- R )- L − C. in C. sakazakii )-catechin (95% purity), ( + C until use or further treatments. 2010 Institute of Food Technologists ◦ doi: 10.1111/j.1750-3841.2010.01531.x Further reproduction without permission is prohibited (Chung and others 1998; Cowan 1999; C 20 − C. Red muscadine juices, regardless ◦ Materials and Methods C. sakazakii . Among synthetic organic acids, tannic acid and to identify these antimicrobial substances. sakazakii Red muscadine juice (hot-pressed) donated by the Mississippi Folin & Ciocalteu’s phenol reagent, sodium carbonate and stan- . excellent antioxidant capacity (Pastrana-BonillaLee and others and 2003; Talcott 2004),Mertens-Talcott and anticancer others property 2006), (Yi and(Greenspan and anti-inflammatory and others activity others 2005; Bralley 2005; andesize others that 2007). We red hypoth- muscadine juice,taric and rich malic in acids), phenolic natural acids organicphenolic (tannic compounds acids and and gallic (tar- their acids), derivatives and mayactivity have antimicrobial against Akiyama and others 2001; Kim and others 2008)be and a therefore could good candidate for liquidthe baby pathogen. products The objectives that of potentially this carry research wereantimicrobial to activity investigate of the raw and processed redC muscadine juice on Chemicals and reagents Preparation of juice samples Agricultural and Forestry Experiment Station (MAFES),State Mississippi Univ. was processed from purplesamples grape of cultivar red (Noble). muscadine The tal juice were observations divided in into 50tific 30 mL experimen- Inc.) sterile and centrifuge stored tubes at (Fisher Scien- dards of gallic acidepicatechin (90% (90% purity), purity), ellagic ( acid (95%purity), purity), quercetin myricetin (98% (85% purity), trans-resveratrol (95% purity), malic acid, and tannic acid were purchased from Sigma-Aldrich(St. Inc. Louis, Mo., U.S.A.). Tartaric acid, aceticsulfuric acid, hydrochloric acid, acid, acetonitrile, methanol, andchromatography high-performance (HPLC) liquid grade water wereScientific purchased Inc. (Pittsburgh, from Pa., Fisher U.S.A.). C. sakazakii The concentration of total phenolic compounds of com- has ARSHALL Michx.) juices with natural organic, phenolic acids and polyphenol in juice samples for 2 h at 37 Cronobac- have been D. M C. sakazakii AND , , malic acid, red muscadine juice, tannic acid, tartaric acid C. sakazakii ingredients which could UNG C. sakazakii Cronobacter sakazakii. ) have the ability to toler- Vol. 75, Nr. 3, 2010 , while malic and tartaric acids showed less than 0.5-log reduction. These results sug- — Vitis rotundifolia , Y.S. J ILVA C. sakazakii were shown to have acid resistance is considered an emerging opportunis- Introduction C. sakazakii ,J.L.S Vitis rotundifolia Cronobacter sakazakii Cronobacter sakazakii ENG C. sakazakii . inoculated on infant cereals rapidly grew in infant rice resistance to various organic acids and disinfectants, it M: Food Microbiology and Safety ,W.L.W JOURNAL OF FOOD SCIENCE Keywords: IM ronobacter sakazakii tic pathogen, causing rare but life-threatening meningitis, bac- the same time period (2(tannic h). acid) The showed mixture strong of antimicrobial synthetic activitywas organic against acids undetected (malic in and commercial tartaricreduction) acids) baby against and juices. polyphenolic Tannic acid acidgest showed that the red highest muscadine antimicrobial juicesakazakii activity could (1.4- be to utilized 3.8-log as a natural antimicrobial in baby food formulations to inhibit ABSTRACT: Red muscadine ( of processing methods (filtration, pasteurization, and sterilization), achieved a 6-log reduction of compounds were tested against mercial baby juices rangedtivity, from reducing less 176.7 than to 1-log 347.7 of mg/mL. Commercial baby juices showed poor antimicrobial ac- Muscadine grapes ( 150 Cochran Southern Horticulturalquiries to Lab, authors Poplarville, [email protected]). and MS Silva (E-mails: 39470. [email protected], Direct in- M MS 20090647 Submitted 7/6/2009,and Accepted Silva 1/7/2010. are Authors Kim,tion, with Weng, Mississippi Dept. State of Univ.,with Food Mississippi Dept. Science, of State, Biochemistry Nutrition MS andMississippi and 39762. Molecular State, Biology, Author Health Mississippi MS Jung Promo- State Univ., is 39762. Author Marshall is with USDA-ARS, Thad C Substances in Red Muscadine Juice against T.J. K JFS Identification of Natural Antimicrobial benefits of muscadines hascontent increased (Pastrana-Bonilla due and to others their high 2003; phenolic Yi and others 2005), C. sakazakii is necessary to find novel anti- be formulated in baby foods. ate hot, humid climates,predominant and grape resist species Pierce’s cultivated disease. inStates They the are (Chen southeastern the United and others 2001). Recently, interest in the health Many strains of in acidified tryptic soy brothvalues (pH (3.6 3.5) to and fruit 3.9) juices (Kimothers with 2006; and low Lin Beuchat pH and 2005; Beuchat Edelson-Mammelshown various and 2007). levels In of addition, resistance toon surfaces disinfectants, for which formula are preparation used areas inkitchens, hospitals, and food day-care service centers (Beuchat and others 2009). Due to teremia, and necrotizing enterocolitis in infants (Nazarowec-White and Farber 1997; Laiassociated 2001). with Outbreaks of theper ingestion 100 of g) contaminated infantter formula (less sakazakii (Iversen than and Forsythe 1 2003). or cell oatmeal cereals reconstitutedinfant with formula water, (Richards apple and juice, others milk, 2005; or Lin and Beuchat 2007). M: Food Microbiology & Safety ni sd o trl uc ape eepeae yautoclav- by prepared were samples (121 juice ing sterile Hot used. until ape a itrdtruha0.45 a hydrolyzed through acid filtered the of was tem- supernatant samples room each to min), cooling 15 After (about 2008). perature to others and compounds (Kim phenolic aglycons the make to attached carbohydrates remove to rs.Teraig eercre n xrse as expressed and recorded were readings The prism. reading, 300 each (about before drop water one deionized measure- with the calibration during After refractometer ment. the through circulating water aot25 (about t11 ai vv n lcdi ae ah(95 HCl bath water N a 6 in with placed mixed and were (v/v) samples ratio 1:10 Juice at juices. in phenolics jor Inc., Lomb & (Bauch 20 at 33.46.10 maintained was Temperature Refractometer U.S.A.). N.Y., Rochester, Lomb & Bausch equiv- Spectronic acid gallic juice. a of of milliliter milligrams in per alents as The measured expressed Inc.). were was Scientific phenolics approximately (Fisher total nm spectrophotometer in 765 UV-vis occurred 5 at Genesys which Absorption color, min. de- blue 60 to intense allowed were an samples The velop carbonate. sodium Folin–Ciocalteu and with mixed reagent were water distilled with samples juice diluted Properly 2001). (Waterhouse procedure Folin–Ciocalteu the fslbesld n pH and solids soluble of content the of Determination phenolics total of Determination pasteurization conventional (90 to subjected was juice muscadine Red Anti- oyhnlcadognccompounds organic and polyphenolic major of quantification and Identification 0 ovn ;a 1mn 0 ovn ,1%sletB t3 min, 32 at A, B; solvent solvent 10% 30% A, B; min, solvent 30 solvent 90% at 5% min, B; 31 A, solvent at solvent B; 10% solvent 95% A, 70% solvent min, 90% 0 min, at 1 follows: at separa- as phenolics used for gradient was linear tion A acetonitrile. B: mobile solvent 2 and v/v/v), (10:2:88, The acid/water detector. methanol/acetic A: array solvent diode were phases a with equipped U.S.A.) Clara, Santa Calif., Inc., Technologies (Agilent series 1100 HPLC Agilent an (25 injected 250 and U.S.A.) Mass., Bedford, ae rmjieadprecnetae.Alteepout were products these free. pre- were All preservative as was concentrates. juices labeled juice puree grape and berry juice mixed apple from the and pared and grape concentrate, white juice from The made study. this sam- in juice reference as ples used and U.S.A.) Miss., (Starkville, stores cal samples use. juice until muscadine refrigerator a red in stored filtered were and fresh sterilized thawed Both filtering U.S.A.). by 0.20 made a were through min. juices samples 15 juice for filtered U.S.A.) Tenn., Cold Rockwood, Co., Scientific (National vial h ote,pserzdmsaiejie eesoe at stored were juices overnight, muscadine refrigerator pasteurized a in bottled, cooling the After hermetically. U.S.A.), N.Y., sealed Corning, and Inc., (Corning into bottles filled media and Univ., Pyrex State sterilized Mississippi Promotion, Health Ammerman- and Nutri- the tion Science, Food in of kettle Dept. steam Laboratory, Processing open Hearnsberger an in stirring constant with h Hvle fjie eemaue tro temperature room at measured were juices of values pH The eesdpaeHL a sdt eaaeadqatf ma- quantify and separate to used was HPLC Reversed-phase a using measured was solids soluble of concentration The to according phenolics total for analyzed were samples Juice he ye fcmeca ayjie eeprhsdfo lo- from purchased were juices baby commercial of types Three ◦ × ,1mn Mnvleadohr 05 Cort 2005; others and (Montville min) 1 C, rnbce sakazakii Cronobacter . mclm Peoee n. orne ai. ... in U.S.A.) Calif., Torrance, Inc., (Phenomenex column mm 4.6 ◦ ◦ ,134ka h hwdfehjiei screw-capped a in juice fresh thawed the kPa) 103.4 C, )wt onn ince50p ee (Switzerland). meter pH 530 Pinnacle Corning a with C) μ μ )o uc apewspae nteglass the on placed was sample juice of L) yig itr(ilpr,Bdod Mass., Bedford, (Millipore, filter syringe m usacsi e ucdn uc . . . juice muscadine red in substances μ yig itr(Millipore, filter syringe m μ )it eiiC18, Gemini a into L) sadohr 2008) others and es ´ ± ◦ Brix. 5 ◦ )fr1h 1 for C) ◦ − Cwith 20 ◦ C t10rmfr1 t37 at h 16 for shaking with rpm U.S.A.) 150 Md., Sparks, at tryp- Dickinson, in (Becton cultured broth separately soy a were tic on strains The stored slant. were agar cells soy Reactivated tryptic broth. by soy reactivated tryptic and in thawed subculture were cultures The glycerol. 10% taining iid ae ntertnintm n ekae fec standard, each of area peak and respectively. time retention the on based quan- tified, and identified (Agilent was software compound ChemStation Individual were Inc.). Technologies the acids detected using organic were analyzed and acids compounds and phenolic organic integrated for Individual Peaks mL/min. nm. 215 1 at of rate flow a o ikno)atricbto t37 at incubation Viable after control. Dickinson) ton a as used was sakazakii 3.2) acid (pH broth hydrochloric soy Tryptic with min. 120 acidified to up for min, 30 every recorded tc utrswr ananda –65 at maintained were respectively. cultures U.S.A., Health, Stock of others Dept. State and Mississippi the (Zogaj and 2003) Sweden) Center, Tumorbiology and R Ute crobiology Dr. by isolated clinically were strains These study. l o hi niatra ciiy oa oul ois( solids soluble total activity, antibacterial their for ble difference significant and least ( model, protected Fisher’s linear by general separated PROC (except means by design analyzed randomized were completely solids) a soluble in replications 3 least at from obtained facto- Data activity. antimicrobial one-way (treatments of measurement a arrangement for used factorial using 2-way analyzed a were while samples rial, juice the of acids 16 were make glucose to acid, and added fructose then tartaric and first water, were mg/mL; deionized mixture sterile their 1.27 in and prepared mg/mL) acid, 1.71 acid, (malic tannic mg/mL; juice 3.37 muscadine red in h itr a nuae t37 at 2006). others incubated and was (Lekkas mixture CFU/mL create 6.5-log The to about juice of muscadine population red a pasteurized to added and were filtered, cultures sterilized, bacterial the incubation, After U.S.A.). N.J., eoeyo el fe nuain ncltdsmls(100 samples inoculated incubation, h 2 after cells of recovery ciiiswr esrda ecie above. described as measured were activities n omrilbb juices baby commercial and muscadine red of activity Antimicrobial n omrilbb juices baby commercial and muscadine red in polyphenols and organic, phenolics, total pH, solids, Soluble analysis Statistical juice muscadine red in found acids organic synthetic of activity Antibacterial eetaserdt S vr 4h pt 2hadte incubated then and h 72 h. to 24 up for h, TSA on 24 every TSB to transferred were ytma ecie bv.Mbl hs a .1NH N 0.01 was phase HPLC Mobile a above. into described injected and as filtered system was supernatant each and min, 5 PC uc ape eecnrfgda 20 p (1700 rpm 12000 at using centrifuged by were quantified samples and Juice separated HPLC. similarly also were or- was Major rate acids nm. flow 260 ganic The at run. detected post were phenolics min Individual 5 mL/min. with 1 B solvent 5% A, solvent 95% P w tan of strains Two ic rai usacsi ri eeae ol eresponsi- be could beverages fruit in substances organic Since organic and compounds, phenolic phenolics, total pH, for Data found concentrations the at solutions acid synthetic Individual < .5 sn A . SSIs. ay .. U.S.A.). N.C., Cary, Inst., (SAS 9.1 SAS using 0.05) o.7,N.3 2010 3, Nr. 75, Vol. eeeueae ntytcsyaa TA lts(Bec- plates (TSA) agar soy tryptic on enumerated were .sakazakii C. ◦ rxfrec ouin hi antimicrobial Their solution. each for Brix — ◦ IcbtrSae,NwBrunswick, New Shaker, (Incubator C Results ORA FFO SCIENCE FOOD OF JOURNAL e3 n SHwr sdi this in used were MSDH and Fec39 ◦ ,adteval el were cells viable the and C, ◦ ◦ o 8t 4h oseany see To h. 24 to 18 for C ntytcsybohcon- broth soy tryptic in C × mig(Mi- omling ¨ ◦ 2 ie was time) rx,pH, Brix), SO 4 g M with )for 151 μ C. L)

M: Food Microbiology & Safety b b 71a 90a 83a 41b . . . . 9b 3ab 4a 6b 7a . . . . . (Kim and oth- 27a 1 60a 1 62b ND 78a 1 87c ND 48a 1 45a ND ...... 8a 0 10b ND 6a 1 93a 0 4a 0 4a 1 05ab ND ...... activity on both strains. sakazakii strains within 1.5 h. Pre- . C (mg/mL) 37b 1 99d 3 27a 1 48a 1 67c 2 65a 1 67d 4 ...... 1a 3 70a 2 5b 4 63a 6 4a 4 9ab 4 56a 5 sakazakii C (Figure 2A and 2B). The mixed ...... ◦ . sakazakii C . C Discussion activity was determined in tartaric (3.37 activity of synthetic 4a 3 7a 0 4a 4 6a 4 7c 1 9a 4 7b 0 ...... 4a 1 17b 0 1a 0 20b 0 5a 1 0a 0 60b 0 ...... activity (data not shown). This result implies that 338 (mg/100 mL) sakazakii . Brix), equivalent to concentration in red muscadine juice ◦ C sakazakii a . C. sakazakii 7a 24 2a 3 7a 29 5c 2 6a 25 9a 24 5a 2 C ...... he red muscadine juice contained tartaric(1.27 mg/mL), (3.4 tannic mg/mL), acids malic (1.71 mg/mL) as polar compounds 29b 347 16b 16b 319 19ab 321 51a 176 22a 322 47a 210 ...... Regardless of treatment, the red muscadine juices inactivated Anti- (Table 1) and gallic acid (0.2catechin mg/mL), (0.54 catechin mg/mL), (0.54 ellagic mg/mL), acid epi- mg/mL), (0.24 mg/mL), resveratrol myricetin (0.04 (0.01 mg/mL),as and nonpolar compounds quercetin (Table (0.01red 2). muscadine mg/mL) These juice organic were also components foundtracts in in of the “Ison” water-soluble seed (red) ex- taric and (6.6 “Carlos” to (bronze) 7.27 which mg/mL),to contained malic 7.1 tar- (1.33 mg/mL), to ellagic 1.870.35 (0.02 mg/mL), mg/mL), catechin tannic to (0.07 (4.3 0.17 to 0.18 mg/mL),to mg/mL), 0.1 and gallic mg/mL) epicatechin acids (Kim (0.05 and (0.11 others 2008, to 2009a, 2009b). more than 5-log cells of 2 Anti- T (Table 1). The pH of all syntheticThe acid initial solutions was number adjusted of to cells 3.2. imately inoculated 7.5-log in the CFU/mL solution at was 37 approx- mg/mL), malic (1.27 mg/mL),mixture tannic of acid these compounds (1.71 (MXA) with mg/mL), fructoseture and and (16 glucose the mix- acid, MXA solution (Figure 2) wasany of not the as juice effective treatments antimicrobial (Figurenic as 2). acid Among showed synthetic highest acids, anti- tan- Polyphenol fractions (polyphenols and pigments) did notanti- show any tannic acid in muscadine juices isterial activity. the key component for antibac- ers 2009b). When whole muscadine grapes arepressed, heated, water-soluble crushed antimicrobial and components from muscadine vious studies showed that water-solubleinactivated muscadine 5-log seed cells extracts of 2 strains of acids found in red muscadine juice C. 0.05). 0.05). < < 0a 53 7a 46 4a 50 7a 14 0b 47 2b 43 5a 46 ...... P P Brix) pH phenolics acid acid acid ◦ 83 33 23 43 43 03 43 ...... 54 Brix, com- C. sakaza- C. sakaza- ◦ strains: there Soluble Total Tartaric Malic Tannic a a Brix) depending on 7ab 29 6 1a 53 8a 26 2ab 43 0b 43 7b 32 ◦ ...... within 2 h (Figure 1C sakazakii . C Vol. 75, Nr. 3, 2010 — substances in red muscadine juice . . . was measured by the aerobic C. sakazakii C. sakazakii Mixed berry 15 Filtration 16 Sterilization 15 White grape 17 Pasteurization 16 Mixed berry 19 Filtration 21 White grape 22 Sterilization 20 Pasteurization 18 C. sakazakii strains Fec39 and MSDH to either red muscadine or commercial JOURNAL OF FOOD SCIENCE not detected. not detected. Cronobacter sakazakii 0.05) in tartaric acid than commercial baby juices (Table 1). = = cells showed a lag trend in the first 0.5 h, there was about a 6- were reduced to nondetectable levels in all red muscadine juices < The antimicrobial activity of red muscadine and commercial 152 Means of muscadine orND baby juices followed by a different letter differ ( Means of muscadine orND baby juices followed by a different letter differ ( P was less than 1.0-log reduction of and 1D). Among the 3demonstrated commercial slightly baby better juices, antimicrobial mixedgrape berry juices. effect There juice than were no apple differences in and susceptibility between sakazakii baby juices. Juice type Treatment solids ( a b M JuiceRed muscadine juice Fresh Treatment 21 Gallic acid Catechin Epicatechin Ellagic acid Myricetin Resveratrol Quercetin a b Table 2 --- Major phenolic compounds in red muscadine and commercial baby juices. Red muscadine juice Fresh 16 Table 1 --- Solublejuices. solids, pH, total phenolics, organic and phenolic acids in red muscadine and commercial baby Antimicrobial activity of red muscadine and commercial baby juices on Anti- organic and phenolic acids, and majormuscadine phenolic compounds and in red commercial babyHPLC juices and were the results measured were by shownble in using solids Table of 1 red muscadine and juices 2. was approximately While 16 the solu- mercial baby juices showed varied (13.4 to 17.4 plate count method on TSA.kii Within 2 h, both strains(Figure of 1A and 1B). Evenkii though the decrease in viable log reduction in cell number in 1.5of h, regardless red of muscadine processing types juice (Figurebaby juices 1A were and not 1B). inhibitory However, on commercial the 2 juices against 2 the products (Table 1). Overall,( red muscadine juices were higher Tannic acid was the major phenolic acid in allwhile red commercial muscadine baby juices, juices did not containRed tannic acid muscadine (Table juices 1). and commercialthe highest mixed content berry of juice total phenolics,ple showed followed grape juice by and commercial then ap- white grape juicejor (Table phenolic 1). compounds Among detected, the ellagic ma- acid (0.3 mg/mL)11 was 7 times to higher in redjuices muscadine (Table juices 2). than Regardless in of commercialgallic baby treatment acid, of catechin, red epicatechin, muscadine ellagicnot juices, differ acid, in and their concentration. resveratrol did Commercial baby juices Apple grape 13 Commercial baby juice Apple grape 17 M: Food Microbiology & Safety opud uha ai,trai,adtni cd hwdan- of showed strains acids 3 tannic on and polar activity of tartaric, timicrobial mixture malic, In the as extracts. only seed such that in compounds demonstrated than we juice study, muscadine previous red a tartaric, in malic, of acids concentration tannic lower and the to seed due to be compared pe- as could juices time extracts the same of muscadine the activities red in antimicrobial cells Low whereas riod. 2-log 2009b), than others less inactivated and (Noble) (Kim juice h 0.5 within els of cells of CFU/mL) extracts sakazakii 6-log seed (approximately Ison number hot the The reduced However, juices. an- the of explain activity might which timicrobial juice, their into released be might seed Anti- hi itr nasgr(6Bi ihguoeadfuts)slto.Cnrlwstytcsybohajse opH to adjusted broth soy tryptic was Control solution. fructose) and glucose with Brix (16 sugar a 3.2. in mixture their of --- Inhibition 2 Figure of cells --- Viable 1 Figure RJ A )adcmeca ayjie C ) oto a rpi o rt dutdt H3.2. pH to adjusted broth soy tryptic was Control D). (C, juices baby commercial and B) (A, (RMJ)

log CFU/mL Log CFU/mL Log CFU/mL 1 2 3 4 5 6 7 rnbce sakazakii Cronobacter 0 1 2 3 4 5 6 7 2 3 4 5 6 1 7 0 0 0 e3 and Fec39 control acid tartaric mixed acid malic acid tannic acid C 0.5 0.5 . 0.5 sakazakii rnbce sakazakii Cronobacter rnbce sakazakii Cronobacter A A Time (h) SHt eryudtcal lev- undetectable nearly to MSDH Time (h) C Time (h) shrci coli Escherichia 1 1 usacsi e ucdn uc . . . juice muscadine red in substances 1 Control White grape juice Mixed Juice berries Apple grape juice Control Filtered RMJ SterilizedRMJ Pasteurized RMJ 1.5 1.5 17H (Kim O157:H7 1.5 e3 A and (A) Fec39 e3 A )and C) (A, Fec39 2 C. 2 eaiebcei;wihsoe esai aaet N and DNA to damage acid less showed which bacteria; Gram in negative tolerance acid marked induced mecha- rapidly glucose homeostatic where pH nism a explained (1998) Goodson and Rowbury ue h rsneo uasi ytei cdslto retarded solution acid on synthetic activity in antimicrobial sugars their of presence showed The juice the ture. muscadine that in showed anti- sugars higher and also much acids 2009a) Our natural period. others of time and presence same (Kim the findings in previous CFU/mL) all (6.5-log inactivated cells juice muscadine inoculated red respectively, on h, 2 cells within acids 3.9-log MSDH and and sugars 3.8- artificial of only mixture inactivated the While 2009a). others and 2 .sakazakii C. log CFU/mL Log CFU/mL 3 4 5 7 2 6 1 Log CFU/mL 7 0 1 2 3 5 6 4 0 1 2 3 4 5 7 6 .sakazakii C. 0 0 o.7,N.3 2010 3, Nr. 75, Vol. mixed acid control tannic acid acid tartaric malic acid SH()b niiulsnhtcaisand acids synthetic individual by (B) MSDH E 0.5 . coli 0.5 0.5 SH(,D nrdmsaiejuices muscadine red in D) (B, MSDH 17H ciiyta hi ytei mix- synthetic their than activity O157:H7 — B ORA FFO SCIENCE FOOD OF JOURNAL B D Time (h) Time (h) Time (h) E . 1 1 1 coli 17H and O157:H7 C . Control Pasteurized RMJ Filtered RMJ Sterilized RMJ sakazakii 1.5 1.5 Mixed juice berries Control White grape juice Apple grape juice 1.5 C . e3 and Fec39 sakazakii 2 2 M 2 153 . M: Food Microbiology & Safety in infant O157:H7. Vitis rotun- on fresh-cut Enterobacter C. Food Microbiol Cytophaga colum- ◦ :areview.IntJFoodMi- sakazakii, an emergent and potential surrogates. Escherichia coli isolated form the human gas- Enterobacter sakazakii Enterobacter sakazakii Enterobacter ıgola A. 2008. Total antioxidant capacity ´ Bacillus anthracis Enterobacter sakazakii infections among neonates, infants, children, O157:H7. J Food Prot 71:1465–8. and its reversal by cyclic AMP. J Appl Microbiol , and the impact of habituating the cells to an ´ alez R, Fr Enterobacteriaceae coli by Water-Soluble Muscadine Seed Extracts. Int J Food . ¨ omling U. 2003. Production of cellulose and curli fim- E in galotyri cheese stored at 4 and 12 ). J Agric Food Chem 54:5336–43. . Microbiol Immunol 48:251–61. Escherichia coli Enterobacter sakazakii Escherichia coli Enterobacter sakazakii in infant rice cereal reconstituted with water, milk, liquid infant formula, Vitis rotundifolia Enterobacter sakazakii ). J Agric Food Chem 53:8481–4. . J Aquat Anim Health 9:309–13. ´ es C, Barba F, Esteve MJ, Gonz fruits and vegetables andture. in J unpasteurized Food Prot juices 68:2541–33. as affected by storage tempera- muscadine seed extracts on cadine juice and theJ role Appl Microbiol of 107:533–9. their polar compounds on tion of Microbiol 129:3295–99. and adults. Case reports and a review of the literature. Medicinederivatives 80:113–22. and other antioxidant polyphenolics inChem muscadine 52:361–6. grapes. J Agric Food Survival of pathogen associated with infant54. milk formula. Trends Food Sci Technol 14:443– 23:268–76. cereal as affected by composition,J reconstitution Food liquid, Prot 70:1410–22. and storage temperature. caco-2 human colon carcinoma cells bygrapes ellagic ( acid rich fractions form muscadine H. 1992. Inhibitory effectcytopathic of effect, tannic and giant acid cell sulfate formationMed and of 58:535–9. human related imunodeficiency sulfates virus. on Planta infectivity, tance of sproes form virulent strainsJ of Food Prot 68:2362–6. crobiol 34:103–13. tioxidant capacity of muscadine grapes. J Agric Food Chem 51:5497–503. sakazakii or apple juice. J Appl Microbiol 99:844–50. pH in log-phasse 85:615–20. rent protocols in food Analytical8. chemistry. N.Y.: John Wiley & Sons, Inc. p I1.1.1– nolics in vitro. J Agric Food Chem 53:8804–12. tannic acid and related compounds against the fish pathogen naris Soc Exp Biol Med 67:483–8. Hartle DK. 2005. Antiinflammatory properties ofdifolia the muscadine grape ( rick DG, editors. Muscadine grapes. Alexandria, Va.: ASHS Press. p 206–8. borne bacteria by tannic acid, propylcrobiol gallate 17:29–32. and related compounds. Lett Appl Mi- lated compounds on the growth of60. intestinal bacteria. Food Chem Toxicol 36:1053– of refrigerated orange juice treated with pulsed electric fields. Proc Nutr Soc 67:E34. 12:564–82. strains of acidic environment. J Food Sci 71:m201–207. tibacterial activity of hydrolyzableHelicobacter tannins pylori derived form medicinal plants against briae by members oftrointestinal the tract. family Infect Immun 71:4151–8. Kim TJ, Weng WL, Stojanovic J, Lu Y,Kim Jung TJ, YS, Silva JL, Silva Jung JL. YS. 2009a. 2008. Antibacterial Antimicrobial activity effect of fresh of and processed red mus- Kim TJ, Silva JL, Weng WL, Chen WW, Corbitt M, Jung YS, ChenLai YS. 2009b. KK. Inactiva- 2001. Lee JH, Talcott ST. 2004. Fruit maturity and juice extraction influencesLekkas ellagic D, acid Kakouri A, Paleologos E, Voutsinas LP, Kontominas MG, Samelis J. 2006. Kim H, Beuchat LR. 2005. Survival and growth of Lin LC, Beuchat LR. 2007. Survival and growth of Mertens-Talcott SU, Lee JH, Percival SS, Talcott ST. 2006. Induction of cellMizumo death T, in Uchino K, Toukairin T, Tanabe A, Nakashima H, Yamamoto N, Ogawara Montville TJ, Dengrove R, Siano TD, Bonnet M, Schaffner DW. 2005. ThermalNazarowec-White resis- M, Farber JM. 1997. Pastrana-Bonilla E, Akoh CC, Sellappan S, Krewer G. 2003. PhenolicRichards content GM, and an- Gurtler JB, Beuchat LR. 2005. Survival and growth of Rowbury RJ, Goodson M. 1998. Glucose-induced acid tolerance appearing at neutral Waterhouse AL. 2001. Determination of total phenolics. In Wrolstad RE, editor. Cur- Yi W, Fischer J, Akoh CC. 2005. Study of anticancer activities ofZhao muscadine G, grape Chung phe- KT, Milow K, Wang W, Stevens Jr SE. 1997. Antibacterial properties of Zogaj X, Bokranz W, Nimtz M, R Green RH. 1948. Inhibition of multiplication of influenzae virusGreenspan by P, tannic Bauer acid. JD, Proc Pollock SH, Gangemi JD, Mayer EP, Ghaffar A,Iversen Hargrove JL, C, Forsythe S. 2003. Risk profile of Chen J, Copes WE, Miller RW, Lamikanra O. 2001.Chung Diseases. In KT, Basiouny Stevens FM, Jr Himel- SE, Lin WL, Wei CI. 1993. Growth inhibitionChung of KT, selected Lu food- Z, Chou MW. 1998. Mechanism of inhibitionCort of tannic acid and re- Cowan MM. 1999. Plant productsEdelson-Mammel S, as Buchanan antimicrobial RL, agents. Porteous MK. Clin 2006. Microbiol AcidFunatogawa Rev resistance K, Hayashi S, of Shimomura H, twelve Yoshida T, Hatano T, Ito H, Hirai Y. 2004. An- ac- Cy- and .Tryptic .Thisre- sakazakii Cronobacter . (Chung and C sakazakii . C Klebsiella pneu- , C. sakazakii showed less than a 0.5- inhibitor. E. coli have been reported as a Enterobacteriacea Vol. 75, Nr. 3, 2010 Aeromonas hydrophila — substances in red muscadine juice . . . . J Antimicrobiol Chemother 48:487–91. sakazakii . (Funatogawa and others 2004), C C. sakazakii activity of the muscadine juices. Data (muscadine) berry seeds and skins. Pharm Biol References Conclusions Acknowledgments (Zhao and others 1997), HIV viruses (Mizumo sakazakii (Chung and others 1998), Staphylococcus aureus . Cronobacter sakazakii C Helicobacter pylori (Kim and Beuchat 2005; Lin and Beuchat 2007). All the Vitis rotundifolia in foods and factors affecting its survival, growth, and inactivation. Int Listeria monocytogenes, Staphylococcus aureus JOURNAL OF FOOD SCIENCE , Cronobacter sakazakii n conclusion, red muscadineacids juice, and a organic rich acids, including source the of important phenolic tannic acid, sakazakii J Food Microbiol doi:10.1016/j.ijfoodmicro.2009.02.029. activity by 45:667–73. related compounds. J Bacteriol 66:572–5. eral tannins against 154 Bralley E, Hartle DK, Hargrove JL, Greenspan P. 2007. InhibitionCarson RS, of Frisch hyaluronidase AW. 1953. The inactivation of influenzae viruses by tannic acid and Beuchat LR, Kim H, Gurtler JB, Lin LC, Ryu JH, Richards GM. 2009. sult suggests that red muscadine juice mayused have in the baby potential foods to as be a natural showed strong antimicrobial action against M Akiyama H, Fujii K, Yamasaki O, Oono T, Iwatsuki K. 2001. Antibacterial action of sev- Approved for publication as Journalsissippi Article Agricultural Nr J-11694 and of Forestry the ExperimentState Mis- Station, Univ. Mississippi This researchsippi Agricultural was and Forestry supported Experiment Station in371272 Project and Nr by part MIS- USDA-ARS Grant by Nr 58-6402-6-075. the Missis- showed that regardless of their pH (3.2 to(sterilization, 3.8) or filtration, processing method and sothe on), most tannic active antimicrobial acid compound (1.7pounds, among mg/mL) the showing was 3 approximately polar 4-log com- reduction on I soy broth (pH 3.2) acidified with hydrochloric acidreduction did not of show any cells (Figureobserved 1). that 10 Edelson-Mammel of and 12 strains others of log (2006) reduction in tryptic soyacid. broth at Predominant pH organic 3.5, acids adjustedand (citric hydrochloric strawberry and juices malic with acids) lowtivate pH in low values apple (3.6 inoculum to numbers 3.9) (approximatelyC. did 1.5-log sakazakii not CFU/mL) inac- of commercial baby juices tested insame this levels study of contained organic acids almostjuices, and the but phenolic did acids not as have reddid not tannic muscadine contain acid. tannic acid Commercial showed baby muchtivity, juices less suggesting anti- that that tannic acidblefortheanti- is the key component responsi- within 2 h (Figurecrobial 2). activity Previous of studies tannic have acid reported against the antimi- moderately acid resistant member of the Anti- ß-galactosidase. others 1993), and others 1992),Frisch and 1953). The influenza antimicrobial mechanism virus of tannicbe (Green acid totally seems 1948; to different from Carson theIt and antimicrobial may action work of organic like acids. medium a and siderophore make iron to unavailable to chelate theand essential microorganisms others (Chung 1998). iron from the tophaga columnaris Aeromonas sobria moniae M: Food Microbiology & Safety