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Review Articles Psychiatric Complications of Anabolic Steroid Abuse RYAN C.W. HALL, M.D. RICHARD C.W. HALL, M.D. MARCIA J. CHAPMAN The authors review the literature from human and animal studies on the neurochemical and pathological psychiatric effects of supraphysiological doses of anabolic-androgenic steroids (AAS) and discuss the AAS use and abuse patterns, additional drug use patterns, and personality and behavioral characteristics of AAS abusers. (Psychosomatics 2005; 46:285–290) I n 1889, physiologist Charles E. Brown-Sequard made the first public claims about the effects of anabolic-androgenic steroids (AAS). He announced that he had extracted a substance from dog and guinea pig testicles, which, when injected, had increased his strength, improved his intellect, provided relief from constipation, and increased the arc of his urine.1 Since then, an underground population of athletes, coaches, and recreational users has developed complicated AAS regimens to enhance their athletic performance and, in so doing, have unleashed a myriad of psychiatric complications such as addiction, depression, rage, and psychosis on themselves and the public at large. Psychiatric Syndromes and the Issue of Violence Historically, low doses of AAS have been used to treat depression and melancholia, either as primary agents or as adjuncts to standard treatment.1 Misuse of these agents has added a new term to the drug lexicon, “roids rage.”2 Studies comparing steroid abusers with non-steroid-using athletes have shown steroid abusers to have a higher incidence and prevalence of psychiatric symptoms.3–5 The most prominent psychiatric features associated with AAS abuse are manic-like presentations defined by irritability, aggressiveness, euphoria, grandiose beliefs, hyperactivity, and reckless or dangerous behavior. Other psychiatric presentations include the development of acute psychoses, exacerbation of tics and depression, and the development of Psychosomatics 46:4, July-August 2005 acute confusional/delirious states.2,6–8 Extreme variability of symptom presentation exists because of differences in the dose consumed, agent used, duration of use, personality type of the abuser, and current or previous use of other recreational drugs.2,9–11 Studies in which steroid abusers have been used as their own comparison subjects, in the attempt to eliminate the variable of personality disorder, have shown differences in the degree of hostility, aggression, and severity of manic-like symptoms during periods of use and nonuse.4–8 Pope and Katz,6,12 in their reviews of the literature, reported that studies in which steroid use is quantified and categorized on the basis of total weekly dosing have found that psychiatric symptoms become more common and severe as the dose increases. Studies that have used Pope and Katz’s categories of medium steroid use (between 300 and 1000 mg/week of any AAS) and high use (more than 1000 mg/week of any AAS)6 have demonstrated that 23% of subjects using these doses of steroids met the DSM-III-R criteria for a major mood syndrome (mania, hypomania, and major depression) and that 3.4%–12% developed psychotic symptoms.6,8 It is hard to determine whether the unexplained violent Received March 9, 2004; revisions received June 29 and Aug. 19, 2004; accepted Sept. 27, 2004. From the Department of Psychiatry and Behavioral Sciences, Johns Hopkins Hospital, Baltimore; and the Department of Psychiatry, University of Florida, Gainesville. Address correspondence and reprint requests to Richard C.W. Hall, M.D., 100 East Sybelia Ave., Suite 210, Maitland, FL 32751. Copyright 䉷 2005 The Academy of Psychosomatic Medicine. http://psy.psychiatryonline.org 285 Anabolic Steroid Abuse rages that occur with AAS abuse might be better understood as part of a paranoid psychotic state or as instances of unprovoked rage unassociated with other psychiatric findings (i.e., as a psychiatric or cognitive disorder or as an impulse control problem). Psychotic symptoms associated with the use of anabolic steroids generally occur among individuals consuming more than 1,000 mg of testosterone weekly.6 Classic presentations include grandiose and paranoid delusional states that often occur in the context of a frank psychotic or manic episode. The symptoms usually resolve within a few weeks after the individual has discontinued steroid use, although they may persist for as long as 1 month, even if adequately treated with antipsychotic medication. Reactions tend to be more agitated, violent, and coordinated than the agitation that occurs as an adverse reaction to corticosteroids, which can also produce idiosyncratic manic and psychotic symptoms.9,10 Psychiatric Pathology of AAS Abuse Pope and Katz13 interviewed 41 bodybuilders and football players who had used AAS. Applying DSM-III-R criteria, they found that 22% displayed a full affective syndrome and 12% developed psychotic symptoms in association with their steroid use, suggesting that major psychiatric symptoms are an adverse effect of the misuse of these drugs. In a subsequent study, Pope and Katz6 used the Structured Clinical Interview for DSM-III-R to compare 88 athletes who used steroids with 68 nonusers. They found that 23% of the AAS users reported major mood syndromes, including mania, hypomania, and major depression, in association with their steroid use. The steroid abusers experienced mood disorders significantly more frequently when using AAS than when they were steroid free. Su et al.14 administered 40 mg/day and 240 mg/day of methyltestosterone in a 2-week, double-blind, fixed-order, placebo-controlled, crossover inpatient study of healthy male volunteers. The 20 men in the study were otherwise medication free and were free of any medical or psychiatric illness. The researchers noted higher symptom scores during high-dose methyltestosterone administration, compared with baseline. The changes were either moodelevating effects, such as euphoria (“steroid rush”), increased energy, and increased sexual arousal and drive, or mood-dysphoric effects, such as irritability, mood swings, increasingly violent feelings, and increased hostility. The researchers also noted cognitive impairment, including distractibility, forgetfulness, and confusion, in subjects taking the higher dose of steroids. Baseline characteristics, 286 http://psy.psychiatryonline.org including family history and history of previous drug abuse, did not predict the development or the nature of psychiatric symptoms. In a randomized, placebo-controlled crossover trial, Pope et al.15 administered testosterone cypionate for 6 weeks in doses ranging to 600 mg/week, followed by 6 weeks of no treatment and then placebo for 6 weeks to 56 men ages 20–50 years. A variety of outcome measures were used to assess mania, aggression, and depression. The results showed that testosterone significantly increased mania, elevating scores on multiple instruments; that the drug was liked and sought after; and that aggression increased. The investigators noted that the response to the drug, however, was highly variable. Eighty-four percent of the subjects exhibited minimal to no psychiatric effects, 12% became mildly hypomanic, and 4% became markedly hypomanic. The investigators were not able to differentiate the manic responders from the nonresponders on the basis of demographic characteristics or baseline psychological, laboratory, or physiological measures. Yates et al.16 examined the psychosocial effects of low-dose steroids in men as a possible form of birth control and found minimal risk of adverse psychosexual effects in the majority of men receiving less than 500 mg/week of testosterone cypionate. At a dose of 500 mg/week, however, a minority of subjects began to experience significant adverse psychological effects, such as dysphoria, irritability, and hypomania. Hall et al.9–11 and Wyszynski and Wyszynski17 suggested that the adverse effects of testosterone may be similar to those of prednisone and other corticosteroids. Studies by Hall et al.9–11 and the Boston Collaborative Program18 have shown that adverse psychiatric effects increase with increasing dosages of corticosteroids, a finding similar to that of Pope et al.15 for AAS. Investigative Findings and Anecdotal Reports on Aggression Choi and Pope19 noted that increased aggression was associated with the illicit use of AAS by athletes and that the wives and girlfriends of these athletes often become the victims of physical abuse. In a controlled study, they interviewed 23 AAS-using strength athletes and 14 non-AAS using athletes. The AAS users reported significantly more fights, verbal aggression, and violence toward their significant other and had significantly higher scores on two of three indicators of violence during periods when they were taking AAS, compared to periods when they were not takPsychosomatics 46:4, July-August 2005 Hall et al. ing AAS. When they were not taking AAS, the AAS users were not distinguishable from nonusers on the aggression scales. Bond et al.20 investigated the effects of AAS on attentional bias to aggressive cues in 46 male strength athletes. The researchers found no difference in attentional bias between AAS users and nonusers but noted that AAS users who were currently taking AAS had subtle mood changes and slowed cognitive performance, compared to users who were not actively taking AAS. Anecdotal case reports published by Pope and Katz21 highlighted both the psychological and physical dangers of abusing AAS. They described three men with benign premorbid psychiatric histories and no evidence of antisocial personality disorder or violence who impulsively committed violent crimes, including murder, while taking AAS. Pope and Katz suggested that the steroids played a necessary, if not primary, role in the etiology of these violent behaviors. They concluded that steroid-induced violence poses a little-recognized public health threat. We have seen six cases of AAS-induced criminal behavior—three homicides and three violent assaults. Two of the three lethal assaults were senseless, nonpremeditated, and occurred during a psychotic episode. In three of the six cases, there was evidence of significant antisocial behavior, violence, or criminal behavior before the steroidrelated episode. The AAS psychosis in each case was remarkably similar to that in the others, as well as to AAS psychoses described in the literature, and included stereotypic qualities of irritability, aggressiveness, and grandiosity. In each case, an irrational thought of the patient or a minor deed of an unknown individual prompted a violent attack. The mental status of all six perpetrators cleared within weeks to 2 months, and they had specific memory of the act and of their delusional thinking at the time the act was committed. Other studies have tried to measure aggression and psychiatric disturbances in AAS abusers by looking at how they died. An investigational study of 34 deceased male AAS abusers found that nine were the victims of homicide, 11 had committed suicide, and 12 died of accidental causes.22 The authors concluded that AAS abusers are at a higher risk of dying violently because of impulsive/ aggressive behavior and/or depression. Animal Studies of Neurochemical Changes Studies examining neurochemical changes in sexually maturing/adolescent animal brains exposed to supraphysioPsychosomatics 46:4, July-August 2005 logical doses of AAS have found complex changes in multiple neurochemical communication pathways long associated with depression, anger, and sexual behavior in humans. Studies of neurohormonal receptors in adolescent rodent brains found that AAS exposure was associated with a decrease in the inhibitory receptors for c-aminobutyric acid in the medial amygdala, medial preoptic area, and ventromedial nucleus of the hypothalamus.23,24 Studies in nandrolone-treated guinea pigs showed a significantly greater density of c-Fos and Fos-related antigen-positive neurons in the central nucleus of the amygdala and of Fos-related antigen-positive neurons in the frontal cortex, the shell of the nucleus accumbens, and the supraoptic nucleus.25 These areas have been shown to correlate with human brain areas that are involved in stress, behavioral, and reward responses. Animal studies have also shown that AAS have effects on serotonin receptors, specifically a significant down-regulation of 5-HT1B receptor density in the hippocampus CA1 region and the medial globus pallidus and a significant up-regulation of 5-HT2 receptor density in the nucleus accumbens shell.26 Alterations in receptor density were also observed in the lateral globus pallidus, ventromedial hypothalamus, amygdala, and intermediate layers of various cortical regions. In studies of the anterior hypothalamic-arginine vasopressin (AH-AVP) neural system in animals treated with anabolic steroids, the treated animals had biting tendencies and less time to provocation to bite, compared with control animals; these effects could be reduced or reversed by using AH-AVP antagonists.27 Characteristics of AAS Abusers The typical AAS abuser is a male polysubstance abuser who has poor self-esteem, poor school performance, and a cluster B personality disorder or traits and who may or may not participate in an organized sport.28–32 Males are two to three times more likely to abuse AAS, compared with females.29,30 Sixty to 70% of AAS abusers actively participate in organized sports.29 Other factors that correlate with AAS abuse include higher socioeconomic status, a family history of drug abuse, higher rates of self-reported violence and aggression, lower self-esteem, and poor body image before AAS use.29,32,33 In a study by Kindlundh33 in Sweden, being an immigrant was also found to correlate with AAS use. There have been some interesting studies concerning the relationship of personality disorder to AAS abuse. Yates et al.34 found a higher prevalence of cluster B personality disorders of the histrionic and antisocial type in http://psy.psychiatryonline.org 287 Anabolic Steroid Abuse weightlifters who abused AAS, compared to weightlifters who did not use AAS.34 Porcerelli and Sandler35 found that steroid users evidenced higher scores on measures of pathological narcissistic traits (exhibitionism, entitlement, and exploitativeness) and lower ratings for empathy, relative to non-AAS-using weightlifting comparison subjects. Another interesting finding of Porcerelli and Sandler was that 25% of the AAS abusers in their study, but none of the nonabusing comparison subjects, had memories of childhood sexual or physical abuse. In a case control study, Kanayama et al.32 found that AAS abusing weightlifters reported poorer relationships with their fathers and a greater incidence of childhood conduct disorder, relative to non-AAS-using comparison subjects. mon for users to take multiple forms of AAS (five different drugs on average) from multiple classes of steroids to take advantage of the different pharmacokinetic properties of these drugs.6,40,42 Stackers generally take supraphysiological doses of anabolic steroids for 4–18 weeks, followed by a drug-free period of 1–12 months.41 The purpose of the drug-free period is to minimize side effects, promote recuperation of various hormonal systems, and avoid detection of AAS use during athletic competition.2 Some abusers will try to taper off AAS at the end of a stacking cycle to reduce side effects and withdrawal, a practice called “pyramiding.”41 Because of the intricate nature of these stacking regimens, many users have a “coach” who helps coordinate the schedule and drugs given.42 AAS Dependence Polysubstance Abuse and AAS No evidence is reported in the reviewed literature that AAS abuse or dependence develops from the therapeutic use of AAS.36 Conversely, 165 instances of AAS dependence have been reported among weightlifters and bodybuilders who chronically administered supraphysiological doses of anabolic steroids as part of their weight training regimen.36,37 Individuals who use high doses of AAS over prolonged periods may develop depressive symptoms, anhedonia, fatigue, impaired concentration, and even suicidal thoughts when they stop taking AAS, and these withdrawal effects may contribute to a syndrome of dependence. Brower et al.5,38,39 conducted several studies examining the issue of AAS dependence. In their initial studies, 75% of the steroid abusers met the DSM-III-R criteria for psychoactive substance dependence and all steroid-abusing subjects met the criteria for psychoactive substance abuse.38 In subsequent larger studies, Brower et al.38 found a 60% rate of psychoactive substance dependence in anabolic steroid abusers. In general, they found that steroid withdrawal usually presented with depression, especially in cases of intense AAS abuse.5 Steroid discontinuation effects were variable and transient and appeared to be more common when 17-alpha-alkalated formulations of AAS were discontinued.37 Usage Patterns, Including Stacking and Pyramiding Recreational AAS users generally develop complicated multidrug regimens using oral and intramuscular preparations (see Table 1) at progressively higher doses until 40– 100 times the usual physiological levels are reached.28,40,41 This practice is referred to as “stacking.” It is not uncom288 http://psy.psychiatryonline.org AAS users are often polysubstance abusers, and their polysubstance abuse may include use of traditional recreational drugs and misuse of prescription drugs. Even those who avoid traditional recreational drugs are still enveloped in the drug culture to obtain steroids (e.g., from suppliers or pushers), to find ways to administer them (e.g., finding large-gauge needles), and to develop means to continue using steroids (e.g., hiding use and paying for AAS).5,42–44 Studies examining AAS use as a gateway to other drugs of abuse found that 29% of people who abused both steroids and opioids started with steroids and were later introduced to opioids by the person who supplied them with the AAS.36,44 DuRant et al.44 found that 25% of the AAS abusers in their study shared needles to inject drugs and that a positive correlation existed between AAS abuse and the use and abuse of cocaine, injectable drugs, and marijuana. Many dual-substance abusers have reported starting to take opioids to counteract the side effects of AAS, such as insomnia, irritability, jitteriness, and the depression associated with withdrawal from AAS.43 For those who use steroids to enhance “bodily health,” the use of additional drugs to further enhance the effects of AAS or to decrease AAS side effects is common. Other drugs that are frequently abused as adjuncts include human growth hormone, which acts synergistically with AAS; human chorionic gonadotropin to reduce the testicular side effects of the anabolic steroids; diuretics to prevent water retention and improve visual muscle appearance (rippled effect); and antiestrogens such as tamoxifen to block gynecomastia.44,45 To help hide the fact that steroids are being used, some AAS abusers will take antibiotics and antiacne Psychosomatics 46:4, July-August 2005 Hall et al. medications to prevent testosterone-induced acne, which often involves the face, neck, and torso. of certain cancers (hepatocellular carcinoma), and sudden death.2,5,6 Summary Complications and Side Effects of Supraphysiological Doses of Androgens Data defining the cumulative effects of stacking remain speculative and are mostly derived from case reports.41 Reported side effects can be as benign as acne and fluid retention or extend to more distressing effects such as gynecomastia, lower levels of high-density lipoprotein (HDL cholesterol), and sleep apnea. Extreme side effects can lead to lethal complications such as hepatic failure, myocardial infraction, tendon rupture, arrhythmias, the development TABLE 1. Current data suggest that AAS abuse can increase aggression and cause rage, delirium, depression, mania, psychosis, and withdrawal symptoms. Psychiatric symptoms are seen at greater frequency with increasing doses of AAS. After discontinuation of AAS use, most psychiatric sequelae resolve within 8 weeks. Animal data suggest that taking anabolic steroids alters multiple neurochemical pathways. Use of AAS can lead to criminal behavior, such as drug abuse, as well as to assault and homicide that can be random and senseless. Commonly Used Androgenic-Anabolic Steroidsa Oral Agents Fluoxymesterone (Halotestin, AndroidF, Ultandren) Mesterolone (Mestoranum, Proviron) Methandienone, methandrostenolone (Dianabol) Methyltestosterone (Android, Testred, Virilon) Mibolerone (Cheque Dropsb) Oxandrolone (Anavar, Oxandrin) Oxymetholone (Anadrol-50, Hemogenin) Stanozolol (Winstrol) Striant (buccal delivery of testosterone) Intramuscular Agents Transdermal Agents Boldenone undecylenate (Equipoiseb) Testosterone (Androderm, AndroGel, Testim, Testoderm, Testoderm TTS) Methenolone enanthate (Primobolan depot) Nandrolone decanoate (Deca-Durabolin) Nandrolone phenpropionate (Durabolin) Nandrolone undecanoate (Dynabolan) Stanozolol (Winstrol-Vb) Testosterone cypionate (Depo-Testosterone, Virilon IM) Testosterone enanthate (Delatestryl) Testosterone esters blends (Sustanon, Sten) Testosterone propionate (Testoviron, Androlan) Testosterone undecanoate (Andriol, Restandol) Trenbolone acetate (Finajet, Finaplixb) Trenbolone hexahydrobencylcarbonate (Parabolan) a International brand names are included for agents with widespread illicit use in the United States. Veterinary compound. b References 1. Basaria S, Wahlstrom JT, Dobs AS: Anabolic-androgenic steroid therapy in the treatment of chronic diseases. J Clin Endocrinol Metab 2001; 86:5108–5117 2. Porcerelli JH, Sandler BA: Anabolic-androgenic steroid abuse and psychopathology. Psychiatr Clin North Am 1998; 21:829–833 3. Choi P, Parrott A, Cowan D: High-dose anabolic steroids in strength athletes: effects upon hostility and aggression. Hum Psychopharmacol 1990; 5:349–356 Psychosomatics 46:4, July-August 2005 4. Lefavi R, Reeve T, Newland MC: Relationship between anabolic steroid use and selected psychological parameters in male bodybuilders. J Sport Behav 1990; 13:157–166 5. Brower K: Anabolic steroids: addictive, psychiatric and medical consequences. Am J Addic 1992; 1:100–114 6. Pope HG Jr, Katz DL: Psychiatric and medical effects of anabolicandrogenic steroid use: a controlled study of 160 athletes. 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