AGGRESSIVEBEHAVIOR Volume20, pages17-26 (1994\ Intakeand Aggressiveness: Testosterone RealEffector Anticipation? Kaj Bj6rkqvist,Tor Nygren,Ann-ChristinBi6rklund,and Stig-EyrikBj6rkqvist Depaftmentof SociatSciences, AboAkademi university,Vasa,Fintand (40 In a double-blindexperiment,human males(n = 27\ weregiveneither testosterone mg/day), placebo,or no treatment, over a one week period. Subjectiveand observer mood estimationswere conductedbeforeand after treatment. Testosteronelevels assessed in saliva were measuredwith radioimmunoassay.The results revealeda signilicant placebo effect [c.f. Medicine and Sciencein Sports 42124-126]:After treatment, the placebo group scored higher than both the testosteroneand the control group on self-estimated anger, irritation, impulsivity, and frustration. Observer-estimatedmood yielded similar results. The lack ofa placebo effect in the testosteronegroup is intriguing, and may be due to secondary effectscausedby suppressionof the body's own testosterone production, since recorded non-protein bound testosteronedid not significantly rise due to treatment. The results suggestthat androgen usagecausesexpectations,rather than Inc. an actual increaseofaggressiveness. tj 1994wiley-Liss, Key words: testosterone,aggression,radioimmunoassay,mood, steroids INTRODUCTION by sportsmen abusing anabolic of homicidecommitted steroids Reports are,every now and then, presentedin the newsmedia. Such casesare typically describedas having no apparentmotive and as accompaniedby uncontrolled fits of rage. In 1984, a Finnish athletewho killed his girlfriend blamed the usageof steroidsfor his irrational behavior. That same year,a steroid-usingSwedishathletekilled his best friend, and on December 6, 1992, a TV news report on TV announcedthat a Swedish steroid abuser had shot and injured six people. These are but examples,and similar instancescan easily be found in countriesoutsideScandinavia. June9. 1993. for publicationMay 9, 1993:accepted Received of SocialSciences,Abo ekademiUnivenity.Virrigatan to Kaj Bjirrkqvist.Department Addressreprintrequests 9. SF-65100Vasa.Finland. @ 1994Wiley-Liss' Inc. 18 Bjdrkqvisret al. The mediapresentthe connectionbetweenthe useof steroidsandaggressiveness as if it werea well established fact.The pressandTV, naturally,do not reportabusersnot killing or not becomingaggressive. Likewise,whennon-abusers commithomicideor someotherviolentcrime,theprefix "non-abuser"is not containedin thereport.Negativecasesand falsepositivesneverpassthe newsthresholdand thus,everyreported incidentearnsdisproportionate coverage. It hasneverbeenshownthatathletesabusing steroidscommithomicidesignificantlymoreoftenthannonabusing athletes,andeven if this weretrue, it wouldnot be proofof a cause-effect relationship. overthe useof anabolicsteroidshasunquestionably Controversy createda greatdilemmain the world of sports.Alreadytwo decadesago,Coopertl972l reportedthat 80Vaof weightlifters,javelin throwersand shot-putters regularlyusedillegalsteroids. Recentcases,suchas Ben JohnsonandKristinaKrabbe,indicatethat steroidusageis now commonamongshort distancerunners,too. Whethersteroidintakereally improvesperformance hasnot beenscientificallyestablished, althoughsportsmenseeking fastrecoveryafterintensivetrainingandrapidmuscledevelopment seemconvinced that it does[e.g., Lucking, 1982;Perryet al., 1990].In a double-blindexperiment, Freedet al. [975] found a slight improvementin the performance of weight lifters. The only changein physicalperformance Hannanet al. [991] couldestablishwasan improvementin the first trial of a pegboardtask.Ariel and Saville11972)foundplaceboto be moreeffectivethansteroids. The relationshipbetweentestosterone levelsand aggressionin subhumanspecies hasbeenstudiedextensively,and findingssuggesta connectionbetweenthe two [for reviewssee,for instance,Bouissou,1983,and Brain, 19771.Castrationis known to reducephysicalaggressionamonganimals,includingsubhumanprimates[Bernstein et al., 1983].Thereare,however,goodreasonsto believethatlevelsoftestosterone are primarilyrelatedto socialstatusand dominance.Rejeskiet al. [988] gaveinjections of testosterone to an experimentgroupof malecynomolgusmonkeys,while a control groupreceivedshaminjections.Althoughtheadministration of testosterone resultedin a significantincreasein aggression,more importantwas the finding that changesin behaviorare mediatedby socialstatus;the incidenceof both contactand noncontact aggression in dominantmonkeyswasfar greaterthanthe frequencyof thesebehaviors in subordinate monkeys[Rejeskiet al., I 988]. As far ashumansareconcerned,the questionof whetherthe levelof testosterone in malesis relatedto aggressionis moreopento debate.While somestudiesindicatea relationship,othersdo not. For example,Olweuset al. [980] founda correlationbetweenunboundplasmatestosterone andcertainaspectsof aggressiveness andimpulsivity. Ehrenkranzet al. [974] usingprisonersas subjects,foundplasmatestosterone to be correlatednot only with aggression, but with socialdominance,too. Radaet al. |9741 investigated plasmatestosterone levelsin rapistsbut werecautiousaboutinterpreting theirresultsasindicatinga causalrelationship with rape.Lindmanet al. |9921did not find a correlationbetweenserumtestosterone levelandaggression in malesarrested for spouseabuse,neitherat thetime of arrestnor in a sobercontrolstate. Theseexamplesshowthat somestudiesdo indicatea relationship betweentestosterone and aggressiveness, othershavefailedto find a correlation.It is well knownthat positiveresultsaremorereadilypublishedthannull findings,andmanyresearchers do not evenbotherto submit manuscriptsreportingnonconfirmedhypotheses. Accordingly,manystudiesinvestigating thetestosterone-aggression yieldinga negarelationship tive resultarelikely neverto havebeensubmittedand/orpublished. Intal<e Testosterone 19 In view of the inconsistentfindings of researchon this topic, the conclusionsdrawn by reviewersalso tend to be in disagreement.While some claim that a connection can be established[e.g., Donovan, 1985], others [such as Benton, 1992]are of the opinion that, on the basis ofexisting data, there is no reasonto suggestthat human aggression is related to level of testosterone.Benton [983a, 1983b] emphasizedthat the claim of a relationship between testosteroneand aggressionis based primarily on animal data. Extrapolationsfrom animal to human behaviorare questionable,since, among humans, social and cognitive mechanismsplay a much greater role than physiological factors. The closer animal is to man on the phylogenetic scale, the smaller the influence of testosteroneon aggression.Benton's |9921conclusion is that in man, aggressivebehavior is a reflection of psychosocialhistory, and differencesin aggressivenesscan be attributedto the level of testosteroneonly to a very limited extent, if at all. If Benton is correct-and the presentauthors think he is-then the main source of variation in aggressiveness among humans is really to be found in the psychohistoryof the individual. What, then, is the explanationfor the immenseinterestin the testosteroneaggressionconnection? Is it primarily a reflection of hardy attitudes about the aggressive male and the submissivefemale, still prevalentwithin our society? If males within subhumanvertebratespeciesare more aggressivethan females(which is not true for all species) [Adams, 1992], among humans, this seemsto be reflected only in greaterphysical aggression.In regard to direct verbal aggression,human females are as aggressiveas males, and with respectto indirect aggression,evenmore so [Bjokqvist etal.,1992a; Bjorkqvist etal.,1992b; Lagerspetzetal., 1988].The greater amount of physicalaggressionamong males is more likely to be a consequenceof learning mechanismsand greater physical strength, rather than of testosterone[Bjorkqvist and Niemelii, 19921. Most researchon aggressionis conductedby men, with male subjects,perhapsre"male" perspective on the subject. For instance,Frodi et al. |977) sulting in a biased, found that of 314 experimentalstudieson aggression,54Vowere concernedexclusively with men, and only 87ocould be found specifically investigatingaggressionin women. Another revealing example is the different interest arousedby two experimentsconducted by Edwards [Edwards, 1969, and Edwards and Herndon, 19701.In Edwards [969] , it was reported that female mice treated with androgens at birth were more aggressiveas adults. This result is well-known and well-publicized. The secondstudy [Edwards and Herndon, 1970] showedthat newbom female mice treated with estrogen at birth also fought more as adults! This finding has gone almost unnoticed, since it is not in accord with the generally accepted. The aim of the present study was to investigate whether there is any truth in the reports of increasedinitability and aggressivenessin males after steroid intake [Perry etal., l990l.Thestudywasadouble-blindexperiment.Thesubjects,universitysportsmen who volunteeredfor the experiment, were divided into three groups: testosterone, placebo, and no treatment. Testosteronewas administeredperorally for one week. The dose (40 mg/day) was well within the levels administeredfor therapeuticreasonsand, taken for such a limited period, the treatment could not possibly cause the subjects physical harm. The subjects were, however, under strict medical supervision for the duration of the experiment. There are findings suggestingthat it is the level of non-protein-boundtestosterone which is decisive in behavioral manifestations[cf. Vermeulen and Verdonck, 19'12]. Unbound testosteroneconstitutes l-4%oof the total level [Sannikka et al. , 1983]. In the 20 Bjdrkqvisteral. presentresearch,unboundtestosteronelevelswere measuredwith radioimmunoassay of the saliva,beforeand after the treatmentperiod [Furugyamaet al., 1970;deGomez et al., l98l; Ismailet al., 19721.This methodoffersa morebenignwayof measuring in salivacorrelatehighly with the than blood sampling.Measurements testosterone level: .75 accordingto Sannikkaet al. [983], serumtestosterone non-protein-bound to Wanget al. [1981]. and.94according In the presentexperiment,pre- and-posttreatmentbehavior,mood, and physicalfitandobserver-evaluated includingself-estimated by multiplemeasures, nesswereassessed behavior,and interviews.Each subjectwas observedin a mood, observer-estimated werevideotaped.In this papel groupsituationwith two other subjects.All sessions only theeffectof treatmenton moodwill be reportedin detail. MATERIALSAND METHODS Subjects universitystudents,all males,andall but oneactivein sports,particiTwenty-seven patedin the experiment.Most of them weremembersof the sportsassociationof Abo for the experiment,and reAkademiUniversity,Turku, Finland.All had volunteered of 100,-FIM for their participation.Their meanagewas23.9 ceiveda remuneration years(agerange2 I -3 I years). The meanweight of the subjectswas 73.6 kgs (range 62-88 kgs), and the meanheightwas 180.3cm (range170-197cm). None of them or other steroids.Subjects admittedto havinghad pesonalexperienceof androgens groups: placebo, and control, on the testosterone, were divided into three treatment in the saliva.The main criterionfor selection basisof matchedlevelsof testosterone wasthat the testosteronelevel of the threegroupsshouldcorrespondascloselyas posthat therewereno sible.The physicianconductinga medicalexaminationto ascertain for the selection participation experiment was responsible in the medicalobjectionsfor interview andperwere also checked by counterindications of subjects.Psychological possible precaution were rejected. Every volunteers, three Of 30 sonalityassessment. wastaken,bothprior to andduringtheexperiment,to ensurethatsubjectswouldcome wereignorantas to which groupeachsubject to no harm. The actualexperimenters designof thisexperiment. with the double-blind accordance belonged,in Sessions The subjectsattendedthreesessionsin the laboratory:Thesewill be referredto as I and II wereseparatedby2 to 3 weeks, Sessions I, II, and II[, respectively. sessions periodbetweensessions II andIII wasl0 days.Testosterone/placebo andthe intermediate data, intakebeganexactly7 daysbeforesessionIII. SessionII deliveredpre-treatment datawereobtainedfrom sessionIII. andpost-treatment Testosteroneand Placebo producedby consistedof 40 mg pills of Panteston@, testosterone The administered perorally,i.e., it hasto be kept underthe tongue is administered Oregon.Panteston until dissolved,it is not to be swallowed.Administeredperorally,it worksthroughthe lymphaticcirculationand is not brokendown by the liver.The placebopills werecalin thesameway. pills which wereadministered cium carbonate TestosteroneIntakc 2I Radioimmunoassay (RlA) of the Saliva Subjectsdelivered 5 ml saliva into a test tube after first rinsing their mouth with pure water and then chewing on a parafilm in order to stimulate the secretionof saliva. The delivery alwaystook place at the sametime ( 19.00) in order to avoid differencesdue to circadian rhythm. The samples were immediately frozen and stored until the time of actualanalysis.Analysiswasconductedaccordingto the methoddescribedby Sannikka etal. [ 19831. The Self-Estimated Mood Check List The mood check list utilized successivemagnitudescales[Lindman, 1985]. Subjects were requestedto indicate the degree to which they confirmed experiencing certain moods (e.g. relaxed)on a straight 100 mm line, with zero confirmation at one end. and 1007oconfirmationat the other. Twelve items (expressingmood) were included:Relaxed,irritated, excited, angry, indiff'erent. interested,frustrated,elated,nervous,impulsive,self-confident,andactive. Observer-Evaluated Mood All sessions,except for the medical examination, were videotapedfor the subsequent assessmentof subjects' mood during the sessionby two independentobservers. The observerswere unawareof the group to which subjects belonged. A similar sucmood check list cessivemagnitudescaleand the same l2 items as in the self-evaluated wereused.The inter-raterreliability was .86 (P < .01). Session I The sole purposeof the first sessionwas to investigatethe psychologicaland medical suitability of those volunteeringfbr the experiment. SessionI consistedof four parts: l) delivery of saliva fbr the RIA test, 2) a medicalexamination,3) an interview, 4) personalityassessment. datafor alloThe purposeof the salivasamplewas to establishbaselinetestosterone cation into groups.The purposeof the medicalexaminationwas to investigatemedical were conductedin order suitability.while the interviewand the personalityassessment to test fbr psychologicalcounterindicationsto participation in the study. Three subjects were excluded on basis of medical and psychologicalgrounds. The whole session, exceptfbr the medicalexamination,was videotaped. Session ll The subjects were taken to the laboratory in groups of three. each from a different no treatment)group.The sessionconsistedof two parts: treatment(testosterone/placeboi l) completion of the self-estimatedmood check list, to obtain pre-treatmentdata on mood, 2) a physicalperfbrmancetest. The whole sessonwas videotaped self-estimated for subsequentobserverassessmentof subjects' mood. Physical performancewas evaluated during sessionII, fbr comparisonwith post-treatmentperformanceduring session il1. by exercisesdemandingphysicalstrengthas well as fine motor skills. Subjects 3 daysafter sessionII, and 7 daysbeforesessionIII. startedtaking testosteroneiplacebo Session lll SubjectsattendedsessionIll in a different group of three to that of sessionII. The ) d e l i v e r y o f s a l i v a t b r R l A ( a t e x a c t l yl 9 : 0 0 ) , 2 ) c o m p l e t i o n o tf h e s e s s i o n i n c l u d el d 22 Bjdrkqvistet al. self-estimatedmood check list (post-treatmentdata), 3) a physical performance test (post-treatmentdata), 4) completion of the mood check list a secondtime (post-treatment, after-exercisedata), 5) an interview. The whole sessionwas again videotaped, and the mood of subjects subsequently evaluated by observers. RESULTS Effects on Self-Evaluated Mood The results were somewhat surprising: A significant placebo effect was found on four (one third) of the twelve items of the self-evaluatedmood check list, but no similar effect was obtained for the testosteronegroup! Subjectsbelonging to the placebo group experiencedthemselves as more angry [F(2,23): 6.01, p < .01], frustrated p < = 5.85, P .011, impulsive IF(2,23): [F(2,23) 4.30, < .02],andirritated[F(2,23) : 6.99, P < .011. Pre and post data of two of these items (angry and irritated) are presentedas examplesin Figures I and2. Effectson Observer-Eval uatedMood Observer-evaluations were consistent with the self-estimated data, thus supporting the validity of the findings. For example, observer-evaluatedfrustration revealed a sis- ANGRY 100 O = testosterone Q = ptacebo Q = control * =p-.O5 **=p<,O1 BEFORE BEFORE & AFTER TREATMENT PHYSICAL EXERCTSE A F T ER TREATMENT Fig. I . Self-evaluatedangerbeforeand after treatmentin the threeexperimentalgroups TestosteroneIntalcc 23 IRRITATED 100 O = testosterone Q = placebo O = control r =p<.O5 *r= p< .O1 BEFORE T R E A T ME N T BEFORE & AFTER PHYSICAL EXERCISE r*lIIfil"' Fig. 2. Self-evaluatedirritation before and after treatment in the three experimental groups. nificant placebo effectlF(2,23) : 7.05, P < .011. The remaining items also revealed group differences consistent with self-estimatedmood, but these were, however, not significant. When observer-evaluatedanger, irritation, and frustration were added together to create a summed variable (the internal consistencyof which was ct : .90), the summed variablerevealeda significant placebo effect[F(2,23) : 4.05, P < .05], too. Why were group differences based on observer-evaluationscores smaller than group differences basedon self-estimations?Subjectswere aware of the fact that they were being videotaped:they may have attemptedto hide their emotions from the camera. In other words, they may havebeen camera-shy. lnterviews Data obtained in the interviews revealedthe same trends. For instance,one individual belonging to the placebo group expressedhimself with the following typical words: "l have, during this week, felt touchy and irascible, I got irritated almost for no reason. I was very tired at the beginning of the week. I got mad at others, and it showed. I'm not usually like that. My physical training has been more successfulthan ever. I felt self-confidentin competition, which is unusual for me. ' ' 24 Bjdrkqvist et al. RIA Data level was found after I No significantbetweengroupsdifferencesin testosterone levels,but not more increased grouphad slightly week'streatment.The testosterone thanmightbe explainedby chancefluctuation. Physical Performance in physicalperformance. Therewereno betweengroupsdifferences DISCUSSION The resultsdemonstratea clear placebo effect: Subjects,although they denied this in the interview, obviously expectedto become more irritable, frustratedand angry. What is surprising and calls for an explanation, is the absenceof a placebo effect in the group receiving testosterone.This finding is so consistentthat it is difficult to conceive of it as a coincidence. Although the presentauthors do not claim to have an explanation for this finding, the following suggestionis offered: Contrary to expectation. testosterone levels did not differ significantly between the groups after I week's treatment. What may have happened is that the artificially induced testosteronesuppressedthe body's own production of the steroid: If the treatmenthad been carried out for a longer period, or larger doseshad been administered,differencesin testosteronewould probably have appeared.The suppressionof the body's own production may have had secondary psychological effects, depressing excitement and activation which, in turn, balancedout the activating placebo effect. It is worth noting that our resultsare consistentwith thoseof Ariel and Saville ll972l, who also found a significant placebo effect, but no effect of steroid intake. However, unlike the present study, they examined the effect of steroidsonly on physical performance. and not on mood. One has to remember that steroid dosage taken by athletes is considerably larger than that administeredin the presentexperiment, or that which could be prescribedfor therapeutic or experimental reasons.Athletes also continue steroid treatment for long periods and without medical supervision. The question whether steroid abuse causes uncontrollablemood changeand aggressionis still not settled:Hormonal variation may, or may not, be related to significant mood change. A parallel may be drawn to the debateabout the premenstrualsyndrome [Parlee, 1973], or mood changedue to steroid based contraceptives.It is possible that sensitivity to intake of artificial steroids leading to unpleasantmood changesis subject to individual variation. Two recent studies investigating the relationship between anabolic-androgenicsteroid use and mood change [Anderson et al., 1992; Bahrke et aI., 1992] yielded the in same result as the presentexperiment: Steroid intake did not increaseaggressiveness human males. A third double-blind study [Hannan et al., l99l] did find increased "resentment "hostility" and evenmore so in high-dosegroups,with the aggressiveness, and aggression" subscalesof the MMPI as dependentmeasures.Two field studies [Brower et al., l99l; Perry et al., 19901found that sportsmenabusing steroidsreported increasedaggressiveness.It should be borne in mind, however,that the last two studies were not double-blind experiments, and the reports may be explained as placebo effects. A review by Uzych ll992l does not exclude the possibility of increased aggressivenessafter steroid abuse, and another by Bahrke et al. [1990] suggeststhat Intakc Testosterone 25 psychological effects are variable, and related to type (17 alpha-alkalatedratherthan l7 beta-esterified), but not dose, of anabolic-androgenicsteroids administered. The resultsof the presentand other double-blind experimentssuggesthoweverthat much of the effect of steroid intake is really placebo. To claim that aggressionis causedby steroids, as in the news media, is misleading and dangerousfor severalreasons: l) There rs still no scientific evidencefor such a relationship. 2) Even if a correlation were found this would not prove a cause-effectrelationbetweensteroid abuseand aggressiveness, ship. Factors, such as unstablepersonality may be the source of willingness to abuse steroidsas well as aggressiveness.Steroid abuse may, for some, be a mediating factor enhancingaggressivetendenciesby producing statesof elated emotionality. A parallel may be drawn to the complexity of problems encounteredin establishinga causal link betweenalcohol intoxicationand aggression[Brain, 1986; Evans, 1986]. 3) Dissemiconnection may lead to anticipation (a nation of the myth of the steroid-aggressiveness placebo effect) of aggressivenessamong steroid abusersand, in turn, to actual acts of violence. [t may, in fact, work as an excusefor aggression. 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