Cardiovascular toxicity of illicit anabolic-androgenic steroid use

Circulation

Volumn 135, Issue 21, 2017, Pages 1991-2002

  Baggish, Aaron L ^a,b   Weiner, Rory B ^a,b   Kanayama, Gen ^b,c   Hudson, James I ^b,c   Lu, Michael T ^a   Hoffmann, Udo ^a   Pope, Harrison G ^b,c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MCLEAN HOSPITAL   (United States)

Author keywords

Anabolic androgenic steroids; Atherosclerosis; Cardiology; Cardiomyopathy; Diastolic dysfunction; Men

Indexed keywords

ANABOLIC AGENT; ANDROGEN; ILLICIT DRUG; PERFORMANCE ENHANCING SUBSTANCE; TESTOSTERONE DERIVATIVE;

ADULT; ARTICLE; BLOOD PRESSURE; CARDIOTOXICITY; COHORT ANALYSIS; CONGESTIVE HEART FAILURE; CORONARY ARTERY ATHEROSCLEROSIS; CROSS-SECTIONAL STUDY; DRUG EXPOSURE; DRUG USE; DYSLIPIDEMIA; HEART CATHETERIZATION; HEART EJECTION FRACTION; HEART INFARCTION; HUMAN; MAJOR CLINICAL STUDY; MALE; MYOCARDIAL DISEASE; OBSERVATIONAL STUDY; PRIORITY JOURNAL; RESTING HEART RATE; ATHEROSCLEROTIC PLAQUE; CASE CONTROL STUDY; CHEMICALLY INDUCED; COMPLICATION; COMPUTED TOMOGRAPHIC ANGIOGRAPHY; CORONARY ANGIOGRAPHY; CORONARY ARTERY DISEASE; CORONARY BLOOD VESSEL; DIAGNOSTIC IMAGING; DIASTOLE; DOPING; DRUG DEPENDENCE; DRUG EFFECTS; ECHOCARDIOGRAPHY; HEART LEFT VENTRICLE FUNCTION; HEART STROKE VOLUME; MIDDLE AGED; MULTIDETECTOR COMPUTED TOMOGRAPHY; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; RISK ASSESSMENT; RISK FACTOR; SYSTOLE; TIME FACTOR; WEIGHT LIFTING;

ADULT; ANDROGENS; CARDIOTOXICITY; CASE-CONTROL STUDIES; COMPUTED TOMOGRAPHY ANGIOGRAPHY; CORONARY ANGIOGRAPHY; CORONARY ARTERY DISEASE; CORONARY VESSELS; CROSS-SECTIONAL STUDIES; DIASTOLE; DOPING IN SPORTS; ECHOCARDIOGRAPHY; HUMANS; MALE; MIDDLE AGED; MULTIDETECTOR COMPUTED TOMOGRAPHY; PERFORMANCE-ENHANCING SUBSTANCES; PLAQUE, ATHEROSCLEROTIC; RISK ASSESSMENT; RISK FACTORS; STROKE VOLUME; SUBSTANCE-RELATED DISORDERS; SYSTOLE; TESTOSTERONE CONGENERS; TIME FACTORS; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR FUNCTION, LEFT; WEIGHT LIFTING;

EID: 85019668345     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.116.026945     Document Type: Article

References (47)

1. Pope HG Jr, Wood RI, Rogol A, Nyberg F, Bowers L, Bhasin S. Adverse health consequences of performance-enhancing drugs: An Endocrine Society scientific statement. Endocr Rev. 2014;35:341-375. doi: 10.1210/er.2013-1058.
2. Pope HG Jr, Kanayama G, Athey A, Ryan E, Hudson JI, Baggish A. The lifetime prevalence of anabolic-androgenic steroid use and dependence in Americans: Current best estimates. Am J Addict. 2014;23:371-377. doi: 10.1111/j.1521-0391.2013.12118.x.
3. Kanayama G, Hudson JI, Pope HG Jr. Long-term psychiatric and medical consequences of anabolic-androgenic steroid abuse: A looming public health concern? Drug Alcohol Depend. 2008;98:1-12. doi: 10.1016/j.drugalcdep.2008.05.004.
4. McNutt RA, Ferenchick GS, Kirlin PC, Hamlin NJ. Acute myocardial infarction in a 22-year-old world class weight lifter using anabolic steroids. Am J Cardiol. 1988;62:164.
5. Bowman S. Anabolic steroids and infarction. BMJ. 1990;300:750.
6. Ferenchick GS, Adelman S. Myocardial infarction associated with anabolic steroid use in a previously healthy 37-year-old weight lifter. Am Heart J. 1992;124:507-508.
7. Garevik N, Strahm E, Garle M, Lundmark J, Stahle L, Ekström L, Rane A. Long term perturbation of endocrine parameters and cholesterol metabolism after discontinued abuse of anabolic androgenic steroids. J Steroid Biochem Mol Biol. 2011;127:295-300. doi: 10.1016/j.jsbmb.2011.08.005.
8. Hartgens F, Kuipers H. Effects of androgenic-anabolic steroids in athletes. Sports Med. 2004;34:513-554.
9. Thompson PD, Cullinane EM, Sady SP, Chenevert C, Saritelli AL, Sady MA, Herbert PN. Contrasting effects of testosterone and stanozolol on serum lipoprotein levels. JAMA. 1989;261:1165-1168.
10. Cabral AM, Vasquez EC, Moysés MR, Antonio A. Sex hormone modulation of ventricular hypertrophy in sinoaortic denervated rats. Hypertension. 1988;11(2 Pt 2):I93-I97.
11. Malhotra A, Buttrick P, Scheuer J. Effects of sex hormones on development of physiological and pathological cardiac hypertrophy in male and female rats. Am J Physiol. 1990;259(3 Pt 2):H866-H871.
12. Tagarakis CV, Bloch W, Hartmann G, Hollmann W, Addicks K. Anabolic steroids impair the exercise-induced growth of the cardiac capillary bed. Int J Sports Med. 2000;21:412-418. doi: 10.1055/s-2000-3835.
13. Tagarakis CV, Bloch W, Hartmann G, Hollmann W, Addicks K. Testosterone- propionate impairs the response of the cardiac capillary bed to exercise. Med Sci Sports Exerc. 2000;32:946-953.
14. Norton GR, Trifunovic B, Woodiwiss AJ. Attenuated beta-adrenoceptor- mediated cardiac contractile responses following androgenic steroid administration to sedentary rats. Eur J Appl Physiol. 2000;81:310-316. doi: 10.1007/s004210050048.
15. Frankenfeld SP, Oliveira LP, Ortenzi VH, Rego-Monteiro IC, Chaves EA, Ferreira AC, Leitão AC, Carvalho DP, Fortunato RS. The anabolic androgenic steroid nandrolone decanoate disrupts redox homeostasis in liver, heart and kidney of male Wistar rats. PLoS One. 2014;9:e102699. doi: 10.1371/journal.pone.0102699.
16. Medei E, Marocolo M, Rodrigues Dde C, Arantes PC, Takiya CM, Silva J, Rondinelli E, Goldenberg RC, de Carvalho AC, Nascimento JH. Chronic treatment with anabolic steroids induces ventricular repolarization disturbances: Cellular, ionic and molecular mechanism. J Mol Cell Cardiol. 2010;49:165-175. doi: 10.1016/j. yjmcc.2010.04.014.
17. Zaugg M, Jamali NZ, Lucchinetti E, Xu W, Alam M, Shafiq SA, Siddiqui MA. Anabolic-androgenic steroids induce apoptotic cell death in adult rat ventricular myocytes. J Cell Physiol. 2001;187:90-95.
18. Baggish AL, Weiner RB, Kanayama G, Hudson JI, Picard MH, Hutter AM Jr, Pope HG Jr. Long-term anabolic-androgenic steroid use is associated with left ventricular dysfunction. Circ Heart Fail. 2010;3:472-476. doi: 10.1161/CIRCHEARTFAILURE. 109.931063.
19. D'Andrea A, Caso P, Salerno G, Scarafile R, De Corato G, Mita C, Di Salvo G, Severino S, Cuomo S, Liccardo B, Esposito N, Calabrò R. Left ventricular early myocardial dysfunction after chronic misuse of anabolic androgenic steroids: A Doppler myocardial and strain imaging analysis. Br J Sports Med. 2007;41:149-155. doi: 10.1136/bjsm.2006.030171.
20. Krieg A, Scharhag J, Albers T, Kindermann W, Urhausen A. Cardiac tissue Doppler in steroid users. Int J Sports Med. 2007;28:638-643. doi: 10.1055/s-2007-964848.
21. Luijkx T, Velthuis BK, Backx FJ, Buckens CF, Prakken NH, Rienks R, Mali WP, Cramer MJ. Anabolic androgenic steroid use is associated with ventricular dysfunction on cardiac MRI in strength trained athletes. Int J Cardiol. 2013;167:664-668. doi: 10.1016/j.ijcard. 2012.03.072.
22. Nottin S, Nguyen LD, Terbah M, Obert P. Cardiovascular effects of androgenic anabolic steroids in male bodybuilders determined by tissue Doppler imaging. Am J Cardiol. 2006;97:912-915. doi: 10.1016/j.amjcard.2005.10.026.
23. Angell PJ, Ismail TF, Jabbour A, Smith G, Dahl A, Wage R, Whyte G, Green DJ, Prasad S, George K. Ventricular structure, function, and focal fibrosis in anabolic steroid users: A CMR study. Eur J Appl Physiol. 2015;114:921-928.
24. Santora LJ, Marin J, Vangrow J, Minegar C, Robinson M, Mora J, Friede G. Coronary calcification in body builders using anabolic steroids. Prev Cardiol. 2006;9:198-201.
25. Hassan NA, Salem MF, Sayed MA. Doping and effects of anabolic androgenic steroids on the heart: Histological, ultrastructural, and echocardiographic assessment in strength athletes. Hum Exp Toxicol. 2009;28:273-283. doi: 10.1177/0960327109104821.
26. Kasikcioglu E, Oflaz H, Umman B, Bugra Z. Androgenic anabolic steroids also impair right ventricular function. Int J Cardiol. 2009;134:123-125. doi: 10.1016/j.ijcard.2007.12.027.
27. Hudson JI, Pope HG Jr, Glynn RJ. The cross-sectional cohort study: An underutilized design. Epidemiology. 2005;16:355-359.
28. Kanayama G, DeLuca J, Meehan WP 3rd, Hudson JI, Isaacs S, Baggish A, Weiner R, Micheli L, Pope HG Jr. Ruptured tendons in anabolic-androgenic steroid users: A cross-sectional cohort study. Am J Sports Med. 2015;43:2638-2644. doi: 10.1177/0363546515602010.
29. Pope HG Jr, Kanayama G, Hudson JI. Risk factors for illicit anabolic- androgenic steroid use in male weightlifters: A cross-sectional cohort study. Biol Psychiatry. 2012;71:254-261. doi: 10.1016/j. biopsych.2011.06.024.
30. Arnold B, Arana B, Mäusezahl D, Hubbard A, Colford JM Jr. Evaluation of a pre-existing, 3-year household water treatment and handwashing intervention in rural Guatemala. Int J Epidemiol. 2009;38:1651-1661. doi: 10.1093/ije/dyp241.
31. Ljungman C, Kahan T, Schiöler L, Hjerpe P, Wettermark B, Boström KB, Manhem K. Antihypertensive treatment and control according to gender, education, country of birth and psychiatric disorder: The Swedish Primary Care Cardiovascular Database (SPCCD). J Hum Hypertens. 2015;29:385-393. doi: 10.1038/ jhh.2014.100.
32. Kessler RC, Borges G, Walters EE. Prevalence of and risk factors for lifetime suicide attempts in the National Comorbidity Survey. Arch Gen Psychiatry. 1999;56:617-626.
33. Whitlock G, Norton R, Clark T, Pledger M, Jackson R, MacMahon S. Motor vehicle driver injury and socioeconomic status: A cohort study with prospective and retrospective driver injuries. J Epidemiol Community Health. 2003;57:512-516.
34. Bahrke MS, Yesalis CE, Kopstein AN, Stephens JA. Risk factors associated with anabolic-androgenic steroid use among adolescents. Sports Med. 2000;29:397-405.
35. Ip EJ, Barnett MJ, Tenerowicz MJ, Perry PJ. The Anabolic 500 survey: Characteristics of male users versus nonusers of anabolic- androgenic steroids for strength training. Pharmacotherapy. 2011;31:757-766. doi: 10.1592/phco.31.8.757.
36. Parkinson AB, Evans NA. Anabolic androgenic steroids: A survey of 500 users. Med Sci Sports Exerc. 2006;38:644-651. doi: 10.1249/01.mss.0000210194.56834.5d.
37. Kouri EM, Pope HG Jr, Katz DL, Oliva P. Fat-free mass index in users and nonusers of anabolic-androgenic steroids. Clin J Sport Med. 1995;5:223-228.
38. Kanayama G, Pope HG, Cohane G, Hudson JI. Risk factors for anabolic- androgenic steroid use among weightlifters: A case-control study. Drug Alcohol Depend. 2003;71:77-86.
39. First M, Spitzer R, Gibbon M, Williams J. Structured Clinical Interview for DSM?IV Axis I Disorders?Patient Edition. New York: Biometrics Research Department, New York State Psychiatric Institute; 2001.
40. Pope HG, Katz DL. Psychiatric effects of exogenous anabolicandrogenic steroids. In: Wolkowitz OM, Rothschild AJ, eds. Psychoneuroendocrinology: The scientific basis of clinical practice. Washington, DC: American Psychiatric Press; 2003:331-358.
41. Pope HG, Kanayama G. Can you tell if your patient is using anabolic steroids? Curr Psychiatry Prim Care. 2005;1:28-34.
42. Weiner RB, Wang F, Isaacs SK, Malhotra R, Berkstresser B, Kim JH, Hutter AM Jr, Picard MH, Wang TJ, Baggish AL. Blood pressure and left ventricular hypertrophy during American-style football participation. Circulation. 2013;128:524-531. doi: 10.1161/CIRCULATIONAHA. 113.003522.
43. Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, Flachskampf FA, Foster E, Goldstein SA, Kuznetsova T, Lancellotti P, Muraru D, Picard MH, Rietzschel ER, Rudski L, Spencer KT, Tsang W, Voigt JU. Recommendations for cardiac chamber quantification by echocardiography in adults: An update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2015;28:1. e14-39.e14.
44. Nagueh SF, Smiseth OA, Appleton CP, Byrd BF 3rd, Dokainish H, Edvardsen T, Flachskampf FA, Gillebert TC, Klein AL, Lancellotti P, Marino P, Oh JK, Popescu BA, Waggoner AD. Recommendations for the evaluation of left ventricular diastolic function by echocardiography: An update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2016;29:277-314. doi: 10.1016/j.echo.2016.01.011.
45. Maurovich-Horvat P, Ferencik M, Bamberg F, Hoffmann U. Methods of plaque quantification and characterization by cardiac computed tomography. J Cardiovasc Comput Tomogr. 2009;3(Suppl 2):S91-S98. doi: 10.1016/j.jcct.2009.10.012.
46. Hoffmann MH, Shi H, Schmitz BL, Schmid FT, Lieberknecht M, Schulze R, Ludwig B, Kroschel U, Jahnke N, Haerer W, Brambs HJ, Aschoff AJ. Noninvasive coronary angiography with multislice computed tomography. JAMA. 2005;293:2471-2478. doi: 10.1001/jama.293.20.2471.
47. Hartgens F, Rietjens G, Keizer HA, Kuipers H, Wolffenbuttel BH. Effects of androgenic-anabolic steroids on apolipoproteins and lipoprotein (a). Br J Sports Med. 2004;38:253-259.