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Antimicrobial Activities of Tea Catechins and Theaflavins and Tea Extracts Against Bacillus Cereus

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Antimicrobial Activities of Tea Catechins and Theaflavins and Tea Extracts Against Bacillus Cereus 354 1 Journal of Food Protection, Vol. 69, No. 2, 2006, Pages 354-361 71 Antimicrobial Activities of Tea Catechins and Theaflavins and Tea Extracts against Bacillus cereus MENDEL FRIEDMAN,I PHILIP R. HENIKA, CAROL E. LEVIN, ROBERT E. MANDRELL, AND NOBUYUKI KOZUKUE2 Western Regional Research Center, Agricultural Research Service, U.S. Department of Agriculture, 800 Buchanan Street, Albany, California 94710, USA; and Department of Food Service Industry, Uiduck University, Gyongbuk, 780-713, Korea MS 05-266: Received 31 May 2005/Accepted 8 September 2005 ABSTRACT We evaluated the antimicrobial activities of seven green tea catechins and four black tea theaflavins, generally referred to as flavonoids, as well as the aqueous extracts (infusions) of 36 commercial black, green, oolong. white, and herbal teas against Bacillus cereus (strain RM3I90) incubated at 21°C for 3, 15, 30, and 60 mm. The results obtained demonstrate that (I) (- )-gallocatechin-3-gallate, (- )-epigallocatechin-3-gallate. (- )-catechin-3-gallate, (- )-epicatechin-3-gallate, theaflavin-3, 3-digallate, theaflavin-3-gallate, and theaflavin-3-gallate showed antimicrobial activities at nanomolar levels; (ii) most com- pounds were more active than were medicinal antibiotics, such as tetracycline or vancomycin, at comparable concentrations; (iii) the bactericidal activities of the teas could be accounted for by the levels of catechins and theaflavins as determined by high-pressure liquid chromatography; (iv) freshly prepared tea infusions were more active than day-old teas; and (v) tea catechins without gallate side chains, gallic acid and the alkaloids caffeine and theobromine also present in teas, and herbal (chamomile and peppermint) teas that contain no flavonoids are all inactive. These studies extend our knowledge about the antimicrobial effects of food ingredients. The gram-positive, facultative aerobe Bacillus cereus gallate, (- )-gallocatechin, ( - )-gal locatechin-3-gallate, gallic acid, is a foodborne bacterium that has, on occasion, been shown chloramphenicol, gentamycin sulfate, tetracycline, theobromine, to contaminate baked goods, carrots, meat, milk products, and vancomycin were obtained from Sigma (St. Louis, Mo.). Caf- rice, sauces, soups, sprouts, and zucchini (10, 13, 15, 18, feine, clindamycin, and rifampicin were obtained from Fluka 20). In previous studies, we determined the relative activ- (Steinheim, Switzerland), and theaflavin, theaflavin-3-gallate, theaflavin-3-gallate, and theaflavin-3, 3-digallate were obtained ities of plant essential oils and phenolic compounds against from Wako Chemical Company (Richmond, Va.). Thirty-six teas pathogenic bacteria (4, 6-8). These studies have provided in tea bags were obtained from the Stash Tea Company (Portland, insight into the structural features that govern bactericidal Oreg.). activities as well as the candidates for use in formulations designed to reduce pathogens in foods. The present study HPLC analysis of teas. Flavonoids were extracted from tea was designed to extend our knowledge of the antimicrobial leaves by stirring them for 5 min in boiled water previously ad- effectiveness of various flavonoids, individually and as justed to p1-1 7 to approximate the pH of the PBS buffer used for the bactericidal assays. The HPLC technique used to determine mixtures found in teas. To extend our knowledge about the the content of the flavonoids in teas has been described in detail structure-antimicrobial activity relationships of different elsewhere (9). Briefly, HPLC was carried out in Korea on a Hi- classes of plant compounds, the specific objectives of this tachi instrument equipped with an Inertsil column, an Autosam- study were (i) to compare the bactericidal activities against pler, and a Shimadzu UV-VIS detector. The mobile-phase gradient B. cereus of seven tea catechins and four theaflavins to the consisted of a mixture of acetonitrile and 20 mM KH 2PO4. The activities of clinical antibiotics shown to be active against II flavonoids were determined in a single run. The flavonoid con- Bacilli (16) and (ii) to relate the antimicrobial effects of 36 tent of the pH 7 water extracts did not differ from the levels in aqueous tea extracts to their content of these flavonoids as extracts obtained with unadjusted water. The same tea bags were determined by high-pressure liquid chromatography extracted in California for the bactericidal assays described below. (HPLC). Source of bacteria. B. cereus/thuringiensis (strain RM3 190) MATERIALS AND METHODS was isolated in our laboratory by Dr. Michael Cooley from soil and was identified by two bacterial identification systems (Biolog. Test compounds. (+ )-Catechin, (± )-catechin, (- )-catechin, Hayward, Calif., and Microbial ID, Newark, Del.). (-)-catechin-3 -gal late, (+ )-epicatechin, (- )-epicatcchin, (- )-ep- icatechin-3-gallate, (- )-epigallocatechin, (- )-epigallocatechin-3- Preparation of test substances for bactericidal assays. For steeping of tea leaves, a stainless steel screen from a "Beehouse" Author for correspondence. Tel: 510-559-5615; Fax: 510-559-5777; teapot. obtained at a local Peets Coffee and Tea store, was placed E-mail: [email protected]. with 0.9 g of tea leaves into a 250-ml beaker with 150 ml of hot Presented at the XI International Congress of Bacteriology and Applied 50 mM phosphate-buffered saline (PBS, pH 7.0) that had been Microbiology. IUMS-2005 Meeting, San Francisco, California, 23 to 28 brought to a boil and then allowed to sit for 2 mm. The teas were July 2005. Abstract B-I 160. steeped with gentle stirring for 5 mm. A steeped tea aliquot (200 J. Food Prot., Vol. 69, No. 2 ANTIMICROBIAL ACTIVITIES OF TEA FLAVONOIDS AND TEAS AGAINST B. CEREUS 355 FIGURE 1. Structures of the tea catechins 2kOH .. OH H and theaflavins evaluated in this study. H 0 6LJL..i;fI 6 HOH I 4 0H OH OH HO" OH OH °H H (.)_catechèn (4 ).epitechjn (-)-epigallocatechin H OH HO HqH - OH ^OH HO5 OH OH OH OH OH O((OH HO H OH OH OH (-)-catechin-3-gallate tH ()-epicatechin3gallate OH (-)-gallocatechin-3-gallate Hç(JOH OH OH 0 HO H (-)-epigallocatechin-3-gallate theaflavin-3-gallate theaflavin-3 .gatate theaflavin-3,3-digallate jil) was then added to the PBS (1,800 III). This sample (200 p.l) brewed and day-old tea extracts (infusions): 12 wells for PBS- was again diluted with PBS (1,800 11) for a final 100-fold dilu- negative controls and 60 wells for five different teas, each with tion. The latter was used as the first test dose. The second dose the two dilution series as described above for the preparation of was diluted by one third, i.e.. tea (333 p.l) plus PBS (667 .LI). The the tea infusions. The contents of each of the 72 wells were then pH of these samples was 7.0 at 21°C. Steeped teas were left stand- tested after a 60-min incubation at 21°C as described below. ing on the bench top for 24 h at 21°C and tested as "day-old" teas. Antimicrobial assays. The bactericidal assay described pre- For catechins, the test solution was prepared by dissolving viously (6, 8) was modified for this study. B. cereus organisms the test substance (10 mg) in PBS (9.9 ml) in a 50-ml test tube were stored on streaked plates subcultured for 16 to 18 h at 37°C to give a 0.1% solution. The tube was warmed in a microwave with Luria-Bertani agar (LB) plates (Difco, Becton Dickinson, oven for 10 s and vortexed to clarity. Theaflavins were available Sparks, Md.). Overnight LB broth cultures were prepared by har- only in 1-mg quantities in glass vials. PBS (I ml) was added to vesting a few isolated colonies from the plate with a sterile loop these vials. These vials were then warmed in a microwave oven and suspending them into 5 ml of LB broth in a 15-ml sterile for 5 s and vortexed to give clear solutions. These test solutions plastic tube. The capped tubes were incubated with shaking (200 were then diluted 100-fold with PBS before being added to mi- rpm) at 37°C for 18 h. crotiter plates. For the assay, bacterial suspensions (ca. 100 to 200 CFU per The pure compounds in PBS (500 Id each) were added to lane) were placed on the square plates with grids used for count- five sterile tubes (1.9 ml). Starting with the 1/100 test solution (I ing. Briefly, each sample (1 ml) of an 18-h LB broth culture of MI), we performed serial dilutions, using 500 til for each transfer, B. cereus was added to a 1.9-ml microfuge tube, and the bacteria to the sterile tubes for a total of five dilutions. In a typical ex- were pelleted by centrifugation in a microfuge (15,800 X g) for periment, microtiter plates (96 wells; Nalge, Nunc, Rochester, 1 mm. After removal of the supernatant, sterile PBS (1 ml) was N.Y.) were prepared with PBS-negative controls (100 i.l each in added to the pellet. The pellet was then resuspended by gentle six wells) as well as three test substances with five dilutions (100 aspiration in and out of a transfer pipette. The optical density at sl each dilution per well). The contents of these 24 wells were 620 nm of the sample was adjusted with PBS to ca. 1.0. The then tested at three time intervals. suspension (40 il) was added to the PBS (960 p,l). The latter The tea samples. in 72 wells, were prepared for the freshly (160 1.d) was then added to PBS (5 ml), vortexed, and poured into 356 FRIEDMAN El AL. Food Prot., Vol. 69, No. 2 TABLE 1. Antimicrobial activities of tea flavonoids and clinical antibiotics against Bacillus cereus incubated at 21°C for 3, 15, and 30 min" BA50 (nmol/well) Relative ratios of 30-mm Compound 3 mm 15 mm 30 mm act iv it ies" (-)-Gal locatechin-3 -gallate
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