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Home , Brucella agar, Oregano

ie n sntue o omrilpurposes. commercial for used not is and cited odaewt eerhSrie AMdclCne etLsAgls o Angeles, Los [email protected]). Angeles, (E-mail: Los Li West author Center to inquiries Medical Fine- VA Direct U.S.A. and Service, CA, Summanen Research Authors U.S.A. with CA, are David Angeles, Nutrition, gold Los Human Medicine, for of Center School UCLA with Geffen are Li and Heber, Henning, Huang, ac fdfeetbceilgop ihntegtmcoit by microbiota gut the abun- within relative groups the bacterial influence different juices, of fruit dance and tea, fruits, particularly cocoa, sources, wine, dietary -rich A or 2016). Backhed and recent diabetes, (Sonnenburg of 2 diet number type to including linked intimately diseases, are metabolic associated Obe- and health. human sity affects ultimately that composition microbial crobia and bacte- categories abundance include lower phylogenetic ria Other known microbiota. gut of distal 90% the dominate than more up make phylum Most the and humans. to in belong microbiota ing bacteria complex intestinal and of abundant most the o:10.1111/1750-3841.13792 doi: Introduction Finegold, M. Sydney Heber, David Henning, M. Susanne Huang, Li Jianjun Zhaoping Lee, and Ru-Po Summanen, H. Paula Lu, Qing-Yi Extracts Culinary Seven of Composition Chemical and Potential Prebiotic hsi noe cesatceudrtetrso the of terms the under article access open an is This FS21-11Sbitd12/07 cetd52/07 uhr u Lee, Lu, Authors 5/27/2017. Accepted 1/25/2017, Submitted JFDS-2017-0151 C 07TeAuthors. The 2017 h atonetnltat seilytelreitsie houses intestine, large the especially tract, gastrointestinal The irboaadhs eaoimaddsaepeetv feti nmlmdl n uasi needed. is humans and gut models in animal changes on in spice-induced chemicals effect between preventive these connections disease of the and on influence metabolism research potential host Future and the activities. identification microbiota and into The communities insight health. microbial gastrointestinal provided gut of phytochemicals enhancement the spice-specific the their and suggesting of microbiota bacteria, quantification intestinal pathogenic of and of growth regulation the the suppressing in and role bacteria potential beneficial selected of growth against the active promoting were by activity and , , and selected against rcia Application: Practical Keywords: Abstract: td ntecnetosbtensieidcdcagsi u irboaadhs eaoimaddsaepreventive disease and further metabolism for host basis and a humans. microbiota provide and gut results models in These the animal changes promoting bacteria. in spice-induced by pathogenic effect between activity of connections prebiotic-like growth displayed the the on suppressing Some study and chemicals. bacteria major beneficial of of amount growth total the with correlated that ihatoiatcpct htcreae ihtettlaon fmjrceias l pc xrcs ihteexception the with exhibited extracts, spice extracts of All phenolic intestinal growth Spice chemicals. 14 major from quantitated. the of of isolates and enhanced total amount facultative total A identified turmeric, the extracts. and were with of of anaerobic correlated dilutions that and 88 capacity serial acid, of antioxidant containing high cinnamic viability plates , the agar a Brucella on compounds, using extracts by scavenge spice to determined by of extent were the characterized microbiota Effects were colorimetrically cations. constituents measuring by chemical radical determined Major ABTS was water. capacity boiling antioxidant with and Mediterranean , method extracted RP-HPLC-DAD cinnamon, were pepper, cayenne turmeric pepper, black and including rosemary, spices oregano, culinary Seven extracts. spice of capacity Clostridium Bacteroidetes iti n fteipratfcoscnrbtn otegut the to contributing factors important the of one is Diet . , Bifidobacterium h betv fti td a oivsiaepeitcptnil hmclcmoiin n antioxidant and composition, chemical potential, prebiotic investigate to was study this of objective The (including nvitro in ora fFo Science Food of Journal Ruminococcus , , Fusobacteria nvivo in Prevotella , hsrsac hw htauosetato uiaysieehbtdhg nixdn capacity antioxidant high exhibited spice culinary of extract aqueous that shows research This netnlbacteria, intestinal , n ua tde hwdthat showed studies human and , raieCmosAttribution-NonCommercial Commons Creative pce.Cnao,oeao n oeaywr cieaantselected against active were rosemary and oregano, Cinnamon, species. and , Proteobacteria, ulse yWlyProias n.o eafo nttt fFo Technologists. Food of Institute of behalf on Inc. Periodicals, Wiley by published ,and Bacteroides Bifidobacterium Ruminococcus eea,which genera), Lactobacillus and Verrucomi- (includ- genera) p.and spp. iiu niioycnetain spice concentration, inhibitory minimum , ies,wihprisue itiuinadrpouto naymdu,poie h rgnlwr sproperly is work original the provided medium, any in reproduction and distribution use, permits which License, ixdn aaiyta orltdwt oa hnlccnetbut content an- phenolic significant total exhibited with form correlated fresh that that capacity or im- tioxidant reported dry study and in Subsequent spices volunteers, b). 2 commercial 2010a, Type healthy others with and of men (Li in urine diabetes dysfunction the and concen- endothelial in the plasma postprandial marker, proved in in peroxidation reduction and lipid a a meat mix in malondialdehyde, spice resulted of with cooking tration meat to hamburger group prior our of added from consumption research respectively that 5, Previous and reported 2006). 4, gin- others 50 3, oregano, and #2, the them, ranked (Halvorsen Among turmeric of and spices. that cinnamon, were ger, reported 13 1113 among samples, was concentrations food prop- It antioxidant U.S. in antioxidant foods. highest strong products most their food exceed and for Sanlier disease, that known and Kocaadam heart best erties 2017; cancer, are others of They and risk 2017). Bi the 2003; reduce (Surh to diabetes known activities, are functions antimutagenic purposes, and preventive antiinflammatory, medicinal disease antimicrobial, for demonstrated as also of such but number a foods have of and for only used not been have Spices phytochemicals. spice-specific contain often 2015). others gram- and (Duenas certain lactobacilli and pathogens potential negative of numbers the reducing pcsaedrvdfo ak ri,ses rlae fpat and of leaves or seeds, fruit, bark, from derived are Spices Lactobacillus Clostridium Bacteroides o.8,N.8 2017 8, Nr. 82, Vol. p.Alsie xiie niioyactivity inhibitory exhibited spices All spp. p.adehnebnfiilbfioatraand bifidobacteria beneficial enhance and spp. p.Sm pcsdslydprebiotic-like displayed spices Some spp. r ora fFo Science Food of Journal Fusobacterium strains 1807

Food Chemistry L for µ g C. The × ° -azinobis 150 mm, type strains ,2 × species consist- 20 mm, Phenomenex, Bifidobacterium × Lactobacillus m, 4.6 4.6 mm) column with same mobile L of the supernatant was injected µ µ × type strains were studied. Other bacterial g/mL. Lithospermic acid in ORE was charac- species consisting of 11 strains recovered from µ solution in 96-well plates. Absorbance was read at Lactobacillus ·+ m; Agilent, Santa Clare, Calif., U.S.A.) connected to a dis- µ Bifidobacterium Eighty-eight strains of bacteria included in this study were clin- Trolox equivalent antioxidant capacity (TEAC) was deter- After mixing well, an aliquot of 1.0 mL of aqueous extract was human intestinal contents and 6were ATCC studied. Similarly, 16ing strains of of 124ATCC strains recovered from human intestinal contents and 10 min. Aninto aliquot HPLC. The of quantification 25 offormed phenolic in compounds a was per- array 2690 Waters detector HPLC and system3.5 a equipped Zorbax with SB a C18 diode column (4.6 ical isolates from patientscare in Center the as Greater published Los (LiAmerican and Angeles Type others Culture VA Collection 2015a), Health- (ATCC). or Altogether purchased 17of from strains mined by measuring the ability to scavenge 2 mixed with 1.0 mLwas of then dimethyl sulfoxide. vortexed The for resulting 5 mixture min and centrifuged at 20600 posable pre-column (C18, 5 Trolox equivalent antioxidant capacity Bacterial strains, growth stimulation, and inhibition tests Identification and quantification of phenolic compounds 750 nm after 30lar min Devices, in Sunnyvale, Calif., a U.S.A.).trolox VersaMax Final equivalent microplate value (TE). reader is (Molecu- expressed as (3-ethylbenzothiazline-6-sulfonic acid (ABTS) radical cationduced pro- by the oxidation ofviously ABTS described with manganese (Lu dioxidecations as and were pre- prepared by others addingto solid 2015). manganese a Briefly, dioxide (80 5 ABTS mg) (20 mM radical mL using aqueous a 75 stock mMTrolox sodium/potassium solution (6-hydroxy-2, [Na/K] 5, buffer of of 7, pH ABTSacid) 7). 8-tetramethyl-chroman-2-carboxylic diammonium was used asin an Na/K antioxidant buffer, and standard. the Extract resultingof was solution was 1st ABTS mixed diluted with 200 nal calibration curves. Stock solutionsprepared of in reference the standards were concentrationcalibration solutions of were prepared by 1.00 diluting stock mg/mL50% solutions with aqueous in methanol. methanol For and allear calibration relationships between curves, peak there area were andof lin- concentration 0.7825 in the to range 100 Torrance, Calif., U.S.A.) withmobile temperature phase consisted held of at 0.1%100% acetonitrile phosphoric 30 (B). acid A linear in gradient2% water was (A) B performed and with increasing initial to25 25% to B 32 in40 min, 25 to to min, 50 50% andmatograms min. then B were to The from recorded 40% flow 32GIN, at B rate to 310 280 from was 40 nm nm 0.75 minnm for for mL/min and for GIN, CAP, and TUR. 70% BLP, 330 Chemicals CIN, the BPhenomenex from nm and Prodigy chro- from ROS (250 for extract were OREphase, analyzed and using flow ROS, rate, and andgradient. 425 column Chemical temperature identification but forby each slightly comparing spice modified peak was retentionto determined time those and UV fromchemicals absorption reference from spectrum standard. each The spice concentrations extract were of determined major using exter- terized based on theand published others UV 2009) absorption andthe maxima its calibration (Grevsen concentration curve of was rosmarinic determined acid. by using C. ° Lac- , E. coli 20 Bacillus Bacillus , − Staphylococ- groups and re- Klebsiella pneu- ana- 0157:H7, and spp., and established ,and ,and group in the caecum counts in mouse cecal g/mL; Shan and oth- Lactobacillus reuteri µ g/mL (Gunes and others Enterococcus faecalis E. coli E. coli , µ , , g/mL as compared to crude 2500 µ Lactobacillus Vol. 82, Nr. 8, 2017 > r Escherichia coli Bacteroides/Prevotella S. aureus , S. aureus Bifidobacterium , spp. and and effect of 7 spice extracts on the growth of 33 Bifidobacterium lactis , in vitro Lactobacillus Bifidobacterium Lactobacillus/Leuconostoc/Pediococcus , methicillin-resistant -coumaric acid, bisdemethoxycurcumin, demethoxycur- Journal of Food Science Listeria monocytogenes p ) is in the range of 129 to 293 , , ) with MIC being 125 to 500 Seven culinary spice samples, (BLP), cayenne All organic solvents were High-performance liquid chromatog- There is limited amount of information regarding the activity of The concentration of each aqueousper extract milliliter was after 182 adjusting mgwas dry for used spice final directly volume forantioxidant of activity. chemical 38.5 analysis mL, and which the measurement of LF82) than the organic extracts (Sutherland andcooling others 2009). down, After approximately 38.5lected mL after of centrifuging supernatants and were filtration, and col- then stored at by refluxing 7 g ofMilli-Q dry water spice for powder 30 in min. 70 Aqueousbe mL food more (or extracts effective 100 were on reported mg/mL) the to of culturedtobacillus bacteria rhamnosus ( pepper (CAP), cinnamonoregano (CIN), ginger (ORE), (GIN), rosemaryCormick Mediterranean (ROS), Company, and Inc., Sparks, turmeric Md., (TUR; U.S.A.) Mc- were extracted (St. Louis, Mo., U.S.A.).(Rockville, Md., Ferulic U.S.A.) and acid 6- from was ChromadexCalif., (Irvine, purchased U.S.A.). They from were USP tification used of for spice the chemicals. identification and quan- genin, , ,hyde, cinnamic acid,, cinnamalde- , luteolin, luteolin-3-glucuronide, piperine,marinic ros- acid, and were purchased from Sigma-Aldrich raphy (HPLC) gradeU.S.A.). (Thermo Deionized Fisher water Scientific,(Millipore, Fairlawn, was N.J., Bedford, purified Mass., by the U.S.A.). Reference Milli-Q system standards api- 1808 Spice samples and extract preparation Materials and Methods Reagent and chemicals erties against 5 commoncereus foodborne pathogenic bacteria ( subtilis moniae 2016a). Cinnamaldehyde, awas bioactive component shown of to cinnamon, exhibit more potent in vitro antibacterial prop- and colleagues reported that(MIC) of minimum curcumin inhibitory against 7 concentration standardcus bacterial aureus strains ( culinary spice extracts againstand clinical a isolated limited intestinal numbertheir bacteria, susceptibility of or bacterial antimicrobial strains activity have against been spices. assessed Gunes for not with the concentrationothers of 2011). chemical biomarker (Henning and Prebiotic potential of spice extracts . . . Based on potential healththis benefits demonstrated study from investigated ouractivity, major group, and chemical constituents,beneficial antioxidant extract was reported to increase duce the of both obese and lean rats (Romo-Vaquero and others 2014). cinnamon stick extracters (625 2007), to but cinnamaldehydeof did selected not modulate thecontent population (Khare and others 2016). Supplementation of rosemary tum their antimicrobial activity againsttoxigenic bacterial 88 strains. intestinal, pathogenic, and

Food Chemistry oa ocnrto fmjrceiasqatfidwstehighest the was (2475 ROS quantified in chemicals The major extracts. of aqueous concentration in total present constituents re- bioactive major chemicals compounds and of marker of our number to consisted they However, the Because not limited. was constituents, and ported 1). all cooking (Table extract simulate spice to to 1 optimize designed than was more method extraction in rosmarinic and present vanillin, were acid, acid ferulic of as number such small compounds A CIN. phenolic and BLP, from from cinnamaldehyde CAP, and piperine acid of alkaloid cinnamic an extract TUR, aqueous and ROS, the ORE, from GIN, ingredients phenolic quantitated and major identified 14 we study, this characteristic In spice. often particular are each for that terpenoids and alkaloids, compounds, mean as presented were data and licate pc xrc-otiigpae,aheigafia nclmo 10 of inoculum final a achieving plates, extract-containing spice 10 of volume A h rwhsiuainb h etsierahdapaeu(iand (Li plateau a reached spice 2015a). test where others the and effect by growth, the stimulation no stimulated growth had spice the spice the where tested growth, as the each the growth where for on establish concentration of to the appearance recorded strain were the test plate control of the change to the compared Institute- in concen- plate, the Standards resulting control Further, Laboratory 2012). trations the others and and to Clinical (Hecht compared protocol the approved as in growth described of as change marked appearance a or the growth no in in resulting spice each of centration After examined. 2012). were others plates the and incubation, (Jousimies-Somer catalysts palladium by ao hmclcnttet n nixdn capacity antioxidant and constituents chemical Major Discussion and Results analysis Statistical for chamber CO growth anaerobic 5% positive an 37 a at in h as incubated 48 were used plates were The plates control. agar Brucella CFU/spot. magna goldia toxigenic 12 including spp., 1 including strains, . . . extracts spice of potential Prebiotic asadaeae aawr reported. were data as- averaged independent and duplicate says in performed were assays Microbiology n 2 and anaerobius, Peptostreptococcus est qa ota fa05MFradsadr correspond- standard McFarland 10 0.5 of a sus- density of A to that with testing. ing tubes to broth before equal Brucella h prepare density to 48 a used for was colonies plates of were agar pension strains Brucella bacterial The on extracts. con- of cultured mg/mL mg/mL 0.56, per 0.07 9.0 1.13, and 2.25, give spice 4.50, 0.14, give to 0.28, dry to times diluted mg further 20 was (182 which by centration diluted extracts 1st Spice were without 2012). milliliter) plates Jousimies- others 2012; control others and and and Somer (Hecht extract prepared were spice spice tested each the of dilutions and serial (Li published as analysis sequence 2015a). others rRNA 16S by identified pcsotncnanavreyo hmcl hticuephenolic include that chemicals of variety a contain often Spices trip- in out carried were assay antioxidant and analysis Chemical h Iswr eemnd I sdfie stelws con- lowest the as defined is MIC determined. were MICs The rclaaa B B,Sak,M. ... ltscontaining plates U.S.A.) Md., Sparks, BBL, (BD agar Brucella .aureus S. 2 ,5%H ° ,11 .Aarbccniin osse fagsmxueof mixture gas a of consisted conditions Anaerobic C. ± tan,wr lotse.Teebcei aebeen have bacteria These tested. also were strains, 2 Fusobacterium n 0 N 90% and , µ 70 n oeti A (30.7 CAP in lowest and 87.0) fteessesoswsiouae nthe on inoculated was suspensions these of L Akkermansia 8 atra ooyfriguis(CFU)/mL. units forming colony bacterial 4 lsrdu difficile Clostridium Ruminococcus p. 1 spp., 2 h eiuloye a removed was oxygen residual the ; ,7 Bacteroides etnpiu asaccharolyticus Peptoniphilus ± tnaddvain(SD). deviation standard p. 2 spp., p. 21 spp., ,2 amnlatyphi Salmonella ± .coli E. 3.8) Clostridium ,3 µ g/mL. Fine- ,1 5 , iiyo irognssta otiuet h elbigo their of well-being the to contribute that microorganisms of tivity 2016). others enhance and can Madureira they 2009; others or and (Hervert- bacteria, metabolism Hernandez these bacteria affecting by by substrates consumption nutrients as used ingredients be their because can effect stimulatory growth exert can foods I h oet h re fT a ROS was TE and highest of the order being The ORE lowest. from and ROS ranged the with capacity GIN TE antioxidant mM The 13.1 1. to Table 140.4 in listed also is TE CAP. eesiuae yBP yCP yGN n yTUR. by 2 effect and stimulatory GIN, growth the strains better by on 2 showed 4 mg/mL, extracts CAP, 2.25 spice by At all 7 Overall, ORE. BLP, by by 10 stimulated and GIN, were BLP, by by concentration stimulated 7 CAP, were the strains by 4 at 5 mg/mL, CAP 1.13 by At mg/mL. one 0.56 another of and BLP by by At enhanced 6 ORE. CAP, TUR. by by by 10 6 1 BLP, and and by ORE, GIN, stimulated by were 4 by GIN, strains 4 BLP, 7 by mg/mL, mg/mL, stimulated 4.5 2.25 At was strain. strain another of 1 growth the ORE enhanced both BLP mg/mL, 1.13 and concen- At lowest effect. the stimulating mg/mL, the 0.56 showing tration at ORE by stimulated was strain rwh fte17 stimulated the that extract Of growth. spice of concentrations lowest the represent CIN xrcscreae elwt h oa hmclcnetain( concentration chemical total 0.86, the with well correlated extracts h re a ROS was order The rwhsiuaoyeffect stimulatory Growth atyi R,RS n nmany in and fer- abun- ROS, found is ORE, acid, and in rosmarinic phenolic colon example, dantly or For aromatic the 2004). small to (Clifford produce passes acids to reach microbiota intake and gut absorbed the by that are of mented estimated polyphenols 95% is dietary Over It of plasma. form. 10% native to their 5% polymers in about or absorbed glycosides, esters, be of cannot form the that in polyphenols are diet Most the microbiota. in gut present on the the depend by (poly)phenols that biotransformation dietary suggest their to evidences attributable Convincing effects acids. beneficial phenolic polyphe- and to belongs nols majority characterized, activities. chemicals and the communities microbial Among gut influence the potential on chemicals of the these of into quantitation spice- insight and provide of phytochemicals content identification these high The or phytochemicals. moderate specific either contain extracts spice fcfecai n 3-(3 and acid caffeic of n1 tan of strains 17 on h rwho ahgncbcei n tmlt h rwhof growth the 2016). stimulate others and and (Madureira bacteria microorganisms pathogenic inhibit beneficial selectively of to growth found were the metabolites microbial other and study intervention these human confirmed of Results 2009). others and by (Bel-Rhlid or esterases chlorogenate medi- microbial process by a ated hy- metabolites, caffeic yield major The to as 2014). acids transformation droxyphenylpropionic microbial others subsequent and undergoes (Mosele acid feces human after using acid tation caffeic the product and microbial acid, rosmarinic of of generation degradation complete a reported study rboisaedfie ssbtne htidc h rwho ac- or growth the induce that substances as defined are Prebiotics vrg nixdn aaiyo ahsieetatdtrie as determined extract spice each of capacity antioxidant Average fte16 the Of eut rmorceia netgtosidctdta most that indicated investigations chemical our from Results al lutae h rwhsiuaoyefc fsieextracts spice of effect stimulatory growth the illustrates 2 Table > r 2 Lactobacillus = BLP 0.74). Lactobacillus  o.8,N.8 2017 8, Nr. 82, Vol. Bifidobacterium CAP nvitro in p.a oprdto compared as spp. Bifidobacterium ࣙ > ORE nig Msl n tes21) These 2014). others and (Mosele findings ,4 tan etd h rwho tanwas strain 1 of growth the tested, strains I.Teatoiatcpct fspice of capacity antioxidant The GIN. dhdoyhnllci cd recent A acid. -dihydroxyphenyl)lactic > n 6srisof strains 16 and CIN r ora fFo Science Food of Journal tan etd h rwho 1 of growth the tested, strains > Bifidobacterium GIN  atbclu johnsonii Lactobacillus > Lactobacillus ORE lns sa ester an is plants, TUR nvitro in > p.Some spp. > TUR fermen- Values . BLP 1809 r > > =

Food Chemistry 2.1 10.4 1.7 1.3 3.0 1.0 1.9 1.5 and ± ± ± ± ± ± ± ± Bifidobac- 27.6 20.4 22.8 and human studies Bifidobacterium 6.0 91.9 87.0 104 72.0 15.0 ± ± ± ± in vitro 645 4.1 140.4 30.0 2475 11.019.0 1830 spp. in both ± ± ± ± 706 1297 Lactobacillus 0.2 139.6 9.1 2003 0.1 13.2 0.2 11.8 8.5 0.3 8.2 994.54.59nd ± ± ± ± ± ± spp. and b functioning as prebiotics byterium stimulating the growth(Li of and others 2015a,others b; 2010; Molan Vendrame and andin others others support 2009; Mandalari 2011). of and Evidence the is prebiotic effect growing of foods high in polyphenols 99ndndnd4.59nd 9 nd nd 4.5 9 nd 9 4.5 nd nd nd nd nd 9 4.5 9 4.5 2.25 9 nd ndnd 4.5 ndnd 9 nd 9 2.25 nd ndnd ndnd 9 ndnd 1.25 nd 4.5 9 nd 2.25 nd nd nd nd nd nd nd nd nd 4.5 nd nd 4.5 nd nd nd nd nd nd nd 2.25 nd nd nd nd nd nd nd nd nd 9 9 nd 4.5 4.5 nd 9 4.5 9 4.5 4.5 1.13 9 2.25 1.13 9 2.25 4.54.5 4.5 9 9 nd 2.25 2.25 0.56 nd 9 nd nd nd 4.54.5 2.25 4.5 9 2.25 94.5 2.25 nd4.5 4.5 9 2.25 1.13 9 nd 9 9 2.25 nd 2.25 9 1.13 9 9 4.5 4.5 4.54.5 4.5 4.5 9 9 4.5 4.5 2.25 2.25 9 9 nd nd nd 0.56 0.625 92.25 1.13 2.25 1.13 9 9 1.13 nd 1.13 9 nd 2.25 2.251.13 91.13 2.25 1.13 1.13 9 1.13 9 1.13 9 1.13 1.13 nd 1.13 9 9 nd nd 2.25 4.5 9 4.51.13 1.13 4.5 nd 91.131.13 nd 4.5 1.13 2.25 2.25 9 9 9 1.13 1.13 1.13 nd 1.13 9 9 nd nd 0.6 13.1 61.5 177.1 56.0 5.5 are ± ± ± ± Bifidobacterium 1.1 58.8 3.8 992.8 0.3 1.3 0.30.3 1.6 2.0 Gg 4.5 0.56 4.5 2.25 1.13 4.5 2.25 ± ± ± ± ± ± ± and (mg/mL) of black pepper (BLP), (CAP), cinnamon (CIN), ginger (GIN), Mediter- Vol. 82, Nr. 8, 2017 r Lactobacillus a 0.8 21.2 4.2 4.2 30.7 ± ± ± Lactobacillus LactobacillusLactobacillusLactobacillus Gasseri Lactobacillus Gasseri LactobacillusLactobacillus Johnsonii Lactobacillus Lactis Plantarum Reuteri Rhamnosus Bifidobacterium Pseudocatenulatum Lactobacillus Fermentum BifidobacteriumBifidobacterium infantis BifidobacteriumBifidobacterium Longum Bifidobacterium Longum Longum Lactobacillus Longum LactobacillusLactobacillusLactobacillus Acidophilus Lactobacillus Breve Lactobacillus Casei Lactobacillus Casei Casei Crispatus Fermentum BifidobacteriumBifidobacterium Catenaforme Bifidobacterium Infantis Longum BifidobacteriumBifidobacterium Bifidum Breve Bifidobacterium Adolescentis BifidobacteriumBifidobacteriumBifidobacterium Adolescentis Bifidobacterium Animalis Bifidobacterium Animalis Bifidum Bifidum BLP CAP CIN GIN ORE ROS TUR g/mL) of major ingredients and antioxidant capacity (mM) in black pepper (BLP), cayenne pepper (CAP), µ species. Journal of Food Science nd: growth stimulation was not detected. Values are average of 2 tests. StoolStool 19888 19920 ATCCStoolStoolStool 53103 19911 19883 19884 StoolStool 19897 19879 StoolATCC 19935 14931 StoolATCCStoolStoolStool 19925 9595 19882 19908 19893 StoolStoolATCCATCC 19891 19892 27919 4356 Stool 19860 Lactobacillus ATCCStoolATCC 15697 19907 15707 StoolStool 19855 19815 ranean oregano (ORE), rosemary (ROS), and turmeric (TUR) extracts showing the growth stimulation of StoolATCCATCC 19893 15696 15700 StoolStoolStoolStool 19896 19814 19909 19886 1810 These 2 genera produceend-metabolites and acetic do acid not contain andous any lactic studies known by pathogens. acid our Previ- group as and the others have major identified dietary sources host (Hutkins and others 2016). widely established bacterial genera as prebiotic target organisms. a b SourceATCC Strain no. 15703 Genus Species BLP CAP CIN GIN ORE ROS TUR Table 2–Lowest concentrations Piperine 87.6 Table 1–Concentrations ( cinnamon (CIN), ginger (GIN), Mediterranean oregano (ORE), rosemary (ROS), and turmeric (TUR) extracts. Prebiotic potential of spice extracts . . . Vanillin 3.30 LuteolinApigenin 1.1 11.2 Capsaicin 12.9 Antioxidant capacity 21.8 Rosmarinic acid Cinnamaldehyde6-GingerolP-coumaric acid 926 170 1.80 DihydrocapsaicinFerulic acidCinnamic acid 4.1 1.4 66.8 Demethoxycurcumin Curcumin Total concentration 87.6 Lithospermic acid Luteolin-3-glucuronide Bisdemethoxycurcumin

Food Chemistry 43 Stool 14131 Stool 2 87 Stool 18271 Stool 1 46 Stool 14060 84 Stool 18249 63 Intraabdominal 16534 14Fo le,DM ulcer, Foot 3144 Stool 16523 10Fo le,DM ulcer, Foot 3110 88 Stool 18286 76 Stool 17162 52 Intraabdominal 15529 51ATCC ATCC 8501 25586 Stool ATCC 4 27756 Stool 16448 75 Stool 17059 66 Stool 16961 Stool Stool Stool Stool 3 17493 17457 17492 85 Stool 18257 58 ATCC 25286 69 Blood 16996 42 Stool 14824 65 Stool 16351 87ATCC 9817 80 Stool 18406 84 Stool 18241 66 Stool 16469 92 ATCC 29328 68 Stool 16981 47 Stool 14572 58 ATCC 25285 82 Stool ATCC 18421 29328 81 Stool 18410 Stool 17490 Dea n tes21) u eut ugs htsm fthe of of some number growth that a the stimulating of suggest by effect results prebiotic-like exhibit Our spices tested 2015). others and (Duenas d c b a TUR ROS ORE GIN CIN CAP BLP Species Genus ATCC Source 19982 Strain concentrations inhibitory 3–Minimum Table . . . extracts spice of potential Prebiotic n tes21)adi ainswt ogtr sha(Hevia asthma long-term with patients in (Schwiertz and subjects 2010) overweight others in and demonstrated been have bifidobac- of teria levels lower similarly, of 2015); others prevalence bi- and on of higher (Gao children levels to effects Lower linked 2005). their were others through fidobacteria and (Picard diarrhea system immune infectious the been alleviate have to Bifidobacteria 2016). shown others and (Arboleya of conditions abundance relative or diversity, dobacterium composition, The tract. 94 ATCC 29742 GN,Mdtraenoeao(R) oeay(O) n umrc(U)etat gis netnlbceilspecies. bacterial intestinal against extracts (TUR) turmeric and (ROS), rosemary (ORE), oregano Mediterranean (GIN), ausaeaeaeo tests. 2 of average are Values ag;1 Range; ag;1L cdpiu tanhdMC9m/L 15 mg/mL, 9 MIC had strain acidophilus L. 1 Range; 1 Range; idbcei r omlihbtnso h gastrointestinal the of inhabitants normal are Bifidobacteria atbclu acidophilus Lactobacillus .difficile C. pce a enipiae nsvrlitsia disease intestinal several in implicated been has species al 2 Table al 2 Table abscess abscess Stool tanhdMC45m/L 1sris9mg/mL. 9 strains 11 mg/mL, 4.5 MIC had strain Bifidobacterium n 1 and shrci Coli Escherichia shrci Coli Escherichia atrie Thetaiotaomicron Bacteroides lsrdu Difficile Clostridium uoatru Nucleatum Fusobacterium Lactobacillus atrie Ovatus Bacteroides lsrdu Sordellii Clostridium amnlaTyphi Salmonella atrie Fragilis Bacteroides lsrdu Butyricum Clostridium uoatru Necrophorum Fusobacterium uoatru Varium Fusobacterium tpyoocsAureus Typhi Staphylococcus Salmonella Perfringens Clostridium lsrdu Butyricum Clostridium uoatru Nucleatum Nucleatum Fusobacterium Fusobacterium tpyoocsAureus Torques Staphylococcus Productus Obeum Gnavus Ruminococcus Ruminococcus Ruminococcus Ruminococcus atrie Fragilis Bacteroides uoatru Necrophorum Fusobacterium uoatru Nucleatum Fusobacterium lsrdu Perfringens Clostridium lsrdu Bolteae Clostridium uoatru Necrophorum Mortiferum Fusobacterium Fusobacterium etsrpoocsAnaerobius Peptostreptococcus atrie Fragilis Bacteroides lsrdu Bifermentans Clostridium Bifidobacterium uoatru Nucleatum Fusobacterium lsrdu Perfringens Clostridium ieodaMagna Magna Finegoldia Finegoldia etnpiu Asaccharolyticus Peptoniphilus Orbiscindens Clostridium atrie Fragilis Bacteroides ieodaMagna Finegoldia uoatru Nucleatum Fusobacterium kemni Muciniphila Akkermansia atrie Thetaiotaomicron Bacteroides atbclu gasseri Lactobacillus and Lactobacillus Lactobacillus tanwt I f68 gm n 1 and mg/mL 6.82 of MIC with strain a species. p. 6sris6.82 strains 16 spp.; p. 7strains 17 spp.; m/L fbakppe BP,cyneppe CP,cnao CN,ginger (CIN), cinnamon (CAP), pepper cayenne (BLP), pepper black of (mg/mL) .coli E. p.strains spp. toxin toxin ;12strains + + nobese in > 9mg/mL. Bifi- h rwho G tana ocnrto agn rm05 to 0.56 from ranging concentration at mg/mL. strain 4.5 LGG promote to of found were growth extracts the spice all study, and our (Hojsak In infections 2010). tract others respiratory and gastrointestinal of viruses tion others by (Kalliom and disease caused Guandalini atopic 1999; 2000), diarrhea others and treating (Vanderhoof bacteria in and results promising shown of growth spice activity. the stimulatory 7 promoting among in that human active dobacterium in in most findings was bifidobacteria new ORE of extracts reported role study a Our suggesting health. 2016), others and .268 .14509 .62.25 0.36 0.94 4.5 1.71 6.82 6.82 3.42 > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > . . .134 .106 2.84 0.64 1.71 3.42 1.71 4.5 4.5 tde of Studies . .14512 .21.71 0.42 1.25 4.5 1.71 4.5 9 → 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 994.5 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 .gasseri L. 9 c hra I,BP n A rdcdmr modest more produced CAP and BLP, GIN, whereas n 1 and atbclu rhamnosus Lactobacillus > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > .reuteri L. 9 9 9 94.5–9 99 99 9 99 9 9 93.42 9 99 9 94.5 9 94.5 9 99 96.8296.82 9 9 96.82 94.5 96.829 96.82 9 9 99 99 9 92.25 9 9 92.259 9 9 9 9 99 9 94.5 99 99 99 9 o.8,N.8 2017 8, Nr. 82, Vol. .johnsonii L. → and > > > > > > > > > > > > > > > > > > > tanwt I f9mg/mL. 9 of MIC with strain 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 d b .rhamnosus L. k n tes20) n npreven- in and 2001), others and aki ¨ > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > r G(G,AC 30)have 53103) ATCC (LGG, GG 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 94.54.5 9 . .59 2.25 9 2.5 9 99 9 9 9 94.54.5 9 .24.5 6.82 9 9 9 9 9 99 99 9 9 9 9 9 9 99 99 9 9 ora fFo Science Food of Journal r fe de odairy to added often are > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > 9 9 9 9 9 9 9 9 9 9 . 5.65 4.5 9 9 99 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 96.82 9 9 9 9 > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 1811 Bifi- > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > > 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9 9

Food Chemistry and in a GG in the ) at different hirtum Lactobacillus L. ssp L.) essential oils. J Agric Lactobacillus johnsonii in vitro . J Food Agric Environ 5(2):92–4. . PLoS ONE 11(2):e0147809. Salvia officinalis vulgare L. and growth. Int J Food Microbiol 136(1):119–22. and bifidobacteria: a case-control study. BMC Pediatr Salmonella enteritidis and E. coli Bifidobacterium adolescentis Rosmarinus officinalis minimum inhibitory concentration study. Toxicol Ind Health 32(2):246– Bacillus subtilis Lactobacillus acidophilus in vitro GG administered in oral rehydration solution to children with acute diarrhea: a Research was supported by departmental funds from the Center Q. Lu, Z. Li, S. Henning, D. Heber, and S. Finegold designed hydrosols against rosmarinic acid from rosemary extractgastrointestinal with model. esterases J and Agr Food Chem 57(17):7700–5. 217:281–93. of rosemary and sageFood Chem ( 55(19):7879–85. Planta Med 70(12):1103–14. 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Belmont: Star Publishing. to point out that amongand the GIN spices possessed prebiotic-like investigated, effects ORE, byof BLP, CAP, promoting the beneficial growth bacteriabacteria in on the one other,lation suggesting hand of their and potential intestinal role suppressing microbiotatestinal in and health. pathogenic Further the the research regu- on enhancement the connectionsinduced of between spice- changes gastroin- in gutdisease preventive microbiota effect and in animal host models metabolism and and/or humans is needed. for Human Nutrition, Dept.of of Medicine, Univ. Medicine, of David California, Geffen Los School Angeles, Calif., U.S.A. the study, assisted interpretations, andLu wrote revised and the revised manuscript. theJ. Q. manuscript. Huang P. carried Summanen, R. outinterpretations. Lee, the and experimental work and supported data Acknowledgment Authors’ Contributions References Al-Turki AI. 2007. Antibacterial effect of , , sage, black pepper and Bel-Rhlid R, Crespy V, Page-Zoerkler N, Nagy K, Raab T, Hansen CE.Bi 2009. X, Hydrolysis of Lim J, Henry CJ.Bozin 2017. B, Mimica-Dukic Spices N, in Samojlik the I, Jovin management E. 2007. of Antibacterial diabetes and mellitus. antioxidant properties Clifford Food MN. Chem 2004. Diet-derived phenols in plasma and tissues andCueva their implications C, for Bartolome health. B, Moreno-Arribas MV, Bustos I, RequenaDuda-Chodak A. T, 2012. The Gonzalez-Manzano inhibitory effect S, of polyphenols on human gutDuenas microbiota. J M, Physiol Munoz-Gonzalez I, Cueva C, Jimenez-Giron A, Sanchez-Patan F, Santos-Buelga Gao XL, Jia RZ, Xie L, Kuang LH, Feng L, Wan CM. 2015. Obesity in school-aged children Guandalini S, Pensabene L, Abu Zikri M, Dias JA, Casali LG, Hoekstra H, Kolacek S, Massar K, Gunes H, Gulen D, Mutlu R, Gumus A, Tas T, Topkaya AE. 2016. Antibacterial effects of Arboleya S, Watkins C, Stanton C, Ross RP. 2016. Gut bifidobacteria populations in human Hervert-Hernandez D, Pintado C, Rotger R, Goni I.Hevia 2009. Stimulatory A, role Milani of grape C, pomace Lopez P, Donado CD,Hojsak Cuervo I, Snovak A, N, Abdovic Gonzalez S, Szajewska S, H, Misak Suarez Z, Kolacek A, S. 2010. Turroni F, Grevsen K, Frette XC, Christensen LP. 2009. Content and composition of volatile terpenes, Halvorsen BL, Carlsen MH, Phillips KM, Bohn SK, HolteHecht K, DW, Jacobs Citron DM, DR, Dzink-Fox Jr., J, Blomhoff Gregory WW, R. Jacobus NV, Jenkins SG, RosenblattHenning JE, SM, Zhang Y, Seeram NP, Lee RP, WangP, Bowerman S, Heber D. 2011. Antioxidant Hutkins RW, Krumbeck JA, Bindels LB, Cani PD, Fahey G, Jr., Goh YJ, HamakerJousimies-Somer B, Martens HR, Summanen P, Citron D, Baron E, Wexler HM, Finegold SM. 2012. , ¨ a L. E. and spp. E. coli Clostrid- (Suther- , 9mg/mL, with MIC > . It is worthwhile Finegoldia strains tested were Bifidobacterium and CIN, ROS, or , isolates, except that spp. were susceptible L. rhamnosus with MIC of 3.42 and . and species, but minimal or no Lactobacillus acidophilus .Datafromother Bacteroides fragilis Clostridium Bacteroides C. difficile Bacteroides Ruminococcus Vol. 82, Nr. 8, 2017 S. aureus r culture model, this work provided F. magna isolates with MIC of Fusobacterium L. reuteri . C. difficile also to ORE and ROS. CIN exhibited Ruminococcus in vitro strain with MIC of 9 mg/mL. All spice strain with MIC of 6.82 mg/mL and 1 Lactobacillus spp. with varying degree. All spices exhibited high Staphylococcus strains. CIN inhibited the growth of 11 toxigenic and spp., with MIC ranging from 4.5 to 9.0 mg/mL. L. johnsonii F.necrophorum at 9 mg/mL and 1 strain at 4.5 mg/mL. All the other ,and S. typhi Journal of Food Science and 1 showed that minimal growth inhibitions were observed in 2 Lactobacillus and Previous research on the diet and intestinal bacteria interactions Gut microbiota is a mixed population, where the interactions Table 3 lists the MICs of 88 bacterial strains representing the Lactobacillus gasseri sive study comprising ofintestinal, including 7 toxigenic culinary and pathogenic, spices bacterialnot on previously strains been has the reported. viability of 88 ria (Al-Turki 2007; Bozin and othersSaeed 2007; and Shan and Tariq others 2009;others 2007; 2016b; Sutherland Shareef and and others others 2009; 2016); Gunes however, a and comprehen- been shown to haveand antimicrobial others properties 2005; (Puupponen-Pimi Vaquero andCueva others and 2007; others Duda-Chodak 2015).study 2012; Although were all known to of have the activity against spices limited tested strains in of bacte- this has been centered mainly onor the their antimicrobial constituents properties of against foods there pathogenic is microorganisms. a To date, range of foods and their phenolic constituents that have highly susceptible to all4.50 mg/mL spices, being with observed for MICwere CIN, inactive ranging ORE, against and from 2 ROS. All strains 0.36 spices of to to CIN, and modest activity againstTUR toxigenic against a few strains of other MICs ranging fromshowed 3.42 higher to activity 6.82 against 2.25 mg/mL. mg/mL, Both respectively. All BLP 4 and CIN ium strains by CIN, in 2 strains by ROS, and 1 strain by TUR with Salmonella and inhibitory activity against activity against selected strains of C. difficile spices were inactive against Fusobacterium None of the testedcoli spices were bactericidal against the tested extracts were inactiveCIN against was all activeof against 4.5 1 mg/mL. strain Extracterate of activity of against CIN, another GIN, group and of ORE gram-negative showed anaerobes, mod- except that BLP was active against 1 gasseri the inherent limitation of new findings of the effect ofintestinal spices on microbiota. bacteria isolates We from showed normal exception that of all TUR, tested promoted spices, the with growth the of among different species are crucial to establish the balance. Despite 1 major genera andbiota. species Data found revealed in that allBifidobacterium the spice human extracts were intestinal inactive micro- against all 1812 Conclusions land and others 2009). Antimicrobial effect GIN, and ORE enhanced1.13 the or growth 2.25 ofSutherland mg/mL. these who Our reported species that data atchili aqueous are either enhanced extracts the consistent of growth ginger with of and a red study by products, or formulated as dietary supplementsbiotic for controlling bacterial dys- overgrowth during an active infection. BLP, CAP, Prebiotic potential of spice extracts . . .

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