Semin Thromb Hemost 2018; 44(08): 734-746
DOI: 10.1055/s-0038-1670639
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Anabolic Androgenic Steroid Abuse: The Effects on Thrombosis Risk, Coagulation, and Fibrinolysis

Simon Chang
1   Unit for Thrombosis Research, Department of Regional Health Research, University of Southern Denmark and Department of Clinical Biochemistry, Hospital of South West Jutland, Esbjerg, Denmark
,
Anna-Marie B. Münster
1   Unit for Thrombosis Research, Department of Regional Health Research, University of Southern Denmark and Department of Clinical Biochemistry, Hospital of South West Jutland, Esbjerg, Denmark
,
Jørgen Gram
1   Unit for Thrombosis Research, Department of Regional Health Research, University of Southern Denmark and Department of Clinical Biochemistry, Hospital of South West Jutland, Esbjerg, Denmark
,
Johannes J. Sidelmann
1   Unit for Thrombosis Research, Department of Regional Health Research, University of Southern Denmark and Department of Clinical Biochemistry, Hospital of South West Jutland, Esbjerg, Denmark
› Author Affiliations
Further Information

Publication History

Publication Date:
28 September 2018 (online)

Abstract

Anabolic androgenic steroid (AAS) abuse surged during the 1980s and is seen in approximately 1 in 20 of all males today. A wide spectrum of AAS compounds and abuse regimens are applied and AAS abuse has been associated with an unfavorable cardiovascular profile. The aim of this review is to critique the collected data concerning effects of AAS abuse on thrombosis risk through presentation of condensed evidence from studies investigating AAS-induced changes in coagulation, fibrinolysis, and cardiovascular risk markers. AAS abuse inflicts a procoagulant distribution of cardiovascular risk markers including dyslipidemia and atherosclerosis proneness. AAS abuse overall stimulates synthesis of coagulation factors, inhibitors, and fibrinolytic proteins resulting in both increased global coagulation and stimulation of fibrinolysis. Overall, supported by many case reports and some epidemiological studies, AAS abuse is associated with an increased risk of thrombosis. However, to provide clear evidence for a causal relationship between AAS abuse and thrombosis risk, future studies need to address a range of potential biases, insufficient methodology, and other shortcomings of the current literature as highlighted in this review.

 
  • References

  • 1 Kanayama G, Pope Jr HG. History and epidemiology of anabolic androgens in athletes and non-athletes. Mol Cell Endocrinol 2018; 464: 4-13
  • 2 Bhasin S, Storer TW, Berman N. , et al. The effects of supraphysiologic doses of testosterone on muscle size and strength in normal men. N Engl J Med 1996; 335 (01) 1-7
  • 3 Forbes GB, Porta CR, Herr BE, Griggs RC. Sequence of changes in body composition induced by testosterone and reversal of changes after drug is stopped. JAMA 1992; 267 (03) 397-399
  • 4 Giorgi A, Weatherby RP, Murphy PW. Muscular strength, body composition and health responses to the use of testosterone enanthate: a double blind study. J Sci Med Sport 1999; 2 (04) 341-355
  • 5 Pope Jr HG, 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 (03) 341-375
  • 6 Forsdahl G, Erceg D, Geisendorfer T. , et al. Detection of testosterone esters in blood. Drug Test Anal 2015; 7 (11-12): 983-989
  • 7 Johannisson M, Warnecke M, Berge J. , et al , eds. Strategy for Stopping Steroids. 1st ed. Copenhagen: Anti Doping Denmark; 2012
  • 8 Sidelmann JJ, Kluft C, Krug AH, Winkler U, Jespersen J, Gram JB. Fibrin clot structure - pro-fibrinolytic effect of oral contraceptives in apparently healthy women. Thromb Haemost 2017; 117 (04) 700-705
  • 9 Parker C, Coupland C, Hippisley-Cox J. Antipsychotic drugs and risk of venous thromboembolism: nested case-control study. BMJ 2010; 341: c4245
  • 10 Rasmussen JJ, Selmer C, Østergren PB. , et al. Former abusers of anabolic androgenic steroids exhibit decreased testosterone levels and hypogonadal symptoms years after cessation: a case-control study. PLoS One 2016; 11 (08) e0161208
  • 11 Rodenburg G, Spijkerman R, Eijnden Rvd, Mheen Dvd. Nationaal Prevalentie Onderzoek Middelengebruik 2005. Rotterdam: IVO; 2007: 160
  • 12 Sagoe D, Molde H, Andreassen CS, Torsheim T, Pallesen S. The global epidemiology of anabolic-androgenic steroid use: a meta-analysis and meta-regression analysis. Ann Epidemiol 2014; 24 (05) 383-398
  • 13 Pope Jr HG, 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 (04) 371-377
  • 14 McBride JA, Carson III CC, Coward M. The availability and acquisition of illicit anabolic androgenic steroids and testosterone preparations on the Internet. Am J Mens Health 2016; pii: 1557988316648704 [Epub ahead of print]
  • 15 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 (01) 164
  • 16 Huie MJ. An acute myocardial infarction occurring in an anabolic steroid user. Med Sci Sports Exerc 1994; 26 (04) 408-413
  • 17 Ilhan E, Demirci D, Güvenç TS, Calık AN. Acute myocardial infarction and renal infarction in a bodybuilder using anabolic steroids. Turk Kardiyol Dern Ars 2010; 38 (04) 275-278
  • 18 Güneş Y, Erbaş C, Okuyan E, Babalik E, Gürmen T. Myocardial infarction with intracoronary thrombus induced by anabolic steroids. Anadolu Kardiyol Derg 2004; 4 (04) 357-358
  • 19 Poorzand H, Jafarzadeh Esfehani R, Hosseinzadeh P, Vojdanparast M. Acute myocardial infarction in a young male wrestler: a case report. ARYA Atheroscler 2015; 11 (06) 366-369
  • 20 Tischer KH, Heyny-von Haussen R, Mall G, Doenecke P. Coronary thrombosis and ectasia of coronary arteries after long-term use of anabolic steroids [in German]. Z Kardiol 2003; 92 (04) 326-331
  • 21 Ment J, Ludman PF. Coronary thrombus in a 23 year old anabolic steroid user. Heart 2002; 88 (04) 342
  • 22 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 (02) 507-508
  • 23 Kennedy C. Myocardial infarction in association with misuse of anabolic steroids. Ulster Med J 1993; 62 (02) 174-176
  • 24 Hourigan LA, Rainbird AJ, Dooris M. Intracoronary stenting for acute myocardial infarction (AMI) in a 24-year-old man using anabolic androgenic steroids. Aust N Z J Med 1998; 28 (06) 838-839
  • 25 Frankle MA, Eichberg R, Zachariah SB. Anabolic androgenic steroids and a stroke in an athlete: case report. Arch Phys Med Rehabil 1988; 69 (08) 632-633
  • 26 Santamarina RD, Besocke AG, Romano LM, Ioli PL, Gonorazky SE. Ischemic stroke related to anabolic abuse. Clin Neuropharmacol 2008; 31 (02) 80-85
  • 27 Colburn S, Childers WK, Chacon A, Swailes A, Ahmed FM, Sahi R. The cost of seeking an edge: recurrent renal infarction in setting of recreational use of anabolic steroids. Ann Med Surg (Lond) 2017; 14: 25-28
  • 28 McCulloch NA, Abbas JR, Simms MH. Multiple arterial thromboses associated with anabolic androgenic steroids. Clin J Sport Med 2014; 24 (02) 153-154
  • 29 McCarthy K, Tang AT, Dalrymple-Hay MJ, Haw MP. Ventricular thrombosis and systemic embolism in bodybuilders: etiology and management. Ann Thorac Surg 2000; 70 (02) 658-660
  • 30 Nieminen MS, Rämö MP, Viitasalo M. , et al. Serious cardiovascular side effects of large doses of anabolic steroids in weight lifters. Eur Heart J 1996; 17 (10) 1576-1583
  • 31 Chu K, Kang DW, Kim DE, Roh JK. Cerebral venous thrombosis associated with tentorial subdural hematoma during oxymetholone therapy. J Neurol Sci 2001; 185 (01) 27-30
  • 32 Sveinsson O, Herrman L. Cortical venous thrombosis following exogenous androgen use for bodybuilding. BMJ Case Rep 2013; 2013: bcr2012008638
  • 33 Sahraian MA, Mottamedi M, Azimi AR, Moghimi B. Androgen-induced cerebral venous sinus thrombosis in a young body builder: case report. BMC Neurol 2004; 4 (01) 22
  • 34 Richard S, Lacour JC, Frotscher B, Enea A, Mione G, Ducrocq X. Report of a recurrent cerebral venous thrombosis in a young athlete. BMC Neurol 2014; 14: 182
  • 35 Choe H, Elfil M, DeSancho MT. Inherited antithrombin deficiency and anabolic steroids: a risky combination. Blood Coagul Fibrinolysis 2016; 27 (06) 717-719
  • 36 Liljeqvist S, Helldén A, Bergman U, Söderberg M. Pulmonary embolism associated with the use of anabolic steroids. Eur J Intern Med 2008; 19 (03) 214-215
  • 37 Gaede JT, Montine TJ. Massive pulmonary embolus and anabolic steroid abuse. JAMA 1992; 267 (17) 2328-2329
  • 38 Jaillard AS, Hommel M, Mallaret M. Venous sinus thrombosis associated with androgens in a healthy young man. Stroke 1994; 25 (01) 212-213
  • 39 Pärssinen M, Kujala U, Vartiainen E, Sarna S, Seppälä T. Increased premature mortality of competitive powerlifters suspected to have used anabolic agents. Int J Sports Med 2000; 21 (03) 225-227
  • 40 Thiblin I, Garmo H, Garle M. , et al. Anabolic steroids and cardiovascular risk: a national population-based cohort study. Drug Alcohol Depend 2015; 152: 87-92
  • 41 Morgentaler A, Miner MM, Caliber M. , et al. Testosterone therapy and cardiovascular risk: advances and controversies. Mayo Clin Proc 2015; 90 (02) 224-251
  • 42 Martinez C, Suissa S, Rietbrock S. , et al. Testosterone treatment and risk of venous thromboembolism: population based case-control study. BMJ 2016; 355: i5968
  • 43 Vanberg P, Atar D. Androgenic anabolic steroid abuse and the cardiovascular system. Handb Exp Pharmacol 2010; (195) 411-457
  • 44 Angell P, Chester N, Green D, Somauroo J, Whyte G, George K. Anabolic steroids and cardiovascular risk. Sports Med 2012; 42 (02) 119-134
  • 45 Achar S, Rostamian A, Narayan SM. Cardiac and metabolic effects of anabolic-androgenic steroid abuse on lipids, blood pressure, left ventricular dimensions, and rhythm. Am J Cardiol 2010; 106 (06) 893-901
  • 46 Baggish AL, Weiner RB, Kanayama G. , et al. Cardiovascular toxicity of illicit anabolic-androgenic steroid use. Circulation 2017; 135 (21) 1991-2002
  • 47 Far HR, Ågren G, Thiblin I. Cardiac hypertrophy in deceased users of anabolic androgenic steroids: an investigation of autopsy findings. Cardiovasc Pathol 2012; 21 (04) 312-316
  • 48 Kinson GA, Layberry RA, Hébert B. Influences of anabolic androgens on cardiac growth and metabolism in the rat. Can J Physiol Pharmacol 1991; 69 (11) 1698-1704
  • 49 Takala TE, Rämö P, Kiviluoma K, Vihko V, Kainulainen H, Kettunen R. Effects of training and anabolic steroids on collagen synthesis in dog heart. Eur J Appl Physiol Occup Physiol 1991; 62 (01) 1-6
  • 50 Luke JL, Farb A, Virmani R, Sample RH. Sudden cardiac death during exercise in a weight lifter using anabolic androgenic steroids: pathological and toxicological findings. J Forensic Sci 1990; 35 (06) 1441-1447
  • 51 Thiblin I, Lindquist O, Rajs J. Cause and manner of death among users of anabolic androgenic steroids. J Forensic Sci 2000; 45 (01) 16-23
  • 52 Frati P, Busardò FP, Cipolloni L, Dominicis ED, Fineschi V. Anabolic androgenic steroid (AAS) related deaths: autoptic, histopathological and toxicological findings. Curr Neuropharmacol 2015; 13 (01) 146-159
  • 53 Santora LJ, Marin J, Vangrow J. , et al. Coronary calcification in body builders using anabolic steroids. Prev Cardiol 2006; 9 (04) 198-201
  • 54 Hoff JA, Chomka EV, Krainik AJ, Daviglus M, Rich S, Kondos GT. Age and gender distributions of coronary artery calcium detected by electron beam tomography in 35,246 adults. Am J Cardiol 2001; 87 (12) 1335-1339
  • 55 Fineschi V, Baroldi G, Monciotti F, Paglicci Reattelli L, Turillazzi E. Anabolic steroid abuse and cardiac sudden death: a pathologic study. Arch Pathol Lab Med 2001; 125 (02) 253-255
  • 56 Darke S, Torok M, Duflou J. Sudden or unnatural deaths involving anabolic-androgenic steroids. J Forensic Sci 2014; 59 (04) 1025-1028
  • 57 Lyngberg KK. Myokardieinfarkt og død af bodybuilder behandlet med anabole steroider. Ugeskr Laeger 1991; 153 (08) 587-588
  • 58 Rasmussen JJ, Schou M, Madsen PL. , et al. Increased blood pressure and aortic stiffness among abusers of anabolic androgenic steroids: potential effect of suppressed natriuretic peptides in plasma?. J Hypertens 2018; 36 (02) 277-285
  • 59 Barbosa Neto O, da Mota GR, De Sordi CC. , et al. Long-term anabolic steroids in male bodybuilders induce cardiovascular structural and autonomic abnormalities. Clin Auton Res 2018; 28 (02) 231-244
  • 60 Rasmussen JJ, Schou M, Selmer C. , et al. Insulin sensitivity in relation to fat distribution and plasma adipocytokines among abusers of anabolic androgenic steroids. Clin Endocrinol (Oxf) 2017; 87 (03) 249-256
  • 61 Severo CB, Ribeiro JP, Umpierre D. , et al. Increased atherothrombotic markers and endothelial dysfunction in steroid users. Eur J Prev Cardiol 2013; 20 (02) 195-201
  • 62 Grace FM, Davies B. Raised concentrations of C reactive protein in anabolic steroid using bodybuilders. Br J Sports Med 2004; 38 (01) 97-98
  • 63 Ebenbichler CF, Sturm W, Gänzer H. , et al. Flow-mediated, endothelium-dependent vasodilatation is impaired in male body builders taking anabolic-androgenic steroids. Atherosclerosis 2001; 158 (02) 483-490
  • 64 Ferenchick G, Schwartz D, Ball M, Schwartz K. Androgenic-anabolic steroid abuse and platelet aggregation: a pilot study in weight lifters. Am J Med Sci 1992; 303 (02) 78-82
  • 65 Ajayi AA, Mathur R, Halushka PV. Testosterone increases human platelet thromboxane A2 receptor density and aggregation responses. Circulation 1995; 91 (11) 2742-2747
  • 66 Melchert RB, Welder AA. Cardiovascular effects of androgenic-anabolic steroids. Med Sci Sports Exerc 1995; 27 (09) 1252-1262
  • 67 Cunha TS, Moura MJ, Bernardes CF, Tanno AP, Marcondes FK. Vascular sensitivity to phenylephrine in rats submitted to anaerobic training and nandrolone treatment. Hypertension 2005; 46 (04) 1010-1015
  • 68 Sidelmann JJ, Gram J, Jespersen J, Kluft C. Fibrin clot formation and lysis: basic mechanisms. Semin Thromb Hemost 2000; 26 (06) 605-618
  • 69 Kluft C, Preston FE, Malia RG. , et al. Stanozolol-induced changes in fibrinolysis and coagulation in healthy adults. Thromb Haemost 1984; 51 (02) 157-164
  • 70 Thorisdottir H, Evans JA, Schwartz HJ, Comp P, Haluschak J, Ratnoff OD. Some clotting factors in plasma during danazol therapy: free and total protein S, but not C4b-binding protein, are elevated by danazol therapy. J Lab Clin Med 1992; 119 (06) 698-701
  • 71 Gralnick HR, Maisonneuve P, Sultan Y, Rick ME. Benefits of danazol treatment in patients with hemophilia A (classic hemophilia). JAMA 1985; 253 (08) 1151-1153
  • 72 Gralnick HR, Rick ME. Danazol increases factor VIII and factor IX in classic hemophilia and Christmas disease. N Engl J Med 1983; 308 (23) 1393-1395
  • 73 Saidi P, Lega BZ, Kim HC, Raska Jr K. Effect of danazol on clotting factor levels, bleeding incidence, factor infusion requirements, and immune parameters in hemophilia. Blood 1986; 68 (03) 673-679
  • 74 Greer IA, Greaves M, Madhok R. , et al. Effect of stanozolol on factors VIII and IX and serum aminotransferases in haemophilia. Thromb Haemost 1985; 53 (03) 386-389
  • 75 Kahn NN, Sinha AK, Spungen AM, Bauman WA. Effects of oxandrolone, an anabolic steroid, on hemostasis. Am J Hematol 2006; 81 (02) 95-100
  • 76 Small M, McArdle BM, Lowe GD, Forbes CD, Prentice CR. The effect of intramuscular stanozolol on fibrinolysis and blood lipids. Thromb Res 1982; 28 (01) 27-36
  • 77 Broekmans AW, Conard J, van Weyenberg RG, Horellou MH, Kluft C, Bertina RM. Treatment of hereditary protein C deficiency with stanozolol. Thromb Haemost 1987; 57 (01) 20-24
  • 78 Ansell JE, Tiarks C, Fairchild VK. Coagulation abnormalities associated with the use of anabolic steroids. Am Heart J 1993; 125 (2, Pt 1): 367-371
  • 79 Kluft C, Bertina RM, Preston FE. , et al. Protein C, an anticoagulant protein, is increased in healthy volunteers and surgical patients after treatment with stanozolol. Thromb Res 1984; 33 (03) 297-304
  • 80 Preston FE, Malia RG, Greaves M, Kluft C, Bertina RM, Segal DS. Effect of stanozolol on antithrombin III and protein C. Lancet 1983; 2 (8348): 517-518
  • 81 González F, Kirwan JP, Rote NS, Minium J. Elevated circulating levels of tissue factor in polycystic ovary syndrome. Clin Appl Thromb Hemost 2013; 19 (01) 66-72
  • 82 Chang S, Rasmussen JJ, Frandsen MN. , et al. Procoagulant state in current and former anabolic androgenic steroid abusers. Thromb Haemost 2018; 118 (04) 647-653
  • 83 Glueck CJ, Freiberg R, Glueck HI, Tracy T, Stroop D, Wang Y. Idiopathic osteonecrosis, hypofibrinolysis, high plasminogen activator inhibitor, high lipoprotein(a), and therapy with Stanozolol. Am J Hematol 1995; 48 (04) 213-220
  • 84 Fearnley GR, Chakrabarti R, Evans JF. Fibrinolytic and defibrinating effect of phenformin plus ethyloestrenol in vivo. Lancet 1969; 1 (7601): 910-914
  • 85 Jarrett PE, Morland M, Browse NL. Treatment of Raynaud's phenomenon by fibrinolytic enhancement. BMJ 1978; 2 (6136): 523-525
  • 86 Burnand K, Clemenson G, Morland M, Jarrett PE, Browse NL. Venous lipodermatosclerosis: treatment by fibrinolytic enhancement and elastic compression. BMJ 1980; 280 (6206): 7-11
  • 87 Owens MR, Cimino CD, Donnelly J. Testosterone effects on biosynthesis of coagulation proteins. Thromb Haemost 1987; 57 (03) 259-262
  • 88 Barbosa J, Seal US, Doe RP. Effects of anabolic steroids on haptoglobin, orosomucoid, plasminogen, fibrinogen, transferrin, ceruloplasmin, alpha-1-antitrypsin, beta-glucuronidase and total serum proteins. J Clin Endocrinol Metab 1971; 33 (03) 388-398
  • 89 Ferenchick GS, Hirokawa S, Mammen EF, Schwartz KA. Anabolic-androgenic steroid abuse in weight lifters: evidence for activation of the hemostatic system. Am J Hematol 1995; 49 (04) 282-288
  • 90 Ledford MR, Horton A, Wang G, Brito M, Delgado L. Efficacy of danazol in a patient with congenital protein-S deficiency: paradoxical evidence for decreased platelet activation with increased thrombin generation. Thromb Res 1997; 87 (05) 473-482
  • 91 Davis III AE, Lu F, Mejia P. C1 inhibitor, a multi-functional serine protease inhibitor. Thromb Haemost 2010; 104 (05) 886-893
  • 92 Naudin C, Burillo E, Blankenberg S, Butler L, Renné T. Factor XII contact activation. Semin Thromb Hemost 2017; 43 (08) 814-826
  • 93 Laurell CB, Rannevik G. A comparison of plasma protein changes induced by danazol, pregnancy, and estrogens. J Clin Endocrinol Metab 1979; 49 (05) 719-725
  • 94 Bork K. Current management options for hereditary angioedema. Curr Allergy Asthma Rep 2012; 12 (04) 273-280
  • 95 Schapira M. Major inhibitors of the contact phase coagulation factors. Semin Thromb Hemost 1987; 13 (01) 69-78
  • 96 Walker ID, Davidson JF, Young P, Conkie JA. Effect of anabolic steroids on plasma antithrombin III. alpha2 macroglobulin and alpha1 antitrypsin levels. Thromb Diath Haemorrh 1975; 34 (01) 106-114
  • 97 Gonzalez R, Alberca I, Sala N, Vicente V. Protein C deficiency--response to danazol and DDAVP. Thromb Haemost 1985; 53 (03) 320-322
  • 98 Mannucci PM, Bottasso B, Sharon C, Tripodi A. Treatment with stanozolol of type I protein C deficiency in an Italian family. Ric Clin Lab 1984; 14 (04) 673-680
  • 99 Anderson RA, Ludlam CA, Wu FC. Haemostatic effects of supraphysiological levels of testosterone in normal men. Thromb Haemost 1995; 74 (02) 693-697
  • 100 Maroney SA, Mast AE. New insights into the biology of tissue factor pathway inhibitor. J Thromb Haemost 2015; 13 (Suppl. 01) S200-S207
  • 101 Jin H, Lin J, Fu L. , et al. Physiological testosterone stimulates tissue plasminogen activator and tissue factor pathway inhibitor and inhibits plasminogen activator inhibitor type 1 release in endothelial cells. Biochem Cell Biol 2007; 85 (02) 246-251
  • 102 Lupu C, Zhu H, Popescu NI, Wren JD, Lupu F. Novel protein ADTRP regulates TFPI expression and function in human endothelial cells in normal conditions and in response to androgen. Blood 2011; 118 (16) 4463-4471
  • 103 Agledahl I, Brodin E, Svartberg J, Hansen JB. Plasma free tissue factor pathway inhibitor (TFPI) levels and TF-induced thrombin generation ex vivo in men with low testosterone levels. Thromb Haemost 2009; 101 (03) 471-477
  • 104 Agledahl I, Brodin E, Svartberg J, Hansen JB. Impact of long-term testosterone treatment on plasma levels of free TFPI and TF-induced thrombin generation ex vivo in elderly men with low testosterone levels. Thromb Haemost 2009; 102 (05) 945-950
  • 105 Ellery PE, Adams MJ. Tissue factor pathway inhibitor: then and now. Semin Thromb Hemost 2014; 40 (08) 881-886
  • 106 Hackeng TM, Seré KM, Tans G, Rosing J. Protein S stimulates inhibition of the tissue factor pathway by tissue factor pathway inhibitor. Proc Natl Acad Sci U S A 2006; 103 (09) 3106-3111
  • 107 Roşca AE, Badiu C, Uscătescu V. , et al. Influence of chronic administration of anabolic androgenic steroids and taurine on haemostasis profile in rats: a thrombelastographic study. Blood Coagul Fibrinolysis 2013; 24 (03) 256-260
  • 108 Borrelli A, Bellino C, Bozzetta E. , et al. Thromboelastometry in veal calves to detect hemostatic variations caused by low doses of dexamethasone treatment. BMC Vet Res 2013; 9: 55
  • 109 Fearnley GR, Chakrabarti R. Increase of blood fibrinolytic activity by testosterone. Lancet 1962; 2 (7247): 128-132
  • 110 Davidson JF, Lochhead M, McDonald GA, McNicol GP. Fibrinolytic enhancement by stanozolol: a double blind trial. Br J Haematol 1972; 22 (05) 543-559
  • 111 Walker ID, Davidson JF, Young P, Conkie JA. Plasma fibrinolytic activity following oral anabolic steroid therapy. Thromb Diath Haemorrh 1975; 34 (01) 236-245
  • 112 Kumada T, Abiko Y. Enhancement of fibrinolytic and thrombolytic potential in the rat by treatment with an anabolic steroid, furazabol. Thromb Haemost 1976; 36 (02) 451-464
  • 113 Blamey SL, McArdle BM, Burns P. , et al. Prevention of fibrinolytic shut-down after major surgery by intramuscular stanozolol. Thromb Res 1983; 31 (03) 451-459
  • 114 Sidelmann J. Contact Activation of the Fibrinolytic System in Human Blood. PhD dissertation. Esbjerg: Odense University; 1997: 83
  • 115 Jones AL, Hulett MD, Parish CR. Histidine-rich glycoprotein: a novel adaptor protein in plasma that modulates the immune, vascular and coagulation systems. Immunol Cell Biol 2005; 83 (02) 106-118
  • 116 Gram J, Jespersen J, Ingeberg S, Bentsen KD, Bach E. Plasma histidine-rich glycoprotein and plasminogen in patients with liver disease. Thromb Res 1985; 39 (04) 411-417
  • 117 Verheijen JH, Rijken DC, Chang GT, Preston FE, Kluft C. Modulation of rapid plasminogen activator inhibitor in plasma by stanozolol. Thromb Haemost 1984; 51 (03) 396-397
  • 118 Heiman M, Gupta S, Khan SS, Vaughan DE, Shapiro AD. Complete plasminogen activator inhibitor 1 deficiency. In: Adam MP, Ardinger HH, Pagon RA. , et al, eds. GeneReviews®. Seattle, WA: University of Washington; 1993
  • 119 Minowa H, Takahashi Y, Tanaka T. , et al. Four cases of bleeding diathesis in children due to congenital plasminogen activator inhibitor-1 deficiency. Haemostasis 1999; 29 (05) 286-291
  • 120 Winwood PJ, Robertson DA, Wright R. Bleeding oesophageal varices associated with anabolic steroid use in an athlete. Postgrad Med J 1990; 66 (780) 864-865
  • 121 Schumacher J, Müller G, Klotz KF. Large hepatic hematoma and intraabdominal hemorrhage associated with abuse of anabolic steroids. N Engl J Med 1999; 340 (14) 1123-1124
  • 122 Alaraj AM, Chamoun RB, Dahdaleh NS, Haddad GF, Comair YG. Spontaneous subdural haematoma in anabolic steroids dependent weight lifters: reports of two cases and review of literature. Acta Neurochir (Wien) 2005; 147 (01) 85-87 , discussion 87–88
  • 123 Yasar Yildiz S, Kuru P, Toksoy Oner E, Agirbasli M. Functional stability of plasminogen activator inhibitor-1. Sci World J 2014; 2014: 858293
  • 124 Declerck PJ, Moreau H, Jespersen J, Gram J, Kluft C. Multicenter evaluation of commercially available methods for the immunological determination of plasminogen activator inhibitor-1 (PAI-1). Thromb Haemost 1993; 70 (05) 858-863
  • 125 Gram J, Declerck PJ, Sidelmann J, Jespersen J, Kluft C. Multicentre evaluation of commercial kit methods: plasminogen activator inhibitor activity. Thromb Haemost 1993; 70 (05) 852-857
  • 126 Kloner RA, Carson III C, Dobs A, Kopecky S, Mohler III ER. Testosterone and cardiovascular disease. J Am Coll Cardiol 2016; 67 (05) 545-557
  • 127 Chang S, Rasmussen JJ, Frandsen MN. , et al. Procoagulant state in current and former anabolic androgenic steroid abusers. Throm Haemost 2018; 118 (04) 647-653
  • 128 Rasmussen JJ, Schou M, Madsen PL. , et al. Increased blood pressure and aortic stiffness among abusers of anabolic androgenic steroids: potential effect of suppressed natriuretic peptides in plasma?. J Hypertens 2018; 36 (02) 277-285
  • 129 Ge Y, Liu S, Singh SM. Strong man with a weak heart: the ill effects of performance-enhancing drug use. Am J Med 2017; 130 (01) e5-e7
  • 130 Jespersen J, Gram J, Kluft C, Astrup T. Protection against venous thrombosis in an antithrombin-III deficient patient suffering from episodes of arterial thrombosis requiring major surgery. Effects of oral stanozolol in combination with subcutaneous heparin and intravenous AT-III. Am J Clin Pathol 1985; 83 (06) 768-771
  • 131 Winter JH, Fenech A, Bennett B, Douglas AS. Prophylactic antithrombotic therapy with stanozolol in patients with familial antithrombin III deficiency. Br J Haematol 1984; 57 (03) 527-537