Microbial fermented tea – a potential source of natural food preservatives

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<ul><li><p>Science and Technology, 453003 Xinxiang,</p><p>industrial applications.</p><p>Holzapfel, 1996). Although plants can provide a vast sourceof natural preservatives, many potential biological preserva-</p><p>for innovative applications in the modern society.This article reveals the background information of micro-</p><p>Trends in Food Science &amp; Technresearch and development of these antimicrobial compounds</p><p>from microbial fermentation of tea are discussed for potential</p><p>nisin by lactic acid bacteria. Some potential and unexploredfood fermentation processes are certainly new possibilities* Corresponding author.</p><p>0924-2244/$ - see front matter 2007 Elsevier Ltd. All rights reserved.doi:10.1016/j.tifs.2007.10.001d</p><p>n</p><p>tives are originated from traditional food fermentations. Themost well known example is probably the production oftation process with tea leaves as substrates. The antimicrobial</p><p>components produced during the fermentation process have</p><p>shown inhibitory effects against several food-borne and patho-</p><p>genic bacteria. With the trend of increasing use of natural and</p><p>biological preservatives in food products, natural antimicrobial</p><p>agents from microbial fermented tea may offer an innovative</p><p>and interesting measure for such applications. However,</p><p>a breakthrough in this field can only be realised after several</p><p>critical aspects are clarified and further studied. Only then,</p><p>the application of these potential, novel and natural antimicro-</p><p>bial substances from microbial fermented tea can be industri-</p><p>alized. The present review describes some unique microbial</p><p>fermentation of tea and the antimicrobial activities forme</p><p>during the fermentation process. Moreover, future needs iHenan Province, ChinabFood and Bioprocess Engineering Group, WageningenUniversity and Research Centre, P.O. Box 8129, 6700</p><p>EV, Wageningen, Netherlands (Tel.:D31 343 538103;</p><p>fax: D31 343 538405; e-mail: yang.zhu@wur.nl)cChinese Tea Research Institute, Chinese Academy of</p><p>Agricultural Sciences, 310008 Hangzhou, Zhejiang</p><p>Province, China</p><p>Antimicrobial activities of microbial fermented tea are much</p><p>less known than its health beneficial properties. These anti-</p><p>microbial activities are generated in natural microbial fermen-Microbial fermented</p><p>tea e a potential</p><p>source of natural</p><p>food preservatives</p><p>Haizhen Moa, Yang Zhub,* andZongmao Chenc</p><p>aDepartment of Food Science, Henan Institute ofReview</p><p>IntroductionTea is one of the most consumed beverages worldwide.</p><p>In fact, there are mainly three different kinds of tea. In Chinaand many Southeast Asian countries, green tea is preferred.In Western countries and the rest of the world, the consump-tion of black tea is the highest. Another kind of tea is Kom-bucha, which is a sweet-sour tea beverage made actuallyfrom tea extract supplemented with sugar and fermentedwith yeast and acetic-acid bacteria. Fermentation processis necessary to produce black tea and Kombucha. Blacktea can be further subdivided into naturally oxidized tea(although the term of fermentation is often used), and micro-bial fermented tea. Fermentation process for producing mostblack teas is actually an oxidation process catalyzed byenzymes that are originally present in tea leaves (Fowler,Leheup, &amp; Cordier, 1998). Because no microorganismsare involved in this kind of enzyme-oxidized black tea,the use of the term fermentation is obviously not completelycorrect. Microbial fermentation in the production of blacktea, however, is found to be carried out solely in certain Chi-nese tea assortments. Therefore, this kind of tea is littleknown outside China, whereas Kombucha is exceptionallywell known because of its increasing interests in the West.</p><p>Recently, several microbial fermented teas got noticed inthe Western world, probably not only because of trade ex-pansions between China and the West, but also because ofseveral health beneficial claims associated with microbialfermented tea. A few studies reveal that extracts from mi-crobial fermented teas contain natural antimicrobial com-ponents that have inhibitive effect on several food-bornepathogen and spoilage bacteria (Greenwalt, Ledford, &amp;Steinkraus, 1998; Mo, Xu, Yan, &amp; Zhu, 2005; Sreeramulu,Zhu, &amp; Knol, 2000; Sreeramulu, Zhu, &amp; Knol, 2001;Steinkraus, Shapiro, Hotchkiss, &amp; Mortlock, 1996).</p><p>Application of natural antibacterial agents has been in-creasingly noticed as a novel trend in biological preserva-tion of foods in recent years (Schillinger, Geisen, &amp;</p><p>ology 19 (2008) 124e130bial fermented Puer tea and Fuzhuan brick-tea, as well as</p></li><li><p>fermented tea beverage Kombucha. The importance of theirantibacterial effects on several food-borne bacteria are givenin detail. Potential applications and research needs of thesemicrobial fermented teas are also critically discussed. Theantimicrobial effects of tea catechins or polyphenols havebeen intensively described previously elsewhere (An et al.,2004; Bandyopadhyay, Chatterjee, Dasgupta, Lourduraja,&amp; Dastidar, 2005; Cushnie &amp; Lamb, 2005; Friedman,Henika, Levin,Mandrell, &amp;Kozukue, 2006; Hamilton-Miller,1995; Hirasawa &amp; Takada, 2004; Kim, Ruengwilysup, &amp;Fung, 2004; Si et al., 2006; Taguri, Tanaka, &amp; Kouno, 2004;Yamamoto, Matsunaga, &amp; Friedman, 2004; Yilmaz, 2006)and so this topic is not included here.</p><p>Microbial fermentation and antimicrobial effect ofPuer tea, Fuzhuan brick-tea and Kombucha</p><p>Both Puer tea and Fuzhuan brick-tea are microbial fer-mented black teas, whereas Kombucha is a fermented drink</p><p>tea polyphenols in tea leaves come into contact with thetea polyphenol oxidases and then oxidized in the conse-quent fermentation process. During the Puer tea fermenta-tion process, fresh leaves are fixed by heat in a drum toinactivate polyphenol oxidases. The fixed leaves are thenrolled and partially dried. The partially dried leaves arepiled up in humid conditions (moisture content w40% at25e60 C) for a few weeks, during which the tea polyphe-nols are more intensively oxidized by the action of micro-organisms and environmental oxygen than in black teafermentation process, resulting in low concentrations oftea polyphenols and tea catechins (Liang, Zhang, &amp; Lu,2005).</p><p>Puer tea has not only a unique flavour but also severalhealth beneficial properties, such as suppressing fatty acidsynthase expression (Chiang et al., 2006), acting as an in-hibitor of lipid and nonlipid oxidative damage and alsoexhibiting metal-binding ability, reducing power, and scav-</p><p>aluatio</p><p>Press</p><p>ion of </p><p>ing</p><p>tion o</p><p>125H. Mo et al. / Trends in Food Science &amp; Technology 19 (2008) 124e130of tea extract supplemented with sucrose and fermentedwith yeasts and acetic-acid bacteria. All three teas haveshown obvious antibacterial effects.</p><p>Fermentation process and antimicrobialcharacteristics of Puer tea</p><p>Puer tea is a unique Chinese microbial fermented tea ob-tained through indigenous tea fermentation where micro-organisms are involved in the manufacturing process. Aschematic description of Puer tea production is shown inFig. 1. This tea is different from common black tea that un-dergoes a natural oxidation process through enzymes orig-inally existing in tea leaves (Fowler et al., 1998). Theprocess of Puer tea manufacture is characterized by solid-state fermentation with natural flora as inoculums of whichthe fungus Aspergillus niger plays a key role (Mo et al.,2005; Xu, Yan, &amp; Zhu, 2005). The processing of Puer teais quite different from that of black tea, although they areboth called fermented teas. During black tea processing,fresh tea leaves are rolled and cut before drying so that</p><p>Wetting and cooling Ripening Ev</p><p>Loose Puer tea productPasteurization</p><p>DryingSteaming and pressing</p><p>Collecting of fresh tea leaves Inactivat</p><p>GradDrying Steaming treatment</p><p>Fig. 1. Schematic descripenging effect for free radicals (Duh, Yen, Yen, Wang, &amp;Chang, 2004; Jie et al., 2006). Kuo et al. (2005) reportedthat Puer tea and oolong tea can lower the levels of triglyc-eride more significantly than that of green tea and black tea,whereas Puer tea and green tea are more efficient thanoolong tea and black tea in lowering the level of totalcholesterol. Liang et al. (2005) reported that Puer tea sup-presses the genotoxicity induced by nitroarenes, lowers theatherogenic index and increases HDL (high density lipo-protein) e total cholesterol ratio. Rather recently, antimuta-genic and antimicrobial activities of Puer tea were alsoreported (Wu, et al., 2007). Although Puer tea has a historyof production and consumption for hundreds of years, fewstudies can be found on its microbiological properties,especially during the fermentation process.</p><p>Mo et al. (2005) have done a microbiological analysis onsamples from the indigenously fermented Puer tea. Micro-bial counting and identification revealed that A. niger wasthe dominating microorganism during the fermentation.Antimicrobial activity of fermentation samples shows</p><p>Inspection and packaging</p><p>n and grading</p><p>ed tea product Storage and ripening</p><p>Inspection and packaging</p><p>enzymes Dispersion of tea blocks</p><p>Natural inoculation and fermentation</p><p>f Puer tea manufacture.</p></li><li><p>inhibitory effect on several food-borne bacteria, includingspore-forming bacteria Bacillus cereus, Bacillus subtilis,Clostridium perfringens and Clostridium sporogenes. Theantimicrobial activity increases with the course of the fer-mentation. This implies that certain metabolites of A. nigergrowing on tea leaves have the feature of inhibiting certainfood-borne bacteria. As the fermentation process willdecrease the content of tea polyphenols and catechins, theincrease in antimicrobial activity of Puer tea results obvi-</p><p>antimicrobial properties of the tested teas. All the parame-</p><p>Both results show that, in addition to the antimicrobialproperties of tea polyphenols and catechins, the inhibitoryeffects are probably due to the metabolites produced duringthe fermentation processing.</p><p>Fermentation process and antimicrobial characteristicsof Kombucha</p><p>Kombucha is a slightly sweet-sour flavoured tea bever-age, obtained by fermentation of sweetened boiled tea</p><p>tivatio</p><p>P</p><p>ation Softening with steam Cooling andbrick-making </p><p>of Fu</p><p>126 H. Mo et al. / Trends in Food Science &amp; Technology 19 (2008) 124e130ters were changed via the inhibitory effects by tea. Theseinhibitory effects have also been examined by using thepour plate count technique for validation of the model.</p><p>Collecting of fresh tea leaves Enzyme inac</p><p>Fungal fermentation Drying</p><p>Natural oxidMixing Steaming</p><p>Fig. 2. Schematic descriptionously in the formation of antimicrobial components otherthan tea polyphenols and catechins, or in their conversionto other new compounds.</p><p>Fermentation process and antimicrobial characteristicsof Fuzhuan brick-tea</p><p>Fuzhuan brick-tea is another kind of microbial fer-mented tea uniquely found in China (Xu, Mo, Yan, &amp;Zhu, 2007). A schematic description of Fuzhuan brick-teaproduction is given in Fig. 2.</p><p>In a similar manner to studying Puer tea, we analyzedthe microbiological composition and tested the antimicro-bial activity of extracts from the indigenously fermentedFuzhuan brick-tea (unpublished data). Microbial countingand identification revealed that Aspergillus spp., Penicil-lium spp. and Eurotium spp. were the main microorganismsisolated from the samples during fermentation and Euro-tium spp. was the dominating fungus during the fermenta-tion. Antibacterial tests of extracts of fermented teashowed inhibitory effect on several food-borne bacteria,including spore-forming bacteria B. cereus, B. subtilis,C. perfringens and C. sporogenes. The antibacterial activityincreased with the course of the fermentation. This impliesthat certain metabolites of the fungi growing on tea leaveshad the feature of inhibiting certain food-borne bacteria.</p><p>Yao, Tan, Zhang, Su, &amp; Wei (1998) developed a bulkacoustic wave bacterial growth sensor to study inhibitoryeffects of tea by continuous monitoring of disturbances inProteus spp. growth in the aqueous extracts of variousteas, including Fuzhuan brick-tea. The kinetic parameters,such as asymptote, maximum specific growth rate, lagtime, and generation time were accurately estimated by us-ing the growth response model. This model characterizesackaging &amp; storage</p><p>zhuan brick-tea manufacture.with a mixed culture of yeasts and acetic-acid bacteria(Aidoo, Nout, &amp; Sarkar, 2006). A flowchart of Kombuchapreparation is given in Fig. 3. Kombucha originated innortheast China (former Manchuria region) and later spreadto Russia and the rest of the world. Kombucha is also fre-quently called tea fungus in the literature, although thereis actually no fungus involved in the fermentation (Benk,1988; Liu, Hsu, Lee, &amp; Liao, 1996; Mayser, Fromme,Leitzmann, &amp; Grunder, 1995; Sievers, Lanini, Weber,SchulerSchmid, &amp; Teuber, 1996; Steinkraus et al., 1996).This beverage reportedly has a number of health benefits,for example, against metabolic disease, arthritis, psoriasis,constipation, indigestion, and hypertension, but there arefew solid scientific evidences available yet for its efficacy(Dufresne &amp; Farnworth, 2000; Ernst, 2003; Greenwalt,Steinkraus, &amp; Ledford, 2000; Hartmann, Burleson, Holmes,&amp; Geist, 2000; Pauline et al., 2001; Ram et al., 2000). Byvirtue of the numerous health-promoting aspects reportedand the easy and safe preparation of this beverage athome, it has gained popularity as other traditional beverages.Kombucha is a symbiotic growth of bacteria (Acetobacterxylinum, Acetobacter xylinoides, Bacterium gluconicum)and yeast strains (Schizosaccharomyces pombe, Saccharo-mycodes ludwigii, Saccharomyces cerevisiae, etc.) culturedin a sugared tea (Chen &amp; Liu, 2000; Chu &amp; Chen, 2006;Greenwalt et al., 1998; Teoh, Heard, &amp; Cox, 2004). The ex-act microbiological composition also depends on the sourceof inoculums of the tea fermentation. Growth patterns ofthese microorganisms during the fermentation process ofKombucha are not well documented. Cellulose producedduring the fermentation by A. xylinum appears as a thinfilm on top of the sugared tea broth where the cell mass ofbacteria and yeasts is attached. This fungus-like mixture ofmicroorganisms and cellulose is likely why Kombucha isalso called tea fungus. Glucose liberated from sucrose ismetabolized for the synthesis of cellulose and gluconicacid by Acetobacter strains. Fructose is metabolized into</p><p>n and grinding Grading and bagging</p></li><li><p>127H. Mo et al. / Trends in Food Science &amp; Technology 19 (2008) 124e130ethanol and carbon dioxide by yeasts. Ethanol is oxidized toacetic acid by Acetobacter strains.</p><p>It is also reported that the fermentation process inducesthe synthesis of B complex of vitamins and folic acid(Bauer-Petrovska &amp; Petrushevska-Tozi, 2000). The pHvalue of Kombucha decreases during the fermentation pro-cess following the increase in organic acid content (Blanc,1996; Sievers et al., 1996). The resultant low pH and pres-ence of antimicrobial metabolites reduce the competition ofother bacteria, yeasts and filamentous fungi.</p><p>The antimicrobial activity of Kombucha was testedagainst a number of pathogenicmicroorganisms (Sreeramuluet al., 2000). Staphylococ...</p></li></ul>

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