2019). Impact of fermentation conditions on the production of bioactive compounds with anticancer, anti-inflammatory and antioxidant properties in kombucha tea extracts. Process Biochemistry, 83, 44–54. https://doi.org/10.1016/J.PROCBIO.2019.05.004
53. Villarreal-Soto, S. A., Beaufort, S., Bouajila, J., Souchard, J. P., & Taillandier, P. (2018). Understanding Kombucha Tea Fermentation: A Review. Journal of Food Science, 83(3), 580–588. https://doi.org/10.1111/1750-3841.14068
54. Villarreal-Soto, S. A., Bouajila, J., Pace, M., Leech, J., Cotter, P. D., Souchard, J. P., Taillandier, P., & Beaufort, S. (2020). Metabolome-microbiome signatures in the fermented beverage, Kombucha. International Journal of Food Microbiology, 333, 108778. https://doi.org/10.1016/J.IJFOODMICRO.2020.108778
55. Vitas, J., Vukmanović, S., Čakarević, J., Popović, L., & Malbaša, R. (2020). Kombucha fermentation of six medicinal herbs: Chemical profile and biological activity. Chemical Industry and Chemical Engineering Quarterly, 26(2), 157–170. https://doi.org/10.2298/CICEQ190708034V
56. Wang, Z., Zhao, X., Zu, Y., Wu, W., Li, Y., Guo, Z., Wang, L., & Wang, L. (2019). Licorice flavonoids nanoparticles prepared by liquid antisolvent re-crystallization exhibit higher oral bioavailability and antioxidant activity in rat. Journal of Functional Foods, 57, 190–201. https://doi.org/10.1016/J.JFF.2019.04.010
57. Watawana, M. I., Jayawardena, N., & Waisundara, V. Y. (2018). Value-added tea (Camellia sinesis) as a functional food using the Kombucha ‘tea fungus.’ Chiang Mai Journal of Science, 45(1), 136–146. http://epg.science.cmu.ac.th/ejournal/
58. Yang, F., Chu, T., Zhang, Y., Liu, X., Sun, G., & Chen, Z. (2020). Quality assessment of licorice (Glycyrrhiza glabra L.) from different sources by multiple fingerprint profiles combined with quantitative analysis, antioxidant activity and chemometric methods. Food Chemistry, 324, 126854. https://doi.org/10.1016/j.foodchem.2020.126854