Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-23T00:22:49.604Z Has data issue: false hasContentIssue false

Associations of anabolic-androgenic steroid use with other behavioral disorders: an analysis using directed acyclic graphs

Published online by Cambridge University Press:  01 March 2018

Gen Kanayama
Affiliation:
From the Biological Psychiatry Laboratory, McLean Hospital/Harvard Medical School, 115 Mill St, Belmont, Massachusetts 02478, USA
Harrison G. Pope Jr*
Affiliation:
From the Biological Psychiatry Laboratory, McLean Hospital/Harvard Medical School, 115 Mill St, Belmont, Massachusetts 02478, USA
James I. Hudson
Affiliation:
From the Biological Psychiatry Laboratory, McLean Hospital/Harvard Medical School, 115 Mill St, Belmont, Massachusetts 02478, USA
*
Author for correspondence: Harrison G. Pope, E-mail: [email protected]

Abstract

Background

Anabolic-androgenic steroid (AAS) use is known to be associated with other psychiatric disorders, such as body image disorders, conduct disorder/sociopathy, and other substance use disorders (SUD) – but the causal pathways among these conditions remain poorly delineated.

Methods

We created a directed acyclic graph to diagram hypothesized relationships among AAS use and dependence, body image disorder (BID), conduct disorder/sociopathy, and other SUD. Using proportional hazards models, we then assessed potentially causal relationships among these variables, using a dataset of 233 male weightlifters, of whom 102 had used AAS.

Results

BID and conduct disorder/sociopathy both strongly contributed to the development of AAS use, but did not appear to contribute further to the progression from AAS use to AAS dependence. Other SUD beginning prior to first AAS use – whether broadly defined or restricted only to opioids – failed to show an effect on AAS use or progression to AAS dependence. Conversely, AAS use contributed significantly to the subsequent first-time development of opioid use disorders but did not significantly increase the risk for first-time development of non-opioid SUD, taken as a whole.

Conclusions

Our analysis suggests that AAS use and other SUD are mutually attributable to underlying conduct disorder/sociopathy. SUD do not appear to represent a ‘gateway’ to subsequent AAS use. AAS use may represent a gateway to subsequent opioid use disorder, but probably not to other SUD.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

American Psychiatric Association (2000) Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition, Text Revision (DSM-IV-TR). Washington: American Psychiatric Association.Google Scholar
Arvary, D and Pope, HG (2000) Anabolic-androgenic steroids as a gateway to opioid dependence. New England Journal of Medicine 342, 1532.Google Scholar
Beaver, KM, Vaughn, MG, Delisi, M and Wright, JP (2008) Anabolic-androgenic steroid use and involvement in violent behavior in a nationally representative sample of young adult males in the United States. American Journal of Public Health 98, 21852187.Google Scholar
Benjamini, Y and Hochberg, Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 57, 289300.Google Scholar
Berger, RL and Hsu, JC (1996) Bioequivalence trials, intersection-union tests and equivalence confidence sets. Statistical Science 11, 283302.Google Scholar
Cafri, G, Olivardia, R and Thompson, JK (2008) Symptom characteristics and psychiatric comorbidity among males with muscle dysmorphia. Comprehensive Psychiatry 49, 374379.Google Scholar
Cafri, G, Thompson, JK, Ricciardelli, L, McCabe, M, Smolak, L and Yesalis, C (2005) Pursuit of the muscular ideal: physical and psychological consequences and putative risk factors. Clinical Psychology Review 25, 215239.Google Scholar
Celerier, E, Yazdi, MT, Castane, A, Ghozland, S, Nyberg, F and Maldonado, R (2003) Effects of nandrolone on acute morphine responses, tolerance and dependence in mice. European Journal of Pharmacology 465, 6981.Google Scholar
Choi, PY, Pope, HG and Olivardia, R (2002) Muscle dysmorphia: a new syndrome in weightlifters. British Journal of Sports Medicine 36, 375376; discussion 377.Google Scholar
Chung, B (2003) Muscle dysmorphia in weightlifters. British Journal of Sports Medicine 37, 280281.Google Scholar
Cox, DR and Wermuth, N (1993) Linear dependencies represented by chain graphs. Statistical Science 8, 204218.Google Scholar
Dodge, T and Hoagland, MF (2011) The use of anabolic androgenic steroids and polypharmacy: a review of the literature. Drug and Alcohol Dependence 114, 100109.Google Scholar
Elkins, IJ, McGue, M and Iacono, WG (2007) Prospective effects of attention-deficit/hyperactivity disorder, conduct disorder, and sex on adolescent substance use and abuse. Archives of General Psychiatry 64, 11451152.Google Scholar
First, M, Spitzer, R, Gibbon, M and Williams, J (2001) Structured Clinical Interview for DSM-IV Axis I Disorders — Non-Patient Edition. New York: Biometrics Research Department, New York State Psychiatric Institute.Google Scholar
Garevik, N and Rane, A (2010) Dual use of anabolic-androgenic steroids and narcotics in Sweden. Drug and Alcohol Dependence 109, 144146.Google Scholar
Grambsch, P and Thernau, T (1994) Proportional hazards test and diagnostics based on weighted residuals. Biometrika 81, 515526.Google Scholar
Greenland, S (2003) Quantifying biases in causal models: classical confounding vs collider-stratification bias. Epidemiology 14, 300306.Google Scholar
Greenland, S, Pearl, J and Robins, JM (1999) Causal diagrams for epidemiologic research. Epidemiology 10, 3748.Google Scholar
Hakansson, A, Mickelsson, K, Wallin, C and Berglund, M. (2012) Anabolic androgenic steroids in the general population: user characteristics and associations with substance use. European Addiction Research 18, 8390.Google Scholar
Hallgren, M, Pope, HG, Kanayama, G, Hudson, JI, Lundin, A and Kallmen, H (2015) Anti-social behaviors associated with anabolic-androgenic steroid use among male adolescents. European Addiction Research 21, 32132–6.Google Scholar
Hernán, MA and Robins, JM (2018) Causal Inference. Boca Raton, Florida: Chapman & Hall/CRC.Google Scholar
Hien, D, Matzner, F, First, M, Spitzer, R, Gibbon, M and Williams, J (2004) Structured Clinical Interview for DSM-IV - Child Edition, 2004. Available at http://www.columbia.edu/~jam119/KidSkid.htm (accessed 20 February 2018).Google Scholar
Hildebrandt, T, Langenbucher, J and Schlundt, DG (2004) Muscularity concerns among men: development of attitudinal and perceptual measures. Body Image 1, 169181.Google Scholar
Hudson, JI, Javaras, KN, Laird, NM, VanderWeele, TJ, Pope, HG and Hernan, MA (2008) A structural approach to the familial coaggregation of disorders. Epidemiology 19, 431439.Google Scholar
Hudson, JI, Pope, HG and Glynn, RJ (2005) The cross-sectional cohort study: an underutilized design. Epidemiology 16, 355359.Google Scholar
Kanayama, G, Barry, S, Hudson, JI and Pope, HG (2006) Body image and attitudes toward male roles in anabolic-androgenic steroid users. American Journal of Psychiatry 163, 697703.Google Scholar
Kanayama, G, Brower, KJ, Wood, RI, Hudson, JI and Pope, HG (2009 a) Issues for DSM-V: clarifying the diagnostic criteria for anabolic-androgenic steroid dependence. American Journal of Psychiatry 166, 642645.Google Scholar
Kanayama, G, Brower, KJ, Wood, RI, Hudson, JI and Pope, HG (2010) Treatment of anabolic-androgenic steroid dependence: emerging evidence and its implications. Drug and Alcohol Dependence 109, 613.Google Scholar
Kanayama, G, Cohane, GH, Weiss, RD and Pope, HG (2003) Past anabolic-androgenic steroid use among men admitted for substance abuse treatment: an underrecognized problem? Journal of Clinical Psychiatry 64, 156160.Google Scholar
Kanayama, G, Hudson, JI and Pope, HG (2009 b) Features of men with anabolic-androgenic steroid dependence: a comparison with nondependent AAS users and with AAS nonusers. Drug and Alcohol Dependence 102, 130137.Google Scholar
Kendler, KS and Myers, J (2014) The boundaries of the internalizing and externalizing genetic spectra in men and women. Psychological Medicine 44, 647655.Google Scholar
Kessler, RC, Ormel, J, Petukhova, M, McLaughlin, KA, Green, JG, Russo, LJ et al. (2011) Development of lifetime comorbidity in the World Health Organization world mental health surveys. Archives of General Psychiatry 68, 90100.Google Scholar
Klotz, F, Garle, M, Granath, F and Thiblin, I (2006) Criminality among individuals testing positive for the presence of anabolic androgenic steroids. Archives of General Psychiatry 63, 12741279.Google Scholar
Klotz, F, Petersson, A, Hoffman, O and Thiblin, I (2010) The significance of anabolic androgenic steroids in a Swedish prison population. Comprehensive Psychiatry 51, 312318.Google Scholar
Klotz, F, Petersson, A, Isacson, D and Thiblin, I (2007) Violent crime and substance abuse: a medico-legal comparison between deceased users of anabolic androgenic steroids and abusers of illicit drugs. Forensic Science International 173, 5763.Google Scholar
Koller, D and Friedman, M (2009) Probabilistic Graphical Models: Principles and Techniques. Cambridge, Massachusetts: MIT press.Google Scholar
Krueger, RF (1999) The structure of common mental disorders. Archives of General Psychiatry 56, 921926.Google Scholar
Krueger, RF, Caspi, A, Moffitt, TE and Silva, PA (1998) The structure and stability of common mental disorders (DSM-III-R): a longitudinal-epidemiological study. Journal of Abnormal Psychology 107, 216227.Google Scholar
Lundholm, L, Frisell, T, Lichtenstein, P and Langstrom, N (2015) Anabolic androgenic steroids and violent offending: confounding by polysubstance abuse among 10365 general population men. Addiction 110, 100108.Google Scholar
Lundholm, L, Kall, K, Wallin, S and Thiblin, I (2010) Use of anabolic androgenic steroids in substance abusers arrested for crime. Drug and Alcohol Dependence 111, 222226.Google Scholar
McBride, AJ, Williamson, K and Petersen, T (1996) Three cases of nalbuphine hydrochloride dependence associated with anabolic steroid use. British Journal of Sports Medicine 30, 6970.Google Scholar
McCabe, SE, Brower, KJ, West, BT, Nelson, TF and Wechsler, H (2007) Trends in non-medical use of anabolic steroids by U.S. College students: results from four national surveys. Drug and Alcohol Dependence 90, 243251.Google Scholar
Milner, A, Page, A and LaMontagne, AD (2014) Cause and effect in studies on unemployment, mental health and suicide: a meta-analytic and conceptual review. Psychological Medicine 44, 909917.Google Scholar
Nyberg, F and Hallberg, M (2012) Interactions between opioids and anabolic androgenic steroids: implications for the development of addictive behavior. International Review of Neurobiology 102, 189206.Google Scholar
Olivardia, R, Pope, HG and Hudson, JI (2000) Muscle dysmorphia in male weightlifters: a case-control study. American Journal of Psychiatry 157, 12911296.Google Scholar
Pearl, J (1995) Causal diagrams for empirical research. Biometrika 82, 669688.Google Scholar
Pearl, J (2000) Causality. Cambridge, England: Cambridge University Press.Google Scholar
Peters, KD and Wood, RI (2005) Androgen dependence in hamsters: overdose, tolerance, and potential opioidergic mechanisms. Neuroscience 130, 971981.Google Scholar
Petersson, A, Bengtsson, J, Voltaire-Carlsson, A and Thiblin, I (2010) Substance abusers' motives for using anabolic androgenic steroids. Drug and Alcohol Dependence 111, 170172.Google Scholar
Phillips, KA, Hollander, E, Rasmussen, SA, Aronowitz, BR, DeCaria, C and Goodman, WK (1997) A severity rating scale for body dysmorphic disorder: development, reliability, and validity of a modified version of the Yale-Brown Obsessive Compulsive Scale. Psychopharmacology Bulletin 33, 1722.Google Scholar
Phillips, KA, McElroy, SL, Hudson, JI and Pope, HG (1995) Body dysmorphic disorder: an obsessive-compulsive spectrum disorder, a form of affective spectrum disorder, or both? Journal of Clinical Psychiatry 56(Suppl. 4), 4151; discussion 52.Google Scholar
Phillips, KA, Stein, DJ, Rauch, SL, Hollander, E, Fallon, BA, Barsky, A et al. (2010 a) Should an obsessive-compulsive spectrum grouping of disorders be included in DSM-V? Depression and Anxiety 27, 528555.Google Scholar
Phillips, KA, Wilhelm, S, Koran, LM, Didie, ER, Fallon, BA, Feusner, J et al. (2010 b) Body dysmorphic disorder: some key issues for DSM-V. Depression and Anxiety 27, 573591.Google Scholar
Pope, HG, Gruber, AJ, Choi, P, Olivardia, R and Phillips, KA (1997) Muscle dysmorphia. An underrecognized form of body dysmorphic disorder. Psychosomatics 38, 548557.Google Scholar
Pope, HG, Kanayama, G, Athey, A, Ryan, E, Hudson, JI and Baggish, A (2014 a) The lifetime prevalence of anabolic-androgenic steroid use and dependence in Americans: current best estimates. American Journal on Addictions 23, 371377.Google Scholar
Pope, HG, Kanayama, G and Hudson, J (2012) Risk factors for illicit anabolic-androgenic steroid use in male weightlifters: a cross-sectional cohort study. Biological Psychiatry 71, 254261.Google Scholar
Pope, HG, Kean, J, Nash, A, Kanayama, G, Samuel, DB, Bickel, WK et al. (2010) A diagnostic interview module for anabolic-androgenic steroid dependence: preliminary evidence of reliability and validity. Experimental and Clinical Psychopharmacology 18, 203210.Google Scholar
Pope, HG, Wood, R, Rogol, A, Nyberg, F, Bowers, L and Bhasin, S (2014 b) Adverse health consequences of performance-enhancing drugs: an endocrine society scientific statement. Endocrine Reviews 35, 341375.Google Scholar
Robbins, J, Hernán, MA and Brumback, B (2000) Marginal structural models and causal inference in epidemiology. Epidemiology 11, 550560.Google Scholar
Robins, JM, Smoller, JW and Lunetta, KL (2001) On the validity of the TDT test in the presence of comorbidity and ascertainment bias. Genetic Epidemiology 21, 326336.Google Scholar
Rohman, L (2009) The relationship between anabolic androgenic steroids and muscle dysmorphia: a review. Eating Disorders 17, 187199.Google Scholar
Schuirmann, DJ (1987) A comparison of the 2 one-sided tests procedure and the power approach for assessing the equivalence of average bioavailability. Journal of Pharmacokinetics and Biopharmaceutics 15, 657680.Google Scholar
Skarberg, K, Nyberg, F and Engstrom, I (2009) Multisubstance use as a feature of addiction to anabolic-androgenic steroids. European Addiction Research 15, 99106.Google Scholar
Skarberg, K, Nyberg, F and Engstrom, I (2010) Is there an association between the use of anabolic-androgenic steroids and criminality? European Addiction Research 16, 213219.Google Scholar
Spirtes, P, Glymour, C and Scheines, R (1993) Causation, Prediction and Search. Springer-Verlag: New York.Google Scholar
Tennant, F, Black, DL and Voy, RO (1988) Anabolic steroid dependence with opioid-type features. New England Journal Of Medicine 319, 578.Google Scholar
Thiblin, I and Parlklo, T (2002) Anabolic androgenic steroids and violence. Acta Psychiatrica Scandanavica Supplementum 412, 125128.Google Scholar
Weinberg, NZ and Glantz, MD (1999) Child psychopathology risk factors for drug abuse: overview. Journal of Clinical Child Psychology 28, 290297.Google Scholar
Wines, JD Jr., Gruber, AJ, Pope, HG and Lukas, SE (1999) Nalbuphine hydrochloride dependence in anabolic steroid users. American Journal on Addictions 8, 161164.Google Scholar