Abstract
Kombucha is a health-promoting fermented beverage traditionally made by fermenting a sweetened tea with a symbiotic culture of yeast species and acetic acid bacteria. The aim of this work was to develop a beverage using red grape juice as an alternative substrate. Grape juice contains various nutrient elements and phytochemicals, such as polyphenols, which possess a wide range of biological activities. We investigated the chemical characteristics and sensory and antimicrobial activities of the fermented grape juice Kombucha beverage. The pH decreased from 3.95 to 2.9 during the fermentation process and remained fairly constant thereafter, and the acetic acid bacteria and yeast counts in the broth increased up to 6 days of fermentation and subsequently decreased. Phenolic and anthocyanin contents and the antioxidant activity of the fermented beverage were higher after fermentation, with the maximum increase observed on the sixth day of fermentation when values were approximately 2.47- and 1.59-fold higher than pre-fermentation values, respectively, as assessed by 2,2-diphenyl-1-picrylhydrazyl and 2,2′-azino-bis (3-ethylbenzothiazoline-6- sulfonic acid) radical scavenging assays. Fourier transform infrared spectroscopy was used for the qualitative analysis of the grape juice before and after fermentation. Distinct peak variations in the spectral region between 2500 and 1650 cm−1 were observed, which matched the appearance of organic acids and changes in phenolic compounds. Fermented juice Kombucha showed antibacterial activity toward all tested bacteria, which can be primarily ascribed to the increased production of acetic acid, but also to the biosynthesis of other metabolites, during the fermentation process. The 6-day fermented juice was the most appreciated by the taste panel based on the overall quality evaluation; with prolongation of fermentation the fermented juice acquired a distinct sour flavor.
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References
Agatonovic-Kustrin S, Morton DW, Yusof APM (2013) The use of fourier transform infrared (FTIR) spectroscopy and Artificial Neural Networks (ANNS) to assess wine quality. Mod Chem Appl 1:4. doi:10.4172/2329-6798.1000110
Alcaide-Hidalgo JM, Pueyo E, Polo MC, Martı´nez-Rodrı´guez AJ (2007) Bioactive peptides released from Saccharomyces cerevisiae under accelerated autolysis in a wine model system. J Food Sci 72:276–279
Arnous A, Makris DP, Kefalas P (2002) Correlation of pigment and flavanol content with antioxidant properties in selected aged regional wines from Greece. J Food Compos Anal 15:655–665
Ayed L, Hamdi M (2015) Manufacture of a beverage from cactus pear juice using tea fungus fermentation. Ann Microbiol 65:2293–2299
Bae S, Fleet GH, Heard GM (2006) Lactic acid bacteria associated with wine grapes from several Australian vineyards. J Appl Microbiol 100:712–727
Balentine DA (1997) Special issue: tea and health. Crit Rev Food Sci Nutr 8:691–692. doi:10.1080/10408399709527796
Burin VM, Falcão LD, Gonzaga LV, Fett R, Rosier JP, Bordignon-Luiz MT (2010) Colour, phenolic content and antioxidant activity of grape juice. Cienc Tecnol Aliment 30(4):1027–1032
Cai Y, Lilley TH, Haslam E (1990) Polyphenol–anthocyanin copigmentation. J Chem Soc Chem Commun 5:380–383
Cantos E, Espin JC, Tomas-Barberan FA (2002) Varietal differences among the polyphenol profiles of seven table grape cultivars studied by LC-DAD-MS-MS. J Agric Food Chem 50:5691–5696
Chen C, Liu BY (2000) Changes in major components of tea fungus metabolites during prolonged fermentation. J Appl Microbiol 89:834–839
Chu SC, Chen C (2006) Effects of origins and fermentation time on the antioxidant activities of kombucha. Food Chem 98:502–507
Dani C, Oliboni LS, Vanderlinde R, Pra D, Dias JF, Yoneama ML, Bonatto D, Salvador M, Henriques JAP (2009) Antioxidant activity and phenolic and mineral content of rose grape juice. J Med Food 12:188–192
Delgado-Andrade C, Rufian-Henares JA, Morales FJ (2005) Assessing the antioxidant activity of melanoidins from coffee brews by different antioxidant methods. J Agric Food Chem 53(20):7832–7836
Dopico-Garcia MS, Fique A, Guerra L, Afonso JM, Pereira O, Valentao P, Andrade PB, Seabra RM (2008) Principal components of phenolics to characterize red Vinho Verde grapes: anthocyanins or non-coloured compounds. Talanta 75:1190–1202
Du Toit WJ, Lambrechts MG (2002) The enumeration and identification of acetic acid bacteria from South African red wine fermentations. Int J Food Microbiol 74:57–64
Dufresne C, Farnworth E (2000) Tea, Kombucha, and health: a review. Food Res Int 33:409–421
Fernández K, Agosin E (2007) Quantitative analysis of red wine tannins using fourier-transform mid-infrared spectrometry. J Agric Food Chem 55:7294–7300
God JM, Tate P, Larcom LL (2007) Anticancer effects of four varieties of muscadine grape. J Med Food 10:54–59
Goh WN, Rosma A, Kaur B, Fazilah A, Karim AA, Rajeev B (2012) Fermentation of black tea broth (Kombucha): I. Effects of sucrose concentration and fermentation time on the yield of microbial cellulose. Int Food Res J 19(1):109–117
Greenwalt CJ, Steinkraus KH, Ledford RA (2000) Kombucha, the fermented tea: microbiology, composition, and claimed health effects. J Food Prot 63:976–981
Han H (2007) Study on optimization of kefir fermentation and freeze dry technics. Beijing, pp 12–13
Jayabalan R, Marimuthu S, Swaminathan K (2007) Changes in content of organic acids and tea polyphenols during kombucha tea fermentation. Food Chem 102:392–398
Jayabalan R, Subathradevi P, Marimuthu S, Sathishkumar M, Swaminathan K (2008) Changes in free radical scavenging ability of kombucha tea during fermentation. Food Chem 109:227–234
Jayabalan R, Malini K, Sathishkumar M, Swaminathan K, Yun SE (2010) Biochemical characteristics of tea fungus produced during Kombucha fermentation. Food Sci Biotechnol 19(3):843–847
Jayabalan R, Malbaša RV, Lonćar ES, Vitas JS, Sathishkumar M (2014) A review on Kombucha tea—microbiology, composition, fermentation, beneficial effects, toxicity, and tea fungus. Comp Rev Food Sci Food Safe 13:539–550
Jung K, Wallig MA, Singletary KW (2006) Purple grape juice inhibits 7,12-dimethylbenz- [a] anthracene (DMBA)-induced rat mammary tumorigenesis and in vivo DMBA-DNA adduct formation. Cancer Lett 233(2):279–288
Kappel T, Anken RH (1993) The tea-mushroom. Mycology 7:12-13
Kurtzman CP, Robnett CJ, Basehoar-Powers E (2001) Zigosaccharomyces kombuchaensis, a new ascosporogeneous yeast from “Kombucha tea”. FEMS Yeast Res 2:133–138
Liao H, Cai Y, Haslam E (1992) Polyphenol interactions. Anthocyanins: copigmentation and colour changes in red wines. J Sci Food Agric 59:299–305
Liu CH, Hsu WH, Lee FL, Liao CC (1996) The isolation and identification of microbes from a fermented tea beverage, Haipao, and their interactions during Haipao fermentation. Food Microbiol 13:407–415
Maier T, Schieber A, Kammerer DR, Carle R (2009) Residues of grape (Vitis vinifera) seed oil production as a valuable source of phenolic antioxidants. Food Chem 112:551–559
Malbaša RV, Loncǎr ES, Vitas JS, Čanadanović-Brunet JM (2011) Influence of starter cultures on the antioxidant activity of kombucha beverage. Food Chem 127:1727–1731
Mani-López E, García HS, López-Malo A (2012) Organic acids as antimicrobials to control Salmonella in meat and poultry products. Food Res Int 45:713–721
Marsh AJ, O’Sullivan O, Hill C, Ross RP, Cotter PD (2014) Sequence-based analysis of the bacterial and fungal compositions of multiple kombucha (tea fungus) samples. Food Microbiol 38:171–178
Mazza G, Brouillard R (1987) Recent developments in the stabilization of anthocyanins in food products. Food Chem 25:207–225
Morata A, Gómez-Cordovés C, Subervolia J, Bartolomé B, Colomo B, Suarez JA (2003) Adsorption of anthocyanins by yeast cell walls during fermentation of red wines. J Agric Food Chem 51:4084–4088
OIV (International Organization of Vine and Wine) (2010) Recueil des méthodes internationales d’analyses des vins et des moûts. In Office International de la vigne et du vin (Eds.), France
Park YS, Im MH, Ham KS, Kang SG, Park YK, Namiesnik J, Leontowicz H, Leontowicz M, Trakhtenberg S, Gorinstein S (2015) Quantitative assessment of the main antioxidant compounds, antioxidant activities and FTIR spectra from commonly consumed fruits, compared to standard kiwi fruit. Food Sci Technol 63:346–352
Pauline T, Dipti P, Anju B, Kavimani S, Sharma SK, Kain AK, Sarada SKS, Sai Ram M, Ilavazhagan G, Kumar D, Selvamurthy W (2001) Studies on toxicity; anti-stress and hepatoprotective properties of kombucha tea. Biomed Environ Sci 14 :207–213
Randazzo W, Corona O, Guarcello R, Francesca N, Germanà MA, Erten H, Moschetti G, Settanni L (2016) Development of new non-dairy beverages from Mediterranean fruit juices fermented with water kefir microorganisms. Food Microbiol 54:40–51
Reiss J. (1994) Influence of different sugars on the metabolism of the tea fungus. Z Lebensm Unters Forsch 198:258–61
Rhodes PL, Mitchell JW, Wilson MW, Melton LD (2006) Antilisterial activity of grape juice and grape extracts derived from Vitis vinifera variety Ribier. Int J Food Microbiol 107:281–286
Shanmuganayagam D, Warner TF, Krueger CG, Reed JD, Folts JD (2007) Concord grape juice attenuates platelet aggregation, serum cholesterol and development of atheroma in hypercholesterolemic rabbits. Atherosclerosis 190:135–142
Sievers M, Lanini C, Weber A, Schuler-Schmid U, Teuber M (1995) Microbiology and fermentation balance in kombucha beverage obtained from a tea fungus fermentation. Syst Appl Microbiol 18:590–594
Singletary KW, Jung KJ, Giusti M (2007) Anthocyanin-rich grape extract blocks breast cell DNA damage. J Med Food 10:244–251
Singleton VL, Orthofer R, Lamuela-Raventor RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocateu reagent. Methods Enzymol 299:152–178
Somers TC, Evans ME (1977) Spectral evaluation of young red wines: anthocyanin equilibria, total phenolics, free and molecular SO2, “chemical age”. J Sci Food Agric 28:279–287
Spacil Z, Novakova L, Solich P (2008) Analysis of phenolic compounds by high performance liquid chromatography and ultra performance liquid chromatography. Talanta 76:189–199
Sreeramulu G, Zhu Y, Knol W (2000) Kombucha fermentation and its antimicrobial activity. J Agric Food Chem 48:2589–2594
Steinkraus KH, Shapiro KB, Hotchkiss JH, Mortlock RP (1996) Examinations on antibiotic activity of tea fungus/Kombucha beverage. Acta Biotechnol 16:199–205
Sun TY, Li JS, Chen C (2015) Effects of blending wheatgrass juice on enhancing phenolic compounds and antioxidant activities of traditional kombucha beverage. J Food Drug Anal 23:709–718
Thapa N, Pal J, Tamang JP (2006) Phenotypic identification and technological properties of lactic acid bacteria isolated from traditionally processed fish products of the Eastern Himalayas. Int J Food Microbiol 107:33–38
Torskangerpoll K, Andersen OM (2005) Color stability of anthocyanins in aqueous solutions at various pH values. Food Chem 89:427–440
Tsanga C, Higginsa S, Duthiea GG, Duthiea SJ, Howiea M, Mullena W, Leana MEJ, Crozier A (2005) The influence of moderate red wine consumption on antioxidant status and indices of oxidative stress associated with CHD in healthy volunteers. Br J Nutr 93:233–240
Velićanski AS, Cvetković DD, Markov SL, Tumbas Šaponjac VT, Vulić JJ (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 Technol Biotechnol 52(4):420–429
Vijayaraghavan R, Singh M, Rao PVL, Bhattacharya R, Kumar P, Sugendran K, Kumar O, Pant SC, Singh R (2000) Subacute (90 days) oral toxicity studies of Kombucha Tea. Biomed Environ Sci 13(4):293–299
Vína I, Semjonovs P, Linde R, Patetko A (2013) Glucuronic acid containing fermented functional beverages produced by natural yeasts and bacteria associations. Int J Res Rev Appl Sci 14:17–25
Vīna I, Semjonovs P, Linde R, Deniņa I (2014) Current evidence on physiological activity of Kombucha fermented beverage and expected health effects. J Med Food 17(2):179–188
Vinson JA, Yang J, Proch J, Liang X (2000) Grape juice, but not orange juice, has in vitro, ex vivo, and in vivo antioxidant properties. J Med Food 3(4):167–171
Xia EQ, Deng GF, Guo YJ, Li HB (2010) Biological activities of polyphenols from grapes. Int J Mol Sci 11:622–646
Yang Z, Zhou F, Ji B, Li B, Luo Y, Yang L, Li T (2010) Symbiosis between microorganisms from Kombucha and Kefir: potential significance to the enhancement of Kombucha function. Appl Biochem Biotechnol 160:446–455
Yavari N, Mazaheri Assadi M, Larijani K, Moghadam MB (2010) Response surface methodology for optimization of glucuronic acid production using kombucha layer on sour cherry juice. Aust J Basic Appl Sci 4(8):3250–3256
Yavari N, Assadi MM, Moghadam MB, Larijani K (2011) Optimizing glucuronic acid production using tea fungus on grape juice by response surface methodology. Aust J Basic Appl Sci 5:1788–1794
Zafra-Rojas QY, Cruz-Cansino N, Ramírez-Moreno E, Delgado-Olivares L, Villanueva-Sánchez J, Alanís-García E (2013) Effects of ultrasound treatment in purple cactus pear (Opuntia ficus-indica) juice. Ultrason Sonochem 20:1283–1288
Zhang Y, Chen J, Lei Y, Zhou Q, Sun S et al (2010) Discrimination of different red wine by Fourier-transform infrared and two-dimensional infrared correlation spectroscopy. J Mol Struct 974:144–150
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Ayed, L., Ben Abid, S. & Hamdi, M. Development of a beverage from red grape juice fermented with the Kombucha consortium. Ann Microbiol 67, 111–121 (2017). https://doi.org/10.1007/s13213-016-1242-2
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DOI: https://doi.org/10.1007/s13213-016-1242-2