Anabolic Steroids and Aggression

The following is a brief synopsis of a talk given at the 115th Annual Convention of the American Psychological Association (APA) in San Francisco, CA on August 19, 2007.

Existing research on substance use has had little impact on the public or researchers’ view of anabolic/androgenic steroids (AAS) and their effects. One reason is morality: It is obvious that, standing in San Francisco, AAS are synonymous with “cheating” in the public eye – I will not discuss this today. The other seemingly reflects an assumption; AAS are endogenous testosterone’s bigger twins and if endogenous testosterone (T) causes physical aggression then AAS surely must. This notion was expressed by a “clinical psychologist and media personality” who was asked if AAS caused Chris Benoit’s actions; she noted: “Testosterone is linked to aggression. We know that murderers, we measure their levels of testosterone. They have higher levels (Macari, 2007).”

Actually, human T is linked to dominance and social status (Booth et al., 2006) and challenge (Archer, 2006); aggression is but one strategy employed in those pursuits. Murderers have high T levels; so do trial lawyers and soldiers. All seek dominant status in “competitive” environments in different and more or less socially acceptable ways. Ultimately, “…many investigators…assume that testosterone level is a trait that explains differences between individuals with respect to aggression and violence. However, there is little empirical support for this position (Booth et al., 2006; p. 169)”.

Animal research is oft cited as support for a direct and exclusive physiological link between AAS and aggression. However, indiscriminate aggression is not universally observed in AAS-treated animals (McGinnis, 2004). AAS effects on non-human aggression vary by context (in rodentia; Breuer, McGinnis, Lumia, & Possidente, 2004) and status (in non-human primates; Dixson, 1980; Rejeski, Brubaker, Herb, Kaplan, & Koritnik, 1988). Additionally, animal studies often use adolescent animals and dosing regimens irrelevant to adult human AAS use; for instance, AAS roughly equal to 3 grams/week in a 90 kg human administered to adolescent animals throughout puberty resulted in longer-term aggression (Fischer, Ricci, & Melloni, 2007). Although these findings were highlighted in several APA publications (e.g., http://www.apa.org/releases/steroids0226.html), total weekly doses of over 2 g per week are rarely reported by AAS users (e.g., Cohen, Collins, Darkes, & Gwartney, In Press) and, given T’s role in adolescent brain development and the establishment of social behavior (Sisk, Schulz, & Zehr, 2003), such results are both unsurprising and uninformative regarding AAS effects in human adult non-medical use.

Research on aggression in adult human AAS users has largely relied on case studies and surveys. Although case studies (e.g., Pope & Katz, 1990; Thiblin, Lindquist, & Rajs, 2000), surveys (e.g., Galligani, Renck, & Hansen, 1996; Lefavi, Reeve, & Newland, 1990) and prospective surveys that follow self-selected users (e.g., Fudala, Weinrieb, Calarco, Kampman, & Boardman, 2003; Yates, Perry, & Murray, 1992) may suggest an AAS use/aggression association, results are both inconsistent and unable to determine cause and effect. Additionally, aggression measures do not reliably relate to AAS use periods (e.g., Fudala et al., 2003) or dose (e.g., Lefavi et al, 1990; Yates et al., 1992).

Within-subject experiments that administer AAS and placebos (e.g., Pope, Kouri, & Hudson, 2000, Su et al., 1993) may show subtle effects, but find no relationship between blood steroid levels and symptoms (e.g., Su et al., 1993).  Between-subject experiments that evaluate causation by controlling for individual differences via rigorous inclusion criteria, random assignment and blinding to drug conditions offer little evidence of an AAS/aggression link (e.g., O’Connor et al., 2002; Tricker et al., 1996).

Experimental findings vary depending on the measure of aggression. Validated self-report measures typically do not show meaningful increases (e.g., Tricker et al., 1996). Self and observer ratings rarely reflect increased aggression (e.g., Pope et al., 2000; Tricker et al., 1996). The Point Subtraction Aggression Paradigm (PSAP), a laboratory task which scores punitive responses to a fictitious opponent as aggression, increased slightly within participants given AAS, although “…most participants showed little change and a few showed marked changes (p. 135; Pope et al., 2000)”. Additionally, the PSAP may assess aggression as a competitive strategy (Archer, 2006) which may not reflect the aggressive behavior of interest. In addition, the PSAP levels during AAS administration resembled those of marijuana users during withdrawal (Kouri, Pope, & Lukas, 1999).

Aggression in AAS users is rare and there is no consistent evidence that it is a direct effect of AAS. The designs used offer discrepant pictures. Case studies exaggerate problems (Hartgens & Kuipers, 2004) by highlighting illustrative “failures” and ignoring “non-problem” cases, which could provide useful information (“Who does not become aggressive and why?”). Surveys of AAS-users and non-users are descriptive but confound correlates, consequences, or antecedents. Experiments administer supraphysiological doses, raising testosterone levels 300%, but cannot mimic real-world doses and polypharmacy. [Still, if the initial T/aggression hypothesis were correct and physiological T variations predicted aggression, then levels three times normal should also do so, if increased T levels were the sole cause.] Lastly, while still blinded, participants could retrospectively distinguish AAS from placebo (Su et al., 1993) in within-subject experiments, suggesting that inert placebo comparison treatments are insufficient (see Riem & Hersey, 1995).

The role of individual differences, learning and context in drug use and drug-related behaviors has long been explored in substance use research. Antecedent factors, context and anticipation influence alcohol use and post-consumption behaviors (see Goldman, Darkes, & Del Boca, 1999).  Expectations for alcohol mediate (transmit) the influence of antecedents (e.g., sensation seeking, aggression) on drinking (Darkes, Greenbaum, & Goldman, 2004; Derman & George, 1989) and predict non-consumptive (outcome) behavior after exposure to drug-relevant cues (Bartholow & Heinz, 2006; Friedman, McCarthy, Bartholow, & Hicks, 2007).  Procedures that modify expectancies affect consumption (Darkes & Goldman, 1993; Stein, Goldman, & Del Boca, 2000). Expectancies predict patterns of cocaine use and subjective response (e.g., Lundahl & Lukas, 2007; Schafer & Brown, 1991). Seventy-five percent of the effects of anti-depressant drugs can be attributed to expectancies (a placebo effect; Kirsch & Saperstein, 1998). AAS researchers have largely failed to avail themselves of this literature.

AAS’ effects on strength and muscle mass gain were once considered placebo-mediated, but are now largely unquestioned (e.g., Bhasin et al., 1996). Still, building on work by Ariel and Saville (1972), recent studies found changes in strength among college students (e.g., Kalasountas, Reed, & Fitzpatrick, 2007) and national level power lifters (Maganaris, Sharp, & Collins, 2000) in those expecting to consume AAS. A similar, but un-replicated expectancy effect for aggression was seen in placebo-treated participants in an AAS study (Björkqvist, Nygren, Björklund, & Björkvist, 1994). Higher levels of trait impulsivity were associated with increased aggression levels above and beyond any effect of experimentally-administered AAS (O’Connor, Archer, Hair, & Wu, 2002).

Numerous researchers (Brower et al., 1994; Grogan, Shepherd, Evans, Wright, & Hunter, 2006; Hildebrandt et al., 2006; Olrich & Vasallo, 2006) have highlighted expectations that could motivate AAS use and predict use-related outcomes. Users and non-users expect AAS may lead to aggression (e.g., Schwerin & Corcoran, 1996). These expectations may be valued differently; some users may value aggression and both use AAS as a result of, and subsequently behave in accordance with, that expectation, as has been demonstrated for alcohol (Friedman et al., 2007). Although a role for psychosocial factors in AAS-related aggression was suggested years ago (Riem & Hersey, 1995; Sharp & Collins, 1998), these factors remain largely unexplored in AAS use and its psychological effects, perhaps reflecting a bias toward physiological explanations.

Discussing Benoit, Nancy Grace lamented: “…it would ease my heart to know maybe he was on steroids…I’d rather think that than think that he could do that (Grace, 2007)”. Her sentiments imply that “true” inevitable causes are physiological; otherwise the act is less “real” or more deliberate. That notion is inconsistent with what we know about human behavior, substance use and its behavioral effects. A role for psychosocial processes does not mean a behavior any less real or more volitional. Aggression is rare but real, no matter the cause. None of these processes requires contemplation. However common the desire may be, it is a disservice to seek comforting answers instead of accurate ones.

The good news is that aggression is rare among anabolic-androgenic steroid users and does not appear to be caused by AAS. The discrepant findings in the literature suggest a complex causal picture, including antecedent, cognitive, and contextual factors. Users view the AAS experience positively (e.g., Olrich & Ewing, 1999; Olrich & Vasallo, 2006) and minimize negative side-effects (e.g., Grogan et al., 2006). They consider medical authorities uninformed (e.g., Cohen et al., in press; Pope, Kanayama, Ionescu-Pioggia, & Hudson, 2004) likely because AAS research seems narrowly focused on effects that most users do not experience. This distrust is likely to perpetuate because most prospective users learn from current users within the subculture, often via the internet (Cohen at al., in press). Still, many AAS researchers seem determined to run the same studies using different measures until they find the results they are sure are there rather than learning from obtained results and moving forward with new study designs that might explain the phenomenon; an approach that reinforces users’ mistrust. Science would progress by forgoing sweeping generalizations and dire predictions of rare outcomes and moving toward identifying the factors that put a small minority at risk for AAS-related aggression, as well as those that may protect the vast majority. It should broaden its scope to include both biological and psychosocial processes that might convey that risk and, in so doing, explore approaches that might be used to reduce risk for negative outcomes.

References

• Archer, J. (2006). Testosterone and human aggression: An evaluation of the challenge hypothesis. Neuroscience and Biobehavioral Reviews, 30, 319-345.
• Ariel, G.B., & Saville, W. (1972). Anabolic steroids; The physiological effects of placebos. Medicine and Science in Sports, 4, 124-126.
• Bhasin, S., Storer, T.W., Berman, N., Callegari, C., Clevenger, B., Phillips, J., Bunnell, T., Tricker, R., Shirazi, A., & Casaburi, R. (1996). The effects of supraphysiological doses of testosterone on muscle size and strength in normal men. The New England Journal of Medicine, 335, 1-7.
• Björkqvist, K., Nygren, T., Björklund, A-C., & Björkvist, S-E. (1994). Testosterone intake and aggressiveness: Real effect or anticipation? Aggressive Behavior, 20, 17-26.
• Booth, A., Granger, D.A., Mazur, A., Kivlighan, K.T. (2006). Testosterone and social behavior. Social Forces, 85, 167-191.
• Breuer, M.E., McGinnis, M.Y., Lumia, A.R., & Possidente, B.P. (2004). Aggression in male rats receiving anabolic androgenic steroids: Effects of social and environmental provocation. Hormones and Behavior, 40, 409-418.
• Cohen, J., Collins, R., Darkes, J., & Gwartney, D. (In Press). A League of Their Own: Demographics, Motivations and Patterns of Use of 1,955 Male Adult Non-Medical Anabolic Steroid Users in the United States. Journal of the International Society of Sports Nutrition.
• Darkes, J., & Goldman, M.S. (1993). Expectancy challenge and drinking reduction: Experimental evidence for a mediational process.  Journal of Consulting and Clinical Psychology, 61, 344-353.
• Darkes, J., Greenbaum, P.E., & Goldman, M.S. (2004). Alcohol expectancy mediation of biopsychosocal risk: Complex patterns of mediation. Experimental and Clinical Psychopharmacology, 12, 27-38.
• Dixson, A.F. (1980).  Androgens and aggressive behavior in primates: A review. Aggressive Behavior, 6, 37-67.
• Fischer, S.G., Ricci, L.A., & Melloni, R.H. (2007). Repeated anabolic-androgenic steroid exposure during adolescence alters phosphate-activated glutamase and glutamate receptor 1 (GluR1) subunit immunoreactivity in hamster brain: Correlation with offensive aggression. Behavioral Brain Research, 180, 77-85.
• Friedman, R.S., McCarthy, D.M., Bartholow, B.D., & Hicks, J.A. (2007). Interactive effects of alcohol outcome expectancies and alcohol cues on nonconsumptive behavior. Experimental and Clinical Psychopharmacology, 15, 102-114.
• Fudala, P.J., Weinrieb, R.M., Calarco, J.S., Kampman, K.M., & Boardman, C. (2003). An evaluation of anabolic-androgenic steroid abusers over a period of 1 year: Seven case studies. Annals of Clinical; Psychiatry, 15, 1573-3238. Galligani, N., Renck, A., & Hansen, S. (1996). Personality profile of men using anabolic androgenic steroids. Hormones and Behavior, 30, 170-175.
• Goldman, M.S., Darkes, J., & Del Boca, F.K. (1999). Expectancy mediation of bioposychosocial risk for alcohol use and alcoholism. In I. Kirsch (Ed.), How expectancies shape experience (pp. 233-262). American Psychological Association; Washington, D.C.
• Grace, N. (2007). http://transcripts.cnn.com/TRANSCRIPTS/0706/28/ng.01.html.
• Grogan, S., Shepherd, S., Evans, R., Wright, S., & Hunter, G. (2006). Experiences of anabolic steroid use: In-depth interviews with men and women body builders. Journal of Health Psychology, 11, 845-856.
• Hartgens, F., & Kuipers, H. (2004). Effects of androgenic-anabolic steroids in athletes. Sports Medicine, 34(8), 513-554.
• Kalasountas, V., Reed, J., & Fitzpatrick, J. (2007). The effect of placebo-induced changes in expectancies on maximal force production in college students. Journal of Applied Sport Psychology, 19, 116-124.
• Kirsch, I., & Saperstein, G. (1998). Listening to prozac but hearing placebo: A meta-analysis of antidepressant medication. Prevention & Treatment, Volume 1, Article 0002a, posted June 26, 1998; accessed August 5, 2007.
• Kouri, E.M., Pope, H.G., & Lukas, S.E. (1999). Changes in aggressive behavior during withdrawal from long-term marijuana use. Psychopharmacology, 143, 302-308.
• Lefavi, R.G., Reeve, T.G., & Newland, M.C. (1990). Relationship between anabolic steroid use and selected psychological parameters in male bodybuilders. Journal of Sport Behavior, 13, 157-166.
• Lundahl, L.H., & Lukas, S.E.  (2007). Negative cocaine effect expectancies are associated with subjective response to cocaine challenge in recreational cocaine users. Addictive Behaviors, 32, 1262-71
• Macari, A. (2007). http://transcripts.cnn.com/TRANSCRIPTS/0707/17/ng.01.html.
• Maganaris, C., Collins, D., & Sharp, M. (2000). Expectancy effects and strength training: Do steroids make a difference? The Sport Psychologist, 14, 272-278.
• McGinnis, M.Y. (2004). Anabolic androgenic steroids and aggression: Studies using animal models. Annals of the New York Academy of Sciences, 1036, 399-415.
• O’Connor, D.B., Archer, J., Hair, W.M., & Wu, F.C.W. (2002). Exogenous testosterone, aggression, and mood in eugonadal and hypogonadal men. Physiology & Behavior, 75, 557-566.
• Olrich, T.W., & Ewing, M.E. (1999). Life on steroids: Bodybuilders describe their perceptions of the anabolic-androgenic steroid use period. The Sport Psychologist, 13, 299-312.
• Olrich, T.W., & Vasallo, M.J. (2006). Psychological dependency to anabolic-androgenic steroids: Exploring the role of social mediation. New England Law Review, 40, 735-746.
• Pope, H.G., Kanayama, G., Ionescu-Pioggia, M., & Hudson, J. (2004). Anabolic steroid user’s attitudes towards physicians. Addiction, 99, 1189-94.
• Pope, H.G., & Katz, D. (1990). Homicide and near homicide by anabolic steroid users.  Journal of Clinical Psychiatry, 51, 28-31.
• Pope, H.G., Kouri, E.M., & Hudson, J.I. (2000). Effects of supraphysiological doses of testosterone on mood and aggression in normal men. Archives Of General Psychiatry, 57, 133-140.
• Rejeski, W.J., Brubaker, P.H., Herb, R.A., Kaplan, J.R., & Koritnik, D.  (1988). Anabolic steroids and aggressive behavior in cynomolgus monkeys. Journal of Behavioral Medicine, 11, 95-105.
• Riem K.E., & Hersey, K.G. (1995). Using anabolic-androgenic steroids to enhance physique and performance: Effects on mood and behavior. Clinical Psychology Review, 15, 235-256.
• Schafer, J., & Brown, S.A.  (1991). Marijuana and cocaine expectancies and drug use patterns. Journal of Consulting and Clinical Psychology, 59, 558-565.
• Sharp, M., & Collins, D.  (1998). Exploring the “inevitability” of the relationship between anabolic-androgenic steroid use and aggression in human males. Journal of Sport and Exercise Psychology, 20, 379-394.
• Sisk, C.L., Schulz, K.M., & Zehr, J.L. (2003). Puberty: A finishing  school for male social behavior. Annals of the New York Academy of Science, 1007, 189–198.
• Su, T-P., Pagliaro, M., Schmidt, P.J., Pickar, D., Wolkowitz, O., & Rubinow, D.R. (1993). Neuropsychiatric effects of anabolic steroids in male normal volunteers. JAMA, 269, 2760-64.
• Thiblin, I., Lindquist, O., & Rajs, J. (2000). Cause and manner of death among users of anabolic androgenic steroids. Journal of Forensic Science, 45, 16-23.
• Tricker, R., Casaburi, R. Storer, T.W., Clevenger, B., Berman, N., Shirazi, A., & Bhasin, S. (1996). The effects of supraphysiological doses of testosterone on angry behavior in healthy eugonadal males—a clinical research center study. Journal of Clinical Endocrinology & Metabolism, 81, 3754-58.
• Yates, W.R., Perry, P., & Murray, S. (1992). Aggression and hostility in anabolic steroid users. Biological Psychiatry, 31, 1232-34.