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A fluid response: Alpha-amylase reactions to acute laboratory stressors are related to sample timing and saliva flow rate

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A fluid response: Alpha-amylase reactions to acute laboratory stressors are related to sample timing and saliva flow rate
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  BiologicalPsychology109(2015)111–119 ContentslistsavailableatScienceDirect Biological   Psychology  journalhomepage:www.elsevier.com/locate/biopsycho A   fluid   response:   Alpha-amylase   reactions   to   acute   laboratorystress   are   related   to   sample   timing   and   saliva   flow   rate Tamás   Nagy a , b , ∗ ,René   van   Lien c ,Gonneke   Willemsen c ,   Gordon   Proctor d ,Marieke   Efting a ,Márta   Fülöp e ,György   Bárdos f  ,Enno   C.I.   Veerman g ,    Jos   A.Bosch a , h , ∗∗ a DepartmentofClinicalPsychology,UniversityofAmsterdam,Weesperplein4,1018XA,Amsterdam,theNetherlands b DoctoralSchoolofPsychology,EducationandPsychology,EötvösLorándUniversity,Izabellau.46,1064,Budapest,Hungary c DepartmentofBiologicalPsychology,VUUniversity,VanderBoechorststraat1,1081BT,Amsterdam,theNetherlands d Mucosal&SalivaryBiologyDivision,King’sCollegeLondonFloor17,Guy’sTowerGuy’sHospitalLondonSE19RTUK  e InstituteforCognitiveNeuroscienceandPsychology,ResearchCentreof    NaturalSciences,HungarianAcademyofSciences,MagyarTud´osokk¨or´utja2, BudapestH-1117,Hungary f  InstituteofHealthPromotionandSportSciences,BogdánffyÖdönu.10,Budapest,H-1117,Hungary g DepartmentofOralBiochemistry,AcademicCentreofDentistry(ACTA),GustavMahlerlaan3004,1081LA,Amsterdam,TheNetherlands h MannheimInstituteof    PublicHealth,SocialandPreventiveMedicine(MIPH),UniversityofHeidelberg,Ludolf-Krehl-Straße7-11,D-68167,Mannheim,Germany a   r   t   i   c   l   e   i   nf   o  Articlehistory: Received4February2014Accepted25April2015Availableonline12   May   2015 Keywords: Alpha-amylaseSalivaryflowrateAcutestressSalivaSympatheticnervoussystemParasympatheticnervoussystem a   b   s   t   ra   ct Salivary   alpha-amylase   (sAA)   is   used   as   asympathetic   (SNS)   stress   marker,thoughits   releaseislikelyco-determinedby   SNS   and   parasympathetic   (PNS)activation.   TheSNS   and   PNS   showasynchronous   changesduring   acute   stressors,   andsAA   responses   may   thus   varywithsample   timing.Thirty-four   participantsunderwent   aneight-minutememorytask(MT)   andcold   pressor   task   (CPT).CardiovascularSNS   (pre-ejection   period,bloodpressure)   andPNS   (heart   rate   variability)   activityweremonitored   continuously.Unstimulated   salivawas   collected   repeatedly   during   andafter   each   laboratorystressor,   andsAA   concentration   (U/ml)   andsecretion   (U/minute)   determined.Both   stressors   increased   anxiety.TheMT   caused   an   immediate   and   continuedcardiac   SNS   activation,but   sAA   concentration   increasedattask   cessationonly   (+54%);   i.e.,whenthere   wasSNS–PNSco-activation.During   the   MTsAA   secretionevendecreased   ( − 35%)   inconjunctionwith   flowrate   andvagal   tone.TheCPT   robustly   increasedblood   pressurebutnot   sAA.In   summary,   sAAfluctuations   did   notparallelchangesincardiac   SNS   activityor   anxiety.   sAA   responsesseem   contingent   onsampletiming   and   flow   rate,   likely   involving   bothSNS   andPNS   influences.   Verifica-tion   using   other   stressors   and   contexts   seems   warranted.©2015   ElsevierB.V.   All   rights   reserved. 1.Introduction Thediscoverythattheadrenalstresshormonecortisolcanbemeasuredreliablyandnon-invasivelyinsalivawasamethod-ologicalbreakthroughin   stressresearch,andmuchefforthassincebeendedicatedtodetermineiftheassessmentof    other ∗ Correspondingauthorat:DoctoralSchoolof    Psychology,EducationandPsychol-ogy,EötvösLorándUniversity,Izabellau.46,1064,Budapest,Hungary.Tel.:+36306276313. ∗∗ Correspondingauthorat:DepartmentofClinicalPsychology,FacultyofSocialandBehavioralSciences,Universityof    Amsterdam;Weesperplein4,1018XA,   Ams-terdam,TheNetherlands.Tel.:+31205256819. E-mailaddresses: nagy.tamas@ppk.elte.hu(T.   Nagy), J.A.Bosch@uva.nl(J.A.Bosch). neuro-endocrinemarkersmay   benefitfromtheeaseof    salivacol-lection.Asa   promisingcandidate,salivaryalpha-amylase(sAA)hasgainedrapidpopularityasa   noninvasivemarkerof    sympa-theticnervoussystem(SNS)activity(Granger,Kivlighan,El-Sheikh,Gordis,&Stroud,2007;Nater&Rohleder,2009;Rohleder&Nater,2009).sAAisa   digestiveenzymethatbreaksdownstarchintoglucoseandmaltose,andenzymaticactivity(inUnits/ml)is   usedasa   proxyforsAAconcentration. 1 Theuseof    sAAasa   markerof    SNSactivityseemsjustified:sAAreleasefromthesalivaryglandsisunderstrongcontrolof    localsympatheticnerves(Proctor&Carpenter,2007),itssalivaryconcentrationrapidlyincreases 1 sAAconcentrationis   inferredfromtheamountof    enzymethatcatalyzestheconversionof    1  mol   ofsubstrate(i.e.,startch)per   minute.http://dx.doi.org/10.1016/j.biopsycho.2015.04.0120301-0511/©2015ElsevierB.V.All   rightsreserved.  112 T.Nagyetal./BiologicalPsychology109   (2015)111–119 duringacutestress,anditsuseasa   markerofsympatheticacti-vationisalsovalidatedbypharmacologicalstudies(Boschetal.,1998;Bosch,deGeus,Veerman,Hoogstraten,&NieuwAmerongen,2003;Ehlert,Erni,Hebisch,&Nater,2006;Takaietal.,2004;vanStegeren,Rohleder,Everaerd,&Wolf,2006;vanStegeren,Wolf,&Kindt,2008).WhereasitisundisputedthatsAAreleaseis   undersympatheticcontrol,theinferencethatincreasesin   sAAthereforesignifysym-patheticactivationis   nonethelessproblematic.Theinferenceislogicallyflawed(i.e.,affirmingtheconsequent),andtherearealsostrongempiricalargumentsto   questionthisinference(c.f.Bosch,Veerman,deGeus,&Proctor,2011).Mostof    theseargumentscenteraroundthefactthattheparasympatheticnervesalsoplaya   signif-icantroleinsAArelease.Forexample,severalsAA-richsalivaryglands,likethesublingualandminorglands,arealmostexclu-sivelyunderparasympatheticnervoussystem(PNS)control(Boschetal.,2011).Further,experimentalstudiesshowthatthesympa-theticeffectsonsAAreleasearestronglymoderatedbyconcurrentPNSactivity,aphenomenondenotedas‘augmentedsecretion’(seeProctor&Carpenter,2007).Inordertobetterunderstandthedifferentialcontributionof thePNSandSNStosAAresponsesduringstress,wehaveprevi-ouslycomparedsAAsecretioninresponsetostressorsthatelicitdistinctpatternsof    autonomicactivity(Boschetal.,   2003).Itwasfoundthatastressorelicitingsympathetic-parasympatheticco-activation(i.e.,viewinga   surgicalvideo)causeda   markedsAArelease(+65%),whereasacognitivestressorcausinga   sympatheticactivationinconjunctionwithparasympatheticinhibition(i.e.,   amemorysearchtask)showedno   significantchangein   sAArelease(+10%).Importantly,thelatterstressorcausedamuchstrongersympatheticactivation(asmeasuredbycardiacPEP,LVET,andbloodpressureresponses)thanthestressfulvideo(Boschetal.,2003).ThesefindingsthereforeareinconsistentwiththeideathatsAAreliablyrepresentsSNSactivity,andconsistentwithamod-eratingeffectofparasympatheticactivity(Berntson,Cacioppo,&Quigley,1991;Proctor&Carpenter,2007).Onthebasisthat   sAAreleaseis   orchestratedbyjointactivityof    thetwoautonomicbranches,we   predictedthatsampletim-ingmay   becriticaltotheobservedsAAresponsesduringstress.Thispredictionbuildsonknowledgethat   activityin   theauto-nomicbranchesisasynchronousoverthecourseofanacutestressor,wherebythePNStendstoexhibitafasteroffandonsetthantheSNS(Berntsonetal.,   1997;Berntson,Quigley,&Lozano,2007;Somsen,Jennings,&VanderMolen,2004).Studieshaveshown,forexample,thatthePNSwithdrawalduringacutestressrapidlyrestoresimmediatelypost-stress,atwhichtimesympa-theticactivationstilllingers(seeBerntsonetal.,2007).Somehaveevenreporteda   parasympatheticreboundimmediatepost-stress,wherebyPNSactivityovershootsbaselinelevels,causinga   tran-sientsympathetic-parasympatheticco-activation(Mezzacappa,Kelsey,Katkin,&Sloan,2001;Rottenberg,Wilhelm,Gross,&Gotlib,2003).Hence,wepredictedthatthelargestsAAincreasewillbeobservedimmediatelypoststress,whenthePNSwillhavelittleeffectorpossiblyevenanaugmentingeffectonsAA,andwe   furtherpredictedthatthesmallestsAAchangeswillbeobservedduringstress,whenSNSeffectsonsAAmaybeattenuatedbya   PNSwith-drawal.ItisnoteworthythatnearlyallpublishedstudieshaveonlysampledsAAatstressortermination,andthestudybyBoschetal.(2003)–whichfoundnoeffectof    a   cognitivestressoronsAArelease–collectedsalivaduringthestressor.Thepresentstudyhadonefurtheraim:to   addresstherole   of salivaryflowrateasafactorrelevanttosAAstudies.TheuseofsAAasaSNSmarkerisbasedonthefactthatsAAsecretion(U/min)isunderSNScontrol.However,moststressstudieshaveinsteadmea-suredsAAconcentration(U/ml)(Boschetal.,2011).Theimplicitassumptionthatthesetwoparametersyieldidenticalresultshasremainedlargelyuntested(Beltzeretal.,2010;Proctor&Carpenter,2001;Rohleder&Nater,2009).Asshownintheformulabelow, 2 salivaflowrate(ml/min)isthesole   determinantof    therelationshipbetweensAAsecretionandconcentration,andflowrateisalmostexclusivelyunderparasympatheticcontrol(Garrett,1987;Proctor&Carpenter,2007).   Accordingly,sAAconcentrationmay   provideanoverestimationof    sAAsecretionwhensalivaryflowratedecreases–reflectingreducedPNSactivationofthesalivaryglands–butmayprovideanunderestimationwhensalivaflowrateincreases.Thisaspectofglandularphysiologymay   alsohaveclearimplica-tionsforsampletiming:duringacutestress,whenPNSactivityshowsa   strongwithdrawal,thelargesteffectsonflowratecanbeanticipatedandherebythelargestdiscrepancybetweensAAcon-centrationandsecretion(Bosch,Ring,deGeus,Veerman,&NieuwAmerongen,2002;Boschetal.,2011).In   lightof    theprecedingdiscussion,thepresentstudyexaminedthetemporaldynamicsof    sAAduringtwo   acutelaboratorystress-orsknowntoelicitdistinctautonomicnervoussystemresponses:i.e.,amemory-searchtask(MT)anda   coldpressortask(CPT)(Boschetal.,   2001,2003;Willemsenetal.,1998;Willemsen,Carroll,Ring,&Drayson,2002).TheMT   elicitsa   prototypical‘fightor   flight’cardiacautonomicresponsepattern,characterizedbya   vagalwithdrawalandenhancedsympatheticdrive.Incontrast,theCPTprimarilyelic-itsa   localizedvascularsympatheticactivationcharacterizedbyarobustbloodpressureresponse,but   elicitslittlecardiacautonomicchange(Allenetal.,1992;Willemsenetal.,   1998,2002;Winzeretal.,   1999;Ringetal.,   2000),andthedataonsAAaremixed(seediscussion).WeanticipatedthelargestsAAincreaseatstressoroff-set,whenautonomicbalanceis   shiftedtowardsSNS–PNSco-activation,andweexpectedthesmallestsAAchangesduringthestressor,whenparasympatheticwithdrawalmay   attenuatesym-patheticeffectsonsAAsecretion.WeexpectedsAAduringCPTto   increaseinparallelwithpain,anxietyandpressorresponses.AutonomicresponsesduringCPThaverarelybeendeterminedbeyond3min   (Mourot,Bouhaddi,&Regnard,2009)andthisisthefirststudytoinvestigatethetemporaldynamicsof    sAAreleaseduringCPT.Correlationanalyseswereperformedtoexploreassoci-ationsbetweenglandularresponsesandcardiovascularautonomicindices. 2.Method  2.1.   Participants Thirty-fouruniversityundergraduates(ofwhich18weremales)volunteeredtotakepartinthestudy(Meanage=22.1yr,   SD=   3.2;MeanBMI   =21.7kg/m 2 ,range:17.7–28.3).Participantsreceivedstudycreditsfortheirparticipation.Inclusioncri-teriawere:(a)   nocurrentmedicaltreatmentorprescribedmedication,(b)nosignsof    coldsor   upperrespiratorytractinfectioninthepasttwo   weeks.Participantssignedinformedconsent,andtheresearchprotocolwasapprovedby   thelocalethicscommitteeof    theVrijeUniversiteit.  2.2.   Procedure Inpreparation,participantswereinstructedtorefrainfromusingalcoholornonprescriptiondrugs24h   beforetesting.Participantswereaskednotto   deviatefromtheirusualsleepinghabitsonthepreviousnight,avoidvigorousexerciseonthedayoftheexperiment,andtoabstainfromsmoking(fiveparticipantsreportedtobesmokers),drinkingcaffeinatedbeverages,eating,andbrushingteeth(topreventgingival   bleeding)onehourpriortotheexperiment.Women   werescheduledwithinthe   sevendaysaftertheirmenses.Compliancewithinstructionswasverifiedbyadetailedhealthbehaviourquestionnaire.Experimentsweresetbetween13:30and16:00   tominimizecircadianeffects(Nater,Rohleder,Schlotz,Ehlert,&   Kirschbaum,2007).Onarrival,theexperimentalprocedurewasexplainedtotheparticipantandelectrodesforelectrocardiography(ECG)andimpedancecardiography(ICG)wereattached.Afterrinsingthemouthwithtapwater,participantswerefamiliarizedwiththesaliva-collectionprocedureandfilledoutquestionnaires,followedbya 2 sAAsecretion(U/min)=sAAconcentration(U/ml) ×   salivaryflow   rate(ml/min).  114 T.Nagyetal./BiologicalPsychology109   (2015)111–119 ****** 253035404550Baseline Stressor Recovery    S   T   A   I  -   S  s  c  o  r  e Memory-search task Cold pressor task Fig.1. Anxietyscores(Mean ± SE)duringbaseline,task,andrecoveryphasesof Memory-searchtaskandColdpressortask.  ***  p <.001,representingdifferencefrombaseline. showninTable1andFig.2,theMT   evokedtheexpectedpat-ternofincreasedsympatheticactivation(evidencedbyreducedPEPandincreasedbloodpressure)anda   vagalwithdrawal(reducedRMSSD).AtMT   offset,RMSSDwasrestoredto   baselinevalueswhereasPEPwasstillsignificantlyshorter,indicatedongoingsym-patheticactivation.Inlinewithpriorresearch,theCPTshowedlittleeffectonheartrateandcardiacautonomicmeasures(SeeTable1),butexhibitedarobustincreasein   bloodpressurethatwas   similartothebloodpressureincreaseduringtheMT.   Forbothtasks,car-diovascularparametersreturnedtobaselinelevelswithin5minafterstressortermination.Adjustingfortaskorder,gender,BMIorsmokingdidnotalteranyof    thereportedresults(seeonlinesupplement).  3.2.Salivaryparameters 3.2.1.Salivaryflowrate Salivaryflowrateresponsesarepresentedin   Fig.3.   RepeatedmeasuresANOVAyieldeda   significantTask × Timeinteraction( F  (5,145)=16.23,  p   <   .001,  p  2 =   .35)showinga   differentpatternofchangeforthetwostressors.SeparateanalysesofeachtaskshowedthatMT   clearlyalteredflowrate( F  (5,160)=45.77,  p   <001, ε =.76,  p  2 =.59).FlowratedecreasedfrombaselineduringtheMT   ( − 55%and − 56%at3.5and7min   respectively; t  (33) = 7.99and6.99,respectively,  p s<.001)whichwasfollowedbya   modestreboundabovebaselinelevelsatstressoroffset(+22%, t  (33)= − 3.88,  p <.001).TheCPTdidnotsignificantlyaffectsalivaryflowrate( F  (5,160)=   1.00,  p   =   418,  p  2 =.03).Maleshada   higheraveragesali-varyflowratethanfemales( F  (1,29)=   9.27,  p   =   .005,  p  2 =.24),butadjustingforsexdidnotaltertheresults.Exploratoryanalysesdidnot   identifyotherpotentialconfounders(seeonlinesupplement).  3.2.2.Salivary ˛ -amylaseconcentration As   canbeseenonFig.4,theeffectof    thetwotaskswasdifferentonsAAconcentrationovertime,yieldingasignificantTask × Timeinteraction( F  (5,150)=5.90,  =   .67,  p =.001,  p  2 =.16).Separateanalysesofeachtaskyieldedasignificantincreasefrombaselineof    sAAconcentrationin   MT   ( F  (5,155)=10.60,  p   <   001, ε =   .61,  p  2 =.26).Post-hocanalysesshowedthatduringtheMTsAAconcentrationdidnotchange(  p s>.90),   andshowedasignif-icantincreaseatstressoroffset(+54%, t  (33)=   − 6.28  p   <   .001),andsubsequentlyreturnedto   baselinelevels(ts<   .81,  p s>.35forrecov-ery).TheCPTdidnotsignificantlyaffectsAAconcentration( F  (5,155)=   1.01, ε =   .68,  p   =.396,  p  2 =   .03).Exploratoryanalysesshowednoresponsedifferencesrelatedto   covariates(seeonlinesupple-ment).  3.2.3.Salivary ˛ -amylasesecretion As   canbe   seenin   Fig.   5,   thetwo   taskseliciteddifferentsAAsecretionpatterns,yieldinga   significantTask × Timeinteraction( F  (5,145)=22.18,  p   <   .001,  p  2 =.43).SeparateanalysesofeachtaskresponseshowedthatMTelicitedsignificantchangesin   sAAsecretion( F  (5,150)=35.63,  p <.001, ε =   .69,  p  2 =   .54),wherebysAAsecretionwasdecreasedfrombaselineduringMT   ( − 43%and − 31%, t    (31)=   5.81and5.95,respectively,  p s<   .001),followedbyarapidincreaseabovebaselinevaluesatstressoroffset(+60%, t  (33)= − 5.92,  p <   .001);duringrecoverysAAsecretionreturnedtobaselinevalues(ts= − 1.36and − 0.63,  p s>   .180).TheCPTdidnotsig-nificantlyaffectsAAsecretion( F  (5,155)=0.51,  p   =   .770,  p  2 =   .02).Men   showeda   highersAAsecretionthanwomen( F  (1,27)=   9.87,  p   =   .004,  p  2 =.27),whichisexplainedbyhighersalivaryflowratesinmen.However,adjustingforsexdidnotaltertheresults(seeonlinesupplement).  3.3.Correlationalanalyses TheincreaseinsalivaryflowrateatMT   offsetcorrelatedposi-tivelywithRMSSDchange( r  (33)=   .56,  p   =   .001),supportingtheideathatenhancedparasympathetictonewasassociatedwithincreasedflowrate.Thisfindingwas   replicatedfortheassociationbetweenRMSSDandsAAsecretion( r  (33)=   .43,  p =.01),butnot   forRMSSDandsAAconcentration.NoassociationswereobservedbetweenPEPchangesandchangesinsalivarymeasuresatanyof    thetimepoints.RelativechangesinsAAconcentrationandsAAsecretionweresignificantlycorrelatedatalltimepoints;correlationcoefficientswere.65,.76,.66,.71,and.56duringCPT,and.59,.61,.63,.57,and  Table1 Statisticalresultsforcardiovascularresponses.Task × TimeinteractionMemorytasktimeeffectColdpressortasktimeeffectMeasureStatistic  p  2 Statistic  p  2 Statistic  p  2 SBP F  (6,156)=   2.46 * .09   F  (6,168)=   6.79 *** .20 F  (6,180)=7.88 *** .21DBP   F  (6,156)=   1.20, ε   =.66.04   F  (6,168)=   11.60 *** , ε   =   .67.29 F  (6,180)=5.52 *** , ε   =   .72.16HR    F  (6,192)=   16.91 *** , ε =   .45   .35 F  (6,192)=   5.32 *** , ε =   .33.36 F  (6,192)=2.23, ε   =   .69.07RMSSD   F  (6,192)=   17.31 *** , ε =   .63   .35 F  (6,192)=   15.96 *** , ε =   .66.33 F  (6,192)=1.82, ε   =   .63.05PEP   F  (6,186)=   4.93 ** , ε   =   .55.14 F  (6,186)=   8.44 *** , ε =   .64.21 F  (6,186)=1.81, ε   =   .51.06 Note :MT:   Memory-searchTask,CPT:ColdPressorTask,SBP:Systolicbloodpressure,DBP:Diastolicbloodpressure,HR:Heartrate,RMSSD:Rootmeansquareofsuccessivedifferences,   PEP:Pre-ejectionperiod. F    valuesrepresentwithin-subjecteffectswithadjustmentfortaskorder. *  p <.05. **  p <.01. ***  p <.001.  T.Nagyetal./    BiologicalPsychology109(2015)111–119 115 Fig.2. Cardiovascularparameters(Mean ± SE)duringMemory-searchtaskandColdpressortask.Asterisksindicatesignificantpair-wisedifferencesfrombaselinevaluesrespectively,usingSidakcorrection;thetimingson   thex-axisindicatethe   endof    each2-minECG/ICGepoch.  **  p <.01,  ***  p <.001. .55duringMT   (all  p s   ≤ .001for3.5,7,8.5(offset),+8,and+20min,respectively). 4.Discussion Forthepresentstudyitwaspredictedthatsampletimingmaybeanimportantdeterminantof    sAAresponsesto   stress,andthisideawastestedbycomparingsAAresponsesduringtwo   stress-orsknowntoelicitdistinctpatternsof    cardiacautonomicactivity.Theresultsappearedconsistentwithexpectations:overthecourseofacognitivestressor(MT)anincreaseinsAAwas   evidentatstressoroffsetonly.Moreover,duringthisstressorsAAconcentra-tionwasvirtuallyunaffectedandsAAsecretionevendecreased,despiteevidenceofconsistentandrobustsympatheticactivation(i.e.,decreasedPEP,increasedBP).ThesefindingsindicatethatsAAincreasesuponstressortermination–themeasurementtimepointusedin   moststudies–may   notberepresentativeof    whatishappen-ingduringstress.AlsonotableisthattheCPThadlittleeffectonsAAlevels,althoughparticipantsreportedpainandshoweda   markedincreaseinanxietyaswellasvascularsympatheticactivation(i.e.,elevatedbloodpressure).Further,thechangeof    sAAandPEPdidnotcorrelateatanytimepoint.Overall,theseresultssuggestthattheinterpretationofsAAasa   markerofstress/arousalor   sympatheticactivityis   lessstraightforwardthanperhapsassumed,andtheroleof    concurrentparasympatheticactivity(relatedtoaspectslikemea-surementtimingandsalivaflowrate)warrantmoreattentioninfuturestudies.Thepresentstudyalsoaimedtoaddresstheongoingdebateonthepossibleconfoundingroleof    salivaryflowratein   deter-miningsAAconcentration.Theempiricalliteraturehasbeen
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