Investigation of antibacterial activity of heated Kombucha beverages prepared with several herbal teas using response surface methodology

مجله پژوهشهای علوم و صنایع غذایی ایران

Volume 17, Issue 6 - Serial Number 72, January and February 2022, Pages 121-136   

Document Type: Research Article-en

DOI: 10.22067/ifstrj.2021.71497.1071

Authors

Fateme Valiyan¹; Hadi Koohsari^{* 2}; Abolfazl Fadavi³

¹Graduated student, Department of Food Science and Technology, Azadshahr branch, Islamic Azad University, Azadshahr, Golestan, Iran

²Department of Microbiology, Azadshahr Branch, Islamic Azad University, Azadshahr, Golestan, Iran

³Department of Food Science and Technology, Azadshahr Branch, Islamic Azad University, Azadshahr, Golestan, Iran

Abstract

The composition and biological activities of kombucha beverage depends on type of herbal tea, concentration of sucrose and the fermentation time. This study aimed to investigate the effect of different preparation conditions on antibacterial activity of heated kombucha beverages by Response Surface Methodology (RSM). Four types of herbal teas, including black tea, green tea, lemon verbena and peppermint were prepared with three concentrations of sucrose (2, 5 and 8%) and inoculated with active kombucha culture. After 7, 14 and 21 days, beverages were heated by autoclaving and their antibacterial activity against four bacteria including Escherichia coli, Shigella dysenteriae, Staphylococcus aureus and Bacillus cereus was evaluated by well method. The RSM was used to investigate the effect of sucrose concentration, fermentation time and type of herbal tea on antibacterial activity of heated beverages. Increasing sucrose concentration had significant effect (P<0.0001) on antibacterial activity of heated beverages against all tested bacteria. Increasing of fermentation time had significant effect (P< 0.0001) on antibacterial activity of heated beverages against E. coli and S. dysenteriae. Type of herbal tea had significant effect on antibacterial activity against S. aureus and S. dysenteriae. The highest antibacterial activity against E. coli and S. dysenteriae was observed in beverages prepared with lemon verbena. Beverages prepared with green tea showed highest antibacterial activity against S. aureus. The highest antibacterial activity against B. cereus was observed in heated beverages prepared with black tea and peppermint. In general, the results showed significant antibacterial activity of heated kombucha beverages against the tested bacteria.

Keywords

Antimicrobial effect; Fermented beverage; Fermentation conditions; Sucrose concentration; Fermentation time

References

An, B.J., Kwak, J.H., & Son, J.H. 2004. Biological and anti-microbial activity of irradiated green tea polyphenols. Food Chemistry, 88, 549– 555.

Atiyeh, H., & Duvnjak, Z. 2003. Production of fructose and ethanol from sugar beet using Saccharomyces cerevisiae ATCC 36858. Biotechnology Progress, 18, 234- 239.

Battikh, H., Bakhrouf, A., & Ammarb, E. 2012. Antimicrobial effect of Kombucha analogues. Food Science and Technology, 47, 71- 77.

Battikh, H., Chaieb, K., Bakhruf, A., & Ammar, E. 2011. Antibacterial and antifungal activities of black and green kompucha teas. Journal of Food Biochemistry, 37, 231- 236.

Bilia, A.R., Giomi, M., Innocenti, M., Gallori, S., & Vincieri, F.F. 2008. HPLC-DAD-ESI-MS analysis of the constituents of aqueous preparations of verbena and lemon verbena and evaluation of the antioxidant activity. Journal of Pharmaceutical and Biomedical Analysis, 13, 463- 470.

Burt, S. 2004. Essential oils: their antibacterial properties and potential application in foods-a review. International Journal of Food Microbiology, 94, 223- 253.

Cetojevic Simin D.D., Bogdanovic G.M., Cvetkovic D.D., & Velicanski A.S. 2008. Antiproliferative and antimicrobial activity of traditional Kombucha and Satureja montana L. Kombucha. J. BUON, 13, 395- 401.

Ceyhan, N., & Ugur, A. 2001. Investigation of in vitro antimicrobial activity of honey. Rivista di Biologia, 94, 363– 371.

Clinical and Laboratory Standards Institute [CLSI]. 2018. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. In (11th ed. CLSI standard M07 ed.): Clinical and Laboratory Standards Institute, 950 West Valley Road, Suit 2500, Wayne, Pennsylvania 19087 USA.

Coton, M., Pawtowski, A., Taminiau, B., Burgaud, G., Deniel, F., Coulloumme-Labarthe, L., & Coton, E. 2017. Unraveling microbial ecology of industrial-scale Kombucha fermentations by metabarcoding and culture-based methods. Fems Microbiology Ecology, 93, 1– 16.

Friedman, M., Henika, P.R., Levin, C. E., Mandrell, R.E., & Kozukue, N. 2006. Antimicrobial activities of tea catechins and theaflavins and tea extracts against Bacillus cereus. Journal of Food Protection, 69, 354– 361.

Greenwalt, C.J., Ledford, R.A., & Steinkraus, K.H. 1998. Determination and Characterization of the Antimicrobial Activity of the Fermented Tea Kombucha. Lebensmittel-Wissenschaft & Technologie, 31, 291– 296.

Haizhen, M., Yang, Z., & Zongmao, C. 2008. Microbial fermented tea- a potential source of natural food preservatives. Trends in Food Science and Technology, 19, 124- 130.

Hayouni, E. A., Abedrabba, M., Bouix, M., & Hamdi, M. 2007. The effects of solvents and extraction method on the phenolic contents and biological activities in vitro of Tunisian Quercus coccifera L. and Juniperus phoenicea L. fruit extracts. Food Chemistry, 105, 1126-1134.

Jayabalan, R., Malbasa, R.V., Loncar, E.S., Vitas, J. S., & Sathishkumar, M. 2014. A Review on Kombucha tea—microbiology, composition, fermentation, beneficial effects, toxicity, and tea fungus. Comprehensive Reviews in Food Science and Food Safety, 10, 538- 550.

Kim, E.S., Liang, Y.R., Jin, J., Sun, Q.F., Lu, J.L., & Du, Y.Y. 2007. Impact of heating on chemical compositions of green tea liquor. Food Chemistry, 103, 1263- 1267.

Malbasa, R.V., Loncar, E.S., Vitas, J.S., & Canadanovic-Brunet, J.M. 2011. Influence of starter cultures on the antioxidant activity of kombucha beverage. Food Chemistry, 127, 1727- 1731.

Mani-Lopez E., Garcia H.S., Lopez-Malo A. 2012. Organic acids as antimicrobials to control Salmonella in meat and poultry products. Food Research International, 45, 713- 721.

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, 8, 171– 178.

Nzeako, B.C., & Hamdi, J. 2000. Antimicrobial potential of honey on some microbial isolates. Sultan Qaboos University medical journal, 2, 75- 79.

Noormandi, A., & Dabaghzadeh, F. 2015. Effects of green tea on Escherichia coli as an uropathogen. Journal of Traditional and Complementary Medicine, 5, 15- 20.

Primiani, C.N., Mumtahanah, P.M., & Ardhi, W. 2018. Kombucha fermentation test used for various types of herbal teas. Journal of Physics: Conference Series, 1025, 1- 9.

Roos, J.D., & Vuyst, L.D. 2018. Acetic acid bacteria in fermented foods and beverages. Current Opinion in Biotechnology, 49, 115- 119.

Russel, A.D. 1991. Mechanisms of bacterial resistance to non-antibiotics: food additives and food pharmaceutical preservatives. Journal of Applied Bacteriology, 71, 191- 201.

Song, J.M., & Seong, B.L. 2007. Tea catechins as a potential alternative anti-infectious agent. Expert Review of Anti-infective Therapy, 5, 497- 506.

Sreeramulu, G., Zhu, Y., & Knol, W. 2000. Kombucha fermentation and its antimicrobial activity. Journal of Agricultural and Food Chemistry, 48, 2589-2594.

Stapleton, P.D., Shah, S., Hamilton-Miller, J.M., Hara, Y., Nagaoka, Y., Kumagai, A., Uesato, S., & Taylor, P.W. 2004. Anti-Staphylococcus aureus activity and oxacillin resistance modulating capacity of 3-O-acyl-catechins. International Journal of Antimicrobial Agents, 24, 374– 380.

Steinkraus, K.H., Shapiro, K.B., Hotchkiss, J.H., & Mortlock, R.P. 1996. Investigations into the antibiotic activity of tea fungus/Kombucha beverage. Acta Biotechnolgia, 16, 199-205.

Talawat, S., Ahantharik, P., Laohawiwattanakul, S., Premsuk, A., & Ratanapo, S. 2006. Efficacy of fermented teas in antibacterial activity. Kasetsart Journal-Natural Science, 40, 925-933.

Taormina, P. J., Niemira, B.A., & Bauchat, L.R. 2001. Inhibitory activity of honey against foodborne pathogens as influenced by the presence of hydrogen peroxide and level of antioxidant power. International Journal of Food Microbiology, 69, 217–225.

Teoh, A.L., Heard, G., & Cox, J. 2004. Yeast ecology of kombucha fermentation. International Journal of Food Microbiology, 2(95), 119- 126.

Tumin, N., Halim, N., Shahjahan, M., Noor Izani, N., Sattar, M.A., Khan, A.H., & Mohsin, S.S. J. 2005. Antibacterial activity of local Malaysian honey. Malaysian Journal of Pharmaceutical Sciences, 3, 1- 10.

Velicanski, A.S., Cvetkovic, D.D., Markov, S.L., Tumbas V.T., & Savatovic, S.M. 2007. Antimicrobial and Antioxidant Activity of Lemon Balm Kombucha. Apteff, 38, 165- 172.

Valiyan, F., Koohsari, H., & Fadavi, A. (2021). Use of Response surface methodology to investigate the effect of several fermentation conditions on the antibacterial activity of several kombucha beverages. Journal of Food Science and Technology, 58(5), 1877- 1891.

Velicanski, A.S. Cvetkovic, D.D., Markov, S.L., Tumbas Saponjac, V.T., & Vulic, 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, 420-429.

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, 580-588.

Wang, Z.W., & Liu, X.L. 2008. Medium optimization for antifungal active substances production from a newly isolated Paenibacillus sp. using response surface methodology. Bioresour Technol. 99, 8245–8251.

Watawana, M.I., Jayawardena, N., Gunawardhana, C.B., & Waisundara, V.Y. 2016. Enhancement of the antioxidant and starch hydrolase inhibitory activities of king coconut water (Cocos nuciferavar. aurantiaca) by fermentation with Kombucha “teafungus.” International Journal of Food Science and Technology, 51, 490-498.

Wolfe, B.E., & Dutton, R.J. 2015. Fermented foods as experimentally tractable microbial ecosystems. Cell, 161, 49-55.

Yadegarinia, D., Gachkar, L., Rezaei, M.B., Taghizadeh, M., Astaneh, S.A., & Rasooli, I. 2006. Biochemical activities of Iranian Mentha piperita L. and Myrtus communis L. essential oils. Phytochemistry, 67, 1249-1255.

Yamada, Y., Yukphan, P., LanVu, H.T., Muramatsu, Y., Ochaikul, D. Tanasupawat, S., & Nakagawa, Y. 2012. Description of Komagataeibacter gen. nov., with proposals of new combinations (Acetobacteraceae). The Journal of General and Applied Microbiology, 58, 397-404.

Yoda, Y., Hu, Z.Q., Zhao, W.H., & Shimamura, T. 2004. Different susceptibilities of Staphylococcus and Gram-negative rods to epigallocatechin gallate. Journal of Infection and Chemotherapy, 10, 55-58.

Zarowska, B., Wojtatowicz, M., & Rymowicz, W. 2001. Production of citric acid on sugar beet molasses by single and mixed cultures of Yarrowia lipolytic. Eletronic Journal of Polish Agriculture Universities. 4 (2), 1-8.