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Seed and peel essential oils obtained from Campomanesia adamantium fruit inhibit inflammatory PDF

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Preview Seed and peel essential oils obtained from Campomanesia adamantium fruit inhibit inflammatory

RESEARCHARTICLE Seed and peel essential oils obtained from Campomanesia adamantium fruit inhibit inflammatory and pain parameters in rodents DanieliZuntiniViscardi1*,Jucicle´iadaSilvaArrigo1,CamiladeAzevedoChavesCorreia1, CaˆndidaAparecidaLeiteKassuya2,ClaudiaAndreaLimaCardoso3,Iriani RodriguesMaldonade4,ElianaJanetSanjinezArgandoña5 1 CollegeofExactandTechnologicalSciences,FederalUniversityofGrandeDourados,Dourados,Mato GrossodoSul,Brazil,2 CollegeofHealthSciences,FederalUniversityofGrandeDourados,Dourados, a1111111111 MatoGrossodoSul,Brazil,3 CourseofChemistry,StateUniversityofMatoGrossodoSul,Dourados,Mato a1111111111 GrossodoSul,Brazil,4 BrazilianAgriculturalResearchAgency(Embrapa),Bras´ılia,FederalDistrict,Brazil, a1111111111 5 CollegeofFoodEngineering,FederalUniversityofGrandeDourados,Dourados,MatoGrossodoSul, a1111111111 Brazil a1111111111 *[email protected] Abstract OPENACCESS Campomanesiaadamantium(Myrtaceae)ispopularlyknownas“gabiroba”andhasbeen Citation:ZuntiniViscardiD,ArrigoJdS,Correia CdAC,KassuyaCAL,CardosoCAL,MaldonadeIR, usedinfolkmedicineasantirheumatic,antidiarrheal,hypocholesterolemicandanti-inflam- etal.(2017)Seedandpeelessentialoilsobtained matory.Thisstudyevaluatedtheanti-inflammatoryandantinociceptiveactivitiesandtoxi- fromCampomanesiaadamantiumfruitinhibit cologyofessentialoilsfrompeel(EOP)andseed(EOS)ofC.adamantiumfruitsinanimal inflammatoryandpainparametersinrodents. models.Differentgroupsweretreatedwithdosesof100and300mg/kgandtheinflamma- PLoSONE12(2):e0157107.doi:10.1371/journal. pone.0157107 toryparameterswereevaluatedincarrageenaninducedpawoedemaandleukocytemigra- tioninpleurisymodel,whileantinociceptiveactivitywasevaluatedusingformalinmethodin Editor:FranciscoJ.Schopfer,Universityof Pittsburgh,UNITEDSTATES rodents.ThemajorconstituentofEOPandEOSwaslimonenewith13.07%and20.89%, respectively.Noclinicalsignsoftoxicityhavebeenobservedinanimals.Itwasobserveda Received:March1,2016 significantdecreased(P<0.01)inleukocytemigrationatthedoseof300mg/kgofEOPand Accepted:January30,2017 EOS,withmaximalinhibitionof89±3%forEOPand80±6%forEOS.Pawoedemawas Published:February21,2017 inhibitedatalltimes,andmaximalinhibitionwasatthedoseof100mg/kgat2haftercarra- Copyright:©2017ZuntiniViscardietal.Thisisan geenaninjectionwith72±2%forEOPand74±2%forEOS.EOSandEOPalsoreducedthe openaccessarticledistributedunderthetermsof firstandsecondphasesofformalin-inducednociceptiontest.Inthefirstformalin-phase, theCreativeCommonsAttributionLicense,which maximalinhibitionswereat48±5%forEOPand66±4%forEOS(300mg/kg).Attheinflam- permitsunrestricteduse,distribution,and reproductioninanymedium,providedtheoriginal matoryphaseinducedbyformalin,maximalinhibitionswere72±2%forEOPand80±2%for authorandsourcearecredited. EOSatthedoseof100mg/kg.SeedandpeelessentialoilsfromC.adamantiumfruitinhib- DataAvailabilityStatement:Allrelevantdataare itedleukocytemigration,inflammatoryandneurogenicpainandoedemasuggestingtheir withinthepaper. useasnutraceuticalorpharmacologicalagent. Funding:Theauthorsalsowishtothankthe Fundac¸ãodeAmparoàPesquisadoEstadodo MatoGrossodoSul(FUNDECT)forfinancial support,throughtheprojectsFUNDECT/CAPESn˚ 45/2014-PAPOSREDEPRO´-CENTRO-OESTE– FASEII-Nº23/200.622/2014andtheConselho NacionaldeDesenvolvimentoCient´ıficoe Tecnolo´gico(CNPq).Thefundershadnorolein PLOSONE|DOI:10.1371/journal.pone.0157107 February21,2017 1/15 PharmacologicaleffectsofCampomanesiaadamantiumessentialoilinvivo studydesign,datacollectionandanalysis,decision Introduction topublish,orpreparationofthemanuscript. CerradoregionisthesecondlargestbiomainBrazil,afterAmazonia.Thisecosystemcom- Competinginterests:Theauthorshavedeclared prisesmorethan7,000plantspecies[1].Duetoitsdiverseflora,researchinteresthasbeen thatnocompetinginterestsexist. increasedandendemicmedicinalplantsfromCerradohavebeenasourceofbioactivecom- pounds.Gabirobaorguabiroba-do-campoorguavira,thefruitofCampomanesiaadamantium (Cambess.)O.Berg,iswidelyfoundandusedinareasofCerrado,mainlyintheMidwest regionandAtlanticForestintheSoutheastandSouthregionsofBrazil[2]. C.adamantiumbelongstoMyrtaceaefamilyandtheirfruits,aswellasfruitsfromother speciesofCampomanesia,aretraditionallyusedintheproductionofhomemadeliqueurs, juices,andsweets[3]andalsoemployedinfolkmedicineasantirheumatic,antidiarrheal, hypocholesterolemic,anti-inflammatory[4],andforthetreatmentofcystitis,andurethritis [5]. OurgrouphaspreviouslyshownthathydroalcoholicextractfromC.adamantiumfruit barksexhibitedanti-inflammatory,antihyperalgesic,andantidepressiveactivityinrodents, withnoevidenceoftoxicologicalsigns[6].Studieswithethylacetateandaqueousextracts fromleavesC.adamantiumhavedemonstratedantinociceptiveandanti-inflammatoryeffects supportingfolkmedicineuseoftheseplants[7].Phytochemicalanalyseshaveattributedthe anti-inflammatory,antiproliferativeandantimicrobialactivitiesofC.adamantiumtothepres- enceofflavonoidsandchalcones,whicharethemajorconstituentsintheextract[5,6,7,8]. TheessentialoilfromC.adamantiumleaveshavebeenpreviouslydescribedasantioxidant andantimicrobial,havingasmajorconstituentsinessentialoillimonene,α-pineneandβ- pinene[9].Despitethisevidence,therearenoreportsontheanti-inflammatory,antinocicep- tiveandtoxicologicalparametersoftheessentialoilofpeelandseedofthisfruit,whichjustify thepresentstudy. Therefore,weaimedtoevaluatethechemicalcompositionofseedsandpeelsofessentialoil fromC.adamantiumfruitandtotheirrelationtoacutetoxicity,leukocytemigration,inflam- matoryandneurogenicpainandpawoedemainanimalmodels. Materialsandmethods Plantmaterial ThevegetablematerialcollectedwasregisteredintheAuthorizationSystemandInformation ofBiodiversity(SISBIO),N˚39462.Thefieldstudiesdidnotinvolveendangeredorprotected species.Theguavira’sfruitswereproducedbysmallfarmerslocatedatPontaPorã-MS,Brazil, (23˚32010@S,55˚37033@W),onNovember2013. AvoucherspecimenwasdepositedintheherbariumoftheFacultyofBiologicalSciencesof UFGD(DDMS4602).Fruitsweresanitizedandpulp,peelandseedswereseparated.Peeland seedsweredriedat40˚Cfor62and72h,respectively,protectingthemfromdirectlightuntil use.Humiditywascalculatedonadrybasis(UBS)at70˚Cfor24hours[10]. Thecalculationoftheyieldwasobtainedtakingintoaccountthemoisturecontentona dry,basis,accordingtothefollowingequation: V Yield ¼ oilessential (cid:3)100 W (cid:0) Wsample(cid:3)H sample 100 WhereV isoilessentialvolumeobtained(mL),w isinitialsamplemass(g) oilessential sample andHisthemoisturecontent. Animals. MaleWistarrats(200–230g)andmaleandfemaleSwissmice(20–25g)were obtainedfromFederalUniversityofGrandeDourados(UFGD)biotherium.Animalswere PLOSONE|DOI:10.1371/journal.pone.0157107 February21,2017 2/15 PharmacologicaleffectsofCampomanesiaadamantiumessentialoilinvivo keptincollectivecages—(6animals/cage)atacontrolledtemperature(23±1˚C)withlight cycle(12hlight/dark),drinkingwaterandacommercialdietadlibitum.The23/2014protocol wasapprovedbythe“EthicsCommitteeonAnimalUse(CEUA)ofFederalUniversityof GrandeDourados”. Extractionandcompositionofessentialoil Essentialoilwasobtainedfrom200gofdriedpeeland200gofdriedseedsfromC.adaman- tiumbyHydrodistillation(3replicates)usingaClevenger-typeapparatusfor3hours.Atthe endofeachdistillation,oilswerecollectedandtransferredtoglassflasks,andkeptatatemper- atureof-18˚Cforfurtheranalyses.Samplesobtainedbyhydrodistillationwereanalyzedby GC/qMS(ShimadzuP2010plus.ShimadzuTokyo,Japan)equippedwithanautoinjectorsplit/ splitless.ThechromatographicseparationwasperformedonaDB-5column(J&W.Folsom, California)5%phenyl-dimethylpolysiloxane(30mlong×0.25mmdiameter×0.25mmof filmthickness)underthefollowingconditions:carriergashelium(99.999%)ataflowrateof1 mL/min;1μLofinjectionvolumesplitratio(1:20).Thetemperatureprogramofthefirstcol- umnstartedat50˚Cfor5min,heatingat3˚C/minuntil250˚C.Theinjectortransferlineand detectortemperatureusedweremaintainedat250˚C.TheMSscanparametersincludedelec- tronimpactionizationvoltageat70V,amassrangefrom50to550Daltonsandascaninterval of0.5s.Samples(1mgoftheessentialoils)wasdilutedin1mLofn-hexanebeforeinjection. Temperature-programmedretentionindexes[11]werecalculatedusingamixtureofnor- malalkanes(C -C )asexternalreferences.Identificationofcompoundswasperformedusing 6 30 retentiontime[12]andcomparingwithinterpretationofmassspectraofunknowncompo- nentsaccordingtoWileymassspectralibrary,WileyMS6thEdition. Relativepeakareasforeachchromatographicpeakwereusedtoevaluatethecontribution ofeachcompoundtothetotalareaandforcomparisonsbetweensamples.Thesumofallpeak areaswasconsidered100%ofthesampleandforeachpeakapercentagewasassignedcorre- spondingtoitsarea[11]. Anti-inflammatorytests Pleurisy. DifferentgroupsoffemaleSwissmice(n=5)wereorallyadministeredwith EOP(essentialoilfrompeel)andEOS(essentialoilfromseed)atthedosesof100and300mg/ kg,respectively,in0,9%ofsalinesolution,whichwasadministeredasacontrolinathird groupofanimals.Positivecontrolgroupreceiveddexamethasonesubcutaneouslyatdoseof1 mg/kg.Pleurisywasinducedintheexperimentalgroupsbyintrapleuralinjectionof100μLof 1%carrageenandilutedinsaline,afteronehouroftreatment(withoutanesthetization),aspre- viouslydescribed[13].Negativecontrolreceived100μLofsterilesalinebyintrapleuralinjec- tion.After4h,animalswereeuthanizedandthepleuralcavitywaswashedwith1mL phosphatebuffer-saline(PBS).Analiquotof20μLoflavage(exudate)wascollectedfromthe pleuralcavity,anddilutedwithTurck(1:20)andusedfortotalleukocytecountinaNeubauer chamber[14]. Carrageenan-inducedpawoedema. DifferentgroupsofmaleSwissmice(n=5)were orallytreatedwithEOPandEOS(100and300mg/kg),orvehicle(controlgroup).Another groupwastreatedsubcutaneouslywithdexamethasone(1mg/kg).After1h,animalsreceived asolutionof50μLcarrageenaninjection(300μg/paw)inthelefthindpaw.Theotherpaw receivedthesamevolumeofsterilesaline0.9%.Thepawvolumewasmeasuredat1,2,3and4 hoursaftercarrageenaninjectionwithapletysmometer.Resultswereexpressedasthediffer- encebetweentheleftandrightpawsateachtime[4]. PLOSONE|DOI:10.1371/journal.pone.0157107 February21,2017 3/15 PharmacologicaleffectsofCampomanesiaadamantiumessentialoilinvivo Antinociceptivetests Formalin-inducedspontaneouspainmodel. Nociceptionwasevaluatedafterinjection offormalin[15,16].Sixtyminutesbefore,maleWistarrats(n=5)weredividedingroups:dex- ametasone(1mg/kg.s.c.),EOS(100and300mg/kg),EOP(100and300mg/kg)andvehicle (salinesolution(0.9%),treatedbyoralroute.Onehouraftertreatmentsitwasinjected20μL ofsalinecontaining2.5%offormalinintherighthindpaw.Painreactiontime(pawlicking)in secondswasevaluatedfrom0to5min(phase1—neurogenicpain)andfrom15to30min (phase2—inflammatoryresponse)afterinjectionofformalininthepaw[14],whichrepresents thetonicresponsetopain,accompaniedbyaninflammatoryresponse.Following,animals weresubmittedtopawoedemameasurement,coldsensitivityandopenfieldtests. Coldsensitivity. Coldhyperalgesiawasmeasuredbytheacetonetestasdescribedby DecosterdandWoolf[17].Aneedleconnectedtoasyringewasusedtodrop30μLofacetone onthepawandtheduration(inseconds)ofthepawwithdrawalwasrecorded.Minimaland maximalcut-offswereassignedat0.5and20sec,respectively.Pawwithdrawalsduetoloco- motionorweightshiftingwerenotcountedandsuchtrialswererepeated[7]. Open-fieldtest. Analysesoflocomotionactivitieswereperformedafterformalinexperi- ment.Theratswereacclimatedinlocomotormeasurementchambersbeforetesting.Forthe test,ratswerepositionedinthecenterofanopen-fieldapparatus,consistedofwhitesquare arena(80×80cm)surroundedbywalls(40cmheight)withitsfloordividedbylinesinto16 squares(20×20cm).Locomotoractivitywasdeterminedbythenumberofsquarescrossed during5minutes.Theapparatuswascleanedwith10%ethanolsolutionandpapertowels betweeneachsection[18]. Formalin-inducedpawoedema. Animalsreceivedanintraplantarinjectionofformalin (20μLofasolution2.5%v/v)intherighthindpaw.Thicknesspawoedemawasassessedusing apletysmometer30minbeforeanytreatmentandafteronehourofformalininjection.Results wereexpressedinμLasthedifferencebetweenthebaselineandpost-injectionoedemavalues, withmodificationsofKassuyaetal.[14] Toxicitytest Acuteoraltoxicity. Treatmentswereperformedbysingleoraladministrationatdoses0, 175,560,1792,or2000mg/kgofbodyweightofEOPandEOS.FemaleSwissmice(n=8) wereobservedforsignsoftoxicityduringthefirst0.5,1,2,4,8,12and24hoursandatevery 48hoursfor14days.Duringtheexperimentalperiodanimalswereobserveddailyforclinical aspects,includingposture,seizures/tremors,consistencyandappearanceofthefeces,eyelid closure,piloerection,appearanceofskinandhair,stress,salivation,behavior,bodyweightand consumptionoffoodandwater[19]. Statisticalanalyses Resultswereexpressedasmean±standarderrorofthemean(S.E.M.).Forcomparisonof resultsamongexperimentalgroupsitwasusedanalysisofvariance(one-wayANOVA)fol- lowedbyNewman-Keulstest.Thenumberofanimalspergroupisindicatedinthelegends. Statisticaldifferenceswereconsideredsignificantatp<0.05. Results ThemoisturecontentdeterminedfordriedpeelandseedofC.adamantiumwere26.07± 3.80%(wt,massofwaterpermassofdriedmatter)and7.29±0.31%(wt),whiletheobtained essentialoilsyieldswereforpeel0.32%andseed0.98%(w/w). PLOSONE|DOI:10.1371/journal.pone.0157107 February21,2017 4/15 PharmacologicaleffectsofCampomanesiaadamantiumessentialoilinvivo Thelistofcompoundsidentifiedwithacompositionhigherthan1%inoilsisshowninthe Table1.Theretentiontimes,whichweredeterminedfromthreeindependentexperiments, showedacoefficientofvariationlessthan2%.Themajorconstituentsinpeeloilswerelimo- nene(13.07%)andthujopsene(6.96%)whileseedoilswerelimonene(20.89%)andβ-pinene (11.48%)(Table1). OraladministrationofEOPandEOSsignificantlyinhibitedtheleukocytemigrationatall dosestested(100and300mg/kg).Asignificantdecreasewasobservedinleukocytemigration, atthedoseof300mg/kgofEOPandEOS,withmaximuminhibitionat89±3%forEOPand 80±6%forEOS(Fig1). EOPandEOScausedareductioninpawoedemainducedbycarrageenan(Fig2)atall times,andmaximuminhibitionwasatthedoseof100mg/kgafter2hofcarrageenaninjection (72±2%forEOPand74±2%forEOS),respectively. EOPandEOS(Fig3,PhaseI)producedsignificantantinociceptiveeffectsinthefirstphase whencomparedtocontrolgroup.EOPandEOS,respectivelyatthedosesof100and300mg/ kgsignificantlyreducedlickingtimeinthesecondphaseofformalintestinrats(Fig3Phase II).Dexametasone(1mg/kg)producedsignificantantinociceptiveactivityinbothphasesof theformalinmethod.ItwasalsofoundthatorallyadministrationofEOPandEOSinhibited formalininducedpawoedema. EOSadministration(100and300mg/kg)significantlyattenuatedcoldhypersensitivity durationafterformalininjection.Animalsalmostdidnotmoveandraisedtheirpawsafew timesafteracetoneapplication(Fig4A).Furthermore,hypersensitiveresponsetocoldwaslon- gerthan10seconds(Fig4B). Fig4AshowsthatoraltreatmentwiththeEOPandEOSwithdosesvaryingfrom100mg/ kgand300mg/kg,theformalin-inducedincreasedinsensitivitytoacoldstimulushassignifi- cantlyreduced,withamaximalinhibitionat65±3%,68±2%,75±6%,77±2%,respectively, comparedtothecontrolgroup.Treatmentwithdexamethasonesignificantlyinhibitedthe coldsensitivityinducedbyformalinat85±3%(Fig4A). EOP(100mg/kgand300mg/kg)andEOS(100mg/kgand300mg/kg)alsocausedareduc- tioninpawoedemainducedbyformalin.Fig4Bshowspawoedemawithreductionof 49±2%,53±2%,72±4%,79±3%,respectively,comparedtothecontrolgroup.Treatment withdexamethasonesignificantlyinhibitedthepawoedemainducedbyformalinby87±3% (Fig4B).TheoraltreatmentwithessentialoilfromseedandpeelofC.adamantiumfruitdid notdecreaselocomotoractivityinopen-fieldtest(datanotshown). Toxicityofextractsandcompoundswereevaluatedasrequiredbyregulatoryagencies. Mortalityisthemostevidentsignoftoxicity.However,otheraspectsprovidemoresubtledata oftheadverseeffects,suchaslossofbodymassduringthestudyperiodandclinicalsignsof toxicity(diarrhea,piloerectionandbehaviorchanges).Animalsusedinthepresentstudy receivedessentialoils(EOSandEOP)ofC.adamantiumanddidnotexhibitanyclinicalsigns oftoxicityatalldosesadministeredandnosignificantchangeswereobservedinwaterand fooduptake.Furthermore,theabsoluteandrelativeweightoftheorgans(liver,kidneysand lungs)presentednostatisticallysignificantdifference(Tables2and3). Discussion Thepresentstudydemonstratedtheanti-inflammatory,antinociceptiveandtoxicological analysesofEOSandEOPfromC.adamantiumfruits.Experimentaldatademonstratedthat EOSandEOPinhibitedleukocytemigration,inflammatoryandneurogenicpainandoedema, suggestingtheiruseasanutraceuticalorpharmacologicalagent. PLOSONE|DOI:10.1371/journal.pone.0157107 February21,2017 5/15 PharmacologicaleffectsofCampomanesiaadamantiumessentialoilinvivo Table1. CompositionofthevolatilecompoundsindentifiedintheessentialoilsofthepeelandseedofCampomanesiaadamantiumfruits. Compounds R RI LI Composition(%) t Peel Seed Cumene 7.378 925 924 0.49 0.85 α-Pinene 7.653 932 932 4.67 8.50 Camphene 8.132 946 946 0.12 0.29 β-Pinene 9.190 976 974 4.82 11.48 Myrcene 9.667 989 988 1.07 1.85 α-Phellandrene 10.206 1003 1002 2.13 3.96 δ-Carene 10.425 1009 1008 0.19 0.11 α-Terpinene 10.679 1015 1014 0.39 0.79 o-Cymene 11.019 1023 1022 1.49 1.05 Limonene 11.186 1025 1024 13.07 20.89 1.8-Cineole 11.232 1026 1026 3.56 0.18 Z-β-Ocimene 11.449 1033 1032 0.12 - E-β-Ocimene 12.001 1045 1044 3.24 4.12 U-Terpinene 12.249 1054 1054 1.00 1.66 Terpinolene 13.724 1091 1086 1.82 2.09 Linalool 14.154 1096 1095 3.17 2.32 endo-Fenchol 14.816 1116 1114 0.11 0.21 Borneol 17.155 1168 1165 0.18 0.38 Terpinen-4-ol 17.477 1175 1174 0.79 0.89 α-Terpineol 18.101 1186 1186 2.40 2.61 Myrtenal 18.507 1196 1195 0.17 0.18 trans-Piperitol 19.007 1208 1207 0.12 0.14 trans-Carveol 19.238 1215 1215 0.12 0.13 Nerol 19.842 1228 1227 0.12 - Carvone 20.468 1240 1239 0.12 - Geraniol 21.020 1250 1249 0.15 - Perillaaldehyde 22.012 1270 1269 0.13 0.10 Carvacrol 23.133 1299 1298 0.12 - Methylgeranate 24.075 1323 1322 0.13 0.16 δ-Elemene 24.568 1335 1335 0.10 0.11 α-Ylangene 26.248 1375 1373 0.11 0.13 Isoledene 26.313 1376 1374 0.10 - α-Copaene 26.350 1375 1374 0.97 0.94 β-Cubebene 27.006 1388 1387 0.10 - β-Elemene 27.024 1389 1389 0.14 0.10 Sibirene 27.319 1400 1400 0.11 0.10 α-Gurjunene 27.697 1409 1409 0.33 0.33 Thujopsene 28.444 1429 1429 6.96 6.82 β-Copaene 28.497 1430 1430 0.41 0.38 Aromadendrene 29.005 1440 1439 2.78 2.15 Cedrane 29.088 1441 1441 0.23 0.13 trans-muurola-3,5-diene 29.421 1451 1451 0.10 0.10 α-Humulene 29.495 1452 1452 2.68 2.37 allo-Aromadendrene 29.830 1459 1458 0.83 0.52 trans-Cadina-1(6),4-diene 30.327 1475 1475 0.35 0.24 U-Muurolene 30.528 1478 1478 1.53 1.35 (Continued) PLOSONE|DOI:10.1371/journal.pone.0157107 February21,2017 6/15 PharmacologicaleffectsofCampomanesiaadamantiumessentialoilinvivo Table1. (Continued) Compounds R RI LI Composition(%) t Peel Seed GermacreneD 30.777 1485 1484 2.28 1.43 Widdra-2,4(14)-diene 30.575 1481 1481 0.69 0.53 α-Amorphene 30.660 1483 1483 0.23 0.05 β-Guaiene 31.091 1492 1492 0.35 0.16 Bicyclogermacrene 31.368 1500 1500 4.91 3.83 α-Muurolene 31.404 1501 1500 0.13 0.41 δ-Amorphene 31.903 1512 1511 0.51 0.13 U-Cadinene 32.002 1513 1513 1.31 1.84 δ-Cadinene 32.292 1522 1521 3.55 3.82 Trans-Cadina-1,4-diene 32.692 1533 1533 0.23 0.27 α-Cadinene 32.910 1537 1537 0.17 0.27 Selina-3,7(11)-diene 33.216 1546 1545 0.36 0.16 GermacreneB 33.676 1560 1559 0.47 0.14 Nerolidol 33.760 1562 1561 0.40 - Palustrol 34.072 1569 1567 0.63 0.10 Spathulenol 34.428 1578 1577 1.95 0.14 Globulol 34.993 1591 1590 4.00 - Cubeban-11-ols 35.163 1595 1595 1.18 0.10 Guaiol 35.365 1600 1600 0.60 0.28 Humuleneepo´xiII 35.637 1608 1608 1.04 0.11 Junenol 36.033 1620 1619 0.24 - 1-epi-Cubenol 36.319 1627 1627 1.00 0.23 α-acorenol 36.404 1632 1632 0.66 0.13 epi-α-Cadinol 36.750 1639 1638 0.71 0.18 α-muurolol 37.000 1645 1644 0.11 - β-Eudesmol 37.087 1648 1649 0.69 0.56 α-Cadinol 37.285 1653 1652 0.39 0.10 Valerianol 37.437 1656 1656 0.50 0.18 Allohimachalol 37.585 1661 1661 - 0.50 7-epi-α-Eudesmol 37.603 1662 1662 1.85 - Bulnesol 38.002 1671 1670 0.19 0.10 Eudesm-7(11)-em-4-ol 39.005 1701 1700 0.13 - CompoundslistedinorderofelutionfromaDB-5column.Rt,retentiontime(min);RI,retentionindicesonDB-5capillarycolumn;LI,literatureindices. doi:10.1371/journal.pone.0157107.t001 TheacutetreatmentwithEOPandEOSdidnotinducechangesinfoodandwaterintakeor behavior(irritability,contortion,tremors,convulsions,tearingandfur).Furthermore,the absoluteandrelativeweightofvitalorgansshowednostatisticallysignificantdifferencesin anyofthetesteddoses.Thus,theorallethaldose(LD50)ofEOPandEOSisgreaterthan2000 mg/kgandbothcanbeclassifiedaslowtoxicityoilsaccordingtotheOrganizationforEco- nomicCooperationandDevelopment[19].TheseresultscorroboratedwithSouzaetal.[6] andextendedworkwhopreviouslyhasshownthathydroalcoholicextractofC.adamantium didnotexhibittoxicityinmice,aswellastheessentialoil. Acuteinflammationischaracterizedbyoedema,fever,rednessandpain.Oedemaisan effectivemeasureofinflammationandisusefultoquantifyinducedcutaneousinflammation [20].Carrageenaninducedoedemaisabiphasicmodelwithmultiplemediatorsactingin PLOSONE|DOI:10.1371/journal.pone.0157107 February21,2017 7/15 PharmacologicaleffectsofCampomanesiaadamantiumessentialoilinvivo Fig1.Effectoforaladministrationofessentialoilfrompeel(EOP)andseed(EOS)ininhibition ofleukocytemigrationatbothdosestestedinpleurisytest.Miceweretreatedonehourbeforean intrapleuralinjectionofcarrageenan,withEOSandEOP(100or300mg/kg),dexamethasone(dexa,1mg/kg, s.c.),orsalinesolution(Vehicle).Naivegroup,alsotreatedwithsalinep.o.,receivedanintrapleuralinjection ofsterilesaline.Thebarsexpressthemean±SEMof5animals.*p<0.001whencomparedtocontrolgroup. Differencesbetweengroupswereanalyzedbyanalysisofvariance(one-wayANOVA)followedbythe Newman-Keulstest. doi:10.1371/journal.pone.0157107.g001 Fig2.Effectoforaladministrationofessentialoilfrompeel(EOP)andseed(EOS)fromCampomanesia adamantiunincarrageenan-inducedpawoedemainmice.AnimalsreceivedEOPandEOS(100or300 mg/kg,p.o.)orcontrol(vehicle)ordexamethasone(DEXA,1mg/kg,s.c.)andafter1hanintraplantarinjectionof carrageenan(300μg/paw)forevaluationofpawoedemafor(A)1,(B)2,(C)3,and(D)4haftercarrageenan injection.Eachbarrepresentsthemean±SEMof5animals.*p<0.001whencomparedwiththecontrol group.Differencesbetweengroupswereanalyzedbyanalysisofvariance(one-wayANOVA)followedbythe Newman-Keulstest. doi:10.1371/journal.pone.0157107.g002 PLOSONE|DOI:10.1371/journal.pone.0157107 February21,2017 8/15 PharmacologicaleffectsofCampomanesiaadamantiumessentialoilinvivo Fig3.Effectoforaladministrationofessentialoilfrompeel(EOP)andseed(EOS)fromC. adamantiumfruitsinformalin-inducedpawlicking.EssentialoilofEOSandEOPatdosesof100and 300mg/kgshowsantinociceptiveeffectsinphaseIandIItest.Resultsrepresentmean±S.E.M.(n=6).* P<0.05,whencomparedtocontrolgroup.Eachbarrepresentsthemean±SEMof5animals.*p<0.001 whencomparedtocontrolgroup.Differencesamonggroupswereanalyzedbyanalysisofvariance(one-way ANOVA)followedbytheNewman-Keulstest. doi:10.1371/journal.pone.0157107.g003 sequencetoproduceaninflammatoryresponse.Intheearlyphase,itwasobservedthatEOP andEOSdecreasedcarrageenan-inducedpawoedema.Therewassignificantreductionin oedemaformationafter3hoursofadministrationoftheEOPandEOSwhencomparedwith controlgroup.PrevioustestsperformedwithC.adamantiumleavesextractbyFerreiraetal. [7]alsodemonstratedreducedoedemawhencomparedtothecontrolgroup.Accordingtothe resultsofthisstudy,EOPandEOSseemtoactmainlyontheinitialphaseofthecarrageenan inducedinflammatoryresponse. PlantsfromtheMyrtaceaeFamilyaredistributedacrosstheCerradoregionofBraziland somespecieshavebeenusedtotreatpainandinflammation,amongotherdiseases[6].The PLOSONE|DOI:10.1371/journal.pone.0157107 February21,2017 9/15 PharmacologicaleffectsofCampomanesiaadamantiumessentialoilinvivo Fig4.Effectoforaladministrationofessentialoilfrompeel(EOP)andseed(EOS)fromC. adamantiumfruitsinformalin-inducedcoldsensitivityandoedemainducedbyformalin.(A)Effectof essentialoilsofC.AdamantiumfruitoncoldsensitivityaftertreatmentwithEOPandEOS.(B)Oedema inducedbyformalin.Eachbarrepresentsthemean±SEMof5animals.*P<0.001whencomparedtothe controlgroup.Differencesamonggroupswereanalyzedbyanalysisofvariance(one-wayANOVA)followed bytheNewman-Keulstest. doi:10.1371/journal.pone.0157107.g004 anti-inflammatoryactivityofEOPandEOSinacuteinflammationwasassessedbycarra- geenan-inducedpleurisymodel.Thisisaclassicaltesttoevaluatethistypeofinflammation, forminganexudateinthepleuralcavitycharacterizedbyinfiltrationofpolymorphonuclear leukocytes,andthereleaseofvariouschemicalmediators,whichareimportantintheinflam- matoryprocess[21]. PLOSONE|DOI:10.1371/journal.pone.0157107 February21,2017 10/15

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cology of essential oils from peel (EOP) and seed (EOS) of C. adamantium fruits in animal models. Different tive and toxicological parameters of the essential oil of peel and seed of this fruit, which justify .. is present in the essential oil of Cedrelopsis leaves and essential oils from Citrus u
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