Skip to main content
SpringerLink
Log in

The Heart as a Special Muscle in Athletes and Anabolic–Androgenic Steroids (Ab)use

  • Chapter
Nuclear Medicine and Radiologic Imaging in Sports Injuries

  • 2390 Accesses

Abstract

Adaptation of the heart muscle in response to exercise has been extensively described. Different forms of sports may imply a different strain to the heart. In this context endurance sports are considered to induce a dynamic, isotonic workload, which is accompanied by an increase in heart rate and stroke volume and a reduction in peripheral vascular resistance.

Sudden athlete death (SAD) is a widely publicised and increasingly reported phenomenon. For many, the athlete population epitomise human physical endeavour and achievement, and their unexpected death comes with a significant emotional impact on the public.

Anabolic–androgenic steroids (AAS) are abused for enhancing muscle mass, strength growth and improving athletic performance. In recent years many observational and interventional studies have shown important adverse cardiovascular effects of AAS abuse.

Imaging with nuclear medicine with or without combined CT techniques, echocardiography and CMR are promising methods to target and image certain biomarkers in the process of cardiovascular pathology that can be used for early detection of sport- and also AAS-associated adverse effects.

This book chapter discusses the physiological background of myocardial (dys)function in athletes and established and novel nuclear molecular imaging techniques, including MRI, that may serve as potential tools for early detection of sport- and AAS-associated cardiovascular disorders and reducing cardiovascular sudden deaths in athletes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

123I-MIBG:

123I-metaiodobenzylguanidine

AS:

Aortic stenosis

ACS:

Acute coronary syndrome

AT1:

Angiotensin-1

AAS:

Anabolic–androgenic steroids

RGD:

Arginine–glycine–aspartate

ARVC:

Arrhythmogenic right ventricular cardiomyopathy

CO:

Cardiac output

CMR:

Cardiovascular magnetic resonance

CPT:

Cold pressure test

CAD:

Coronary artery disease

CR:

Coronary reserve

CTA:

CT angiography

DHEA:

Dehydroepiandrosterone

ECG:

Electrocardiography

FFR:

Fractional flow reserve

gRE:

Global relative enhancement

HCM:

Hypertrophic cardiomyopathy

HRV:

Heart rate variability

H/M:

Heart/mediastinum

BMIPP:

123I-beta-methyl-iodophenylpentadecanoic acid

IDC:

Idiopathic dilated cardiomyopathy

LGE:

Late gadolinium enhancement

LV:

Left ventricle

LVEF:

Left ventricular ejection fraction

LVH:

Left ventricular hypertrophy

MBF:

Myocardial blood flow

MDCT:

Multi-detector computed tomography

MI:

Myocardial infarction

MUGA:

Multigated acquisition scan

MPI:

Myocardial perfusion imaging

MPR:

Myocardial perfusion reserve

PET:

Positron emission tomography

RAS:

Renin–angiotensin system

RPP:

Rate–pressure product

RV:

Right ventricle

RVEF:

Right ventricular ejection fraction

SPECT:

Single-photon emission computed tomography

SV:

Stroke volume

SAD:

Sudden athlete death

USPIO:

Ultra-small superparamagnetic particles of iron oxide

VCAM-1:

Vascular cell adhesion molecule-1

WR:

Washout rate

References

  • Aaron CP, Tandri H, Barr RG et al (2011) Physical activity and right ventricular structure and function. The MESA-Right Ventricle Study. Am J Respir Crit Care Med 183:396–404

    Article  PubMed Central  PubMed  Google Scholar 

  • Ahlgrim C, Guglin M (2009) Anabolics and cardiomyopathy in a bodybuilder: case report and literature review. J Card Fail 15:496–500

    Article  PubMed  Google Scholar 

  • Ajayi AA, Halushka PV (2005) Castration reduces platelet thromboxane A2 receptor density and aggregability. QJM 98:349–356

    Article  CAS  PubMed  Google Scholar 

  • Ajayi AA, Mathur R, Halushka PV (1995) Testosterone increases human platelet thromboxane A2 receptor density and aggregation responses. Circulation 91:2742–2747

    Article  CAS  PubMed  Google Scholar 

  • Alessio AC, Santos CX, Debbas V et al (2011) Evaluation of mild hyperhomocysteinemia during the development of atherosclerosis in apolipoprotein E-deficient and normal mice. Exp Mol Pathol 90:45–50

    Article  CAS  PubMed  Google Scholar 

  • Alves MJ, Dos Santos MR, Dias RG et al (2010) Abnormal neurovascular control in anabolic androgenic steroids users. Med Sci Sports Exerc 42:865–871

    Article  CAS  PubMed  Google Scholar 

  • Angelilli A, Katz ES, Goldenberg RM (2005) Cardiac arrest following anaesthetic induction in a world-class bodybuilder. Acta Cardiol 60:443–444

    Article  PubMed  Google Scholar 

  • Annovazzi A, Bonanno E, Arca M et al (2006) 99mTc-interleukin-2 scintigraphy for the in vivo imaging of vulnerable atherosclerotic plaques. Eur J Nucl Med Mol Imaging 33:117–126

    Article  CAS  PubMed  Google Scholar 

  • Arrigan MT, Killeen RP, Dodd JD et al (2011) Imaging spectrum of sudden athlete cardiac death. Clin Radiol 66:203–223

    Article  CAS  PubMed  Google Scholar 

  • Baggish AL, Wang F, Weiner RB et al (2008) Training-specific changes in cardiac structure and function: a prospective and longitudinal assessment of competitive athletes. J Appl Physiol 104:1121–1128

    Article  PubMed  Google Scholar 

  • Baggish AL, Weiner RB, Kanayama G et al (2010) Long-term anabolic-androgenic steroid use is associated with left ventricular dysfunction. Circ Heart Fail 3:472–476

    Article  PubMed Central  PubMed  Google Scholar 

  • Bartram P, Toft J, Hanel B et al (1998) False-positive defects in technetium-99m sestamibi myocardial single-photon emission tomography in healthy athletes with left ventricular hypertrophy. Eur J Nucl Med 25:1308–1312

    Article  CAS  PubMed  Google Scholar 

  • Basso C, Thiene G, Corrado D et al (1996) Arrhythmogenic right ventricular cardiomyopathy. Dysplasia, dystrophy, or myocarditis? Circulation 94:983–991

    Article  CAS  PubMed  Google Scholar 

  • Basso C, Corrado D, Marcus FI et al (2009) Arrhythmogenic right ventricular cardiomyopathy. Lancet 373:1289–1300

    Article  PubMed  Google Scholar 

  • Behrendt H, Boffin H (1977) Myocardial cell lesions caused by an anabolic hormone. Cell Tissue Res 181:423–426

    Article  CAS  PubMed  Google Scholar 

  • Belhani D, Fanton L, Vaillant F et al (2009) Cardiac lesions induced by testosterone: protective effects of dexrazoxane and trimetazidine. Cardiovasc Toxicol 9:64–69

    Article  CAS  PubMed  Google Scholar 

  • Bengel FM, Schwaiger M (2004) Assessment of cardiac sympathetic neuronal function using PET imaging. J Nucl Cardiol 11:603–616

    Article  PubMed  Google Scholar 

  • Bengel FM, Higuchi T, Javadi MS et al (2009) Cardiac positron emission tomography. J Am Coll Cardiol 54:1–15

    Article  PubMed  Google Scholar 

  • Beutel A, Bergamaschi CT, Campos RR (2005) Effects of chronic anabolic steroid treatment on tonic and reflex cardiovascular control in male rats. J Steroid Biochem Mol Biol 93:43–48

    Article  CAS  PubMed  Google Scholar 

  • Bissoli NS, Medeiros AR, Santos MC et al (2009) Long-term treatment with supraphysiological doses of nandrolone decanoate reduces the sensitivity of Bezold-Jarisch reflex control of heart rate and blood pressure. Pharmacol Res 59:379–384

    Article  CAS  PubMed  Google Scholar 

  • Bjarnason NH, Bjarnason K, Haarbo J et al (1997) Tibolone: influence on markers of cardiovascular disease. J Clin Endocrinol Metab 82:1752–1756

    Article  CAS  PubMed  Google Scholar 

  • Briley-Saebo KC, Cho YS, Tsimikas S (2011) Imaging of oxidation-specific epitopes in atherosclerosis and macrophage-rich vulnerable plaques. Curr Cardiovasc Imaging Rep 4:4–16

    Article  PubMed Central  PubMed  Google Scholar 

  • Buyukdereli G, Kanadasi M, Kibar M (2005) Washout rates of Tc-99m tetrofosmin in asymmetric septal hypertrophy. Ann Nucl Med 19:29–33

    Article  PubMed  Google Scholar 

  • Calkins H (2008) Arrhythmogenic right ventricular dysplasia. Trans Am Clin Climatol Assoc 119:273–286

    PubMed Central  PubMed  Google Scholar 

  • Cecchi F, Olivotto I, Gistri R et al (2003) Coronary microvascular dysfunction and prognosis in hypertrophic cardiomyopathy. N Engl J Med 349:1027–1035

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Bural GG, Torigian DA et al (2009) Emerging role of FDG-PET/CT in assessing atherosclerosis in large arteries. Eur J Nucl Med Mol Imaging 36:144–151

    Article  PubMed  Google Scholar 

  • Choudhury L, Guzzetti S, Lefroy DC et al (1996a) Myocardial beta adrenoceptors and left ventricular function in hypertrophic cardiomyopathy. Heart 75:50–54

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Choudhury L, Rosen SD, Lefroy DC et al (1996b) Myocardial beta adrenoceptor density in primary and secondary left ventricular hypertrophy. Eur Heart J 17:1703–1709

    Article  CAS  PubMed  Google Scholar 

  • Cooper LT Jr (2009) Myocarditis. N Engl J Med 360:1526–1538

    Article  CAS  PubMed  Google Scholar 

  • Corrado D, Basso C, Schiavon M et al (1998) Screening for hypertrophic cardiomyopathy in young athletes. N Engl J Med 339:364–369

    Article  CAS  PubMed  Google Scholar 

  • Corrado D, Pelliccia A, Bjornstad HH et al (2005) Cardiovascular pre-participation screening of young competitive athletes for prevention of sudden death: proposal for a common European protocol. Consensus Statement of the Study Group of Sport Cardiology of the Working Group of Cardiac Rehabilitation and Exercise Physiology and the Working Group of Myocardial and Pericardial Diseases of the European Society of Cardiology. Eur Heart J 26:516–524

    Article  PubMed  Google Scholar 

  • Corrado D, Basso C, Pavei A et al (2006) Trends in sudden cardiovascular death in young competitive athletes after implementation of a preparticipation screening program. JAMA 296:1593–1601

    Article  CAS  PubMed  Google Scholar 

  • Danad I, Raijmakers PG, Appelman YE et al (2012) Quantitative relationship between coronary artery calcium score and hyperemic myocardial blood flow as assessed by hybrid 15O-water PET/CT imaging in patients evaluated for coronary artery disease. J Nucl Cardiol 19:256–264

    Article  PubMed Central  PubMed  Google Scholar 

  • Danias PG, Ahlberg AW, Clark BA III et al (1998) Combined assessment of myocardial perfusion and left ventricular function with exercise technetium-99m sestamibi gated single-photon emission computed tomography can differentiate between ischemic and nonischemic dilated cardiomyopathy. Am J Cardiol 82:1253–1258

    Article  CAS  PubMed  Google Scholar 

  • de Jong RM, Willemsen AT, Slart RH et al (2005) Myocardial beta-adrenoceptor downregulation in idiopathic dilated cardiomyopathy measured in vivo with PET using the new radioligand (S)-[11C]CGP12388. Eur J Nucl Med Mol Imaging 32:443–447

    Article  PubMed  CAS  Google Scholar 

  • de Vries J, DeJongste MJ, Jessurun GA et al (2006) Myocardial perfusion quantification in patients suspected of cardiac syndrome X with positive and negative exercise testing: a [13N]ammonia positron emission tomography study. Nucl Med Commun 27:791–794

    Article  PubMed  Google Scholar 

  • Dec GW, Palacios I, Yasuda T et al (1990) Antimyosin antibody cardiac imaging: its role in the diagnosis of myocarditis. J Am Coll Cardiol 16:97–104

    Article  CAS  PubMed  Google Scholar 

  • Dilsizian V, Bonow RO, Epstein SE et al (1993) Myocardial ischemia detected by thallium scintigraphy is frequently related to cardiac arrest and syncope in young patients with hypertrophic cardiomyopathy. J Am Coll Cardiol 22:796–804

    Article  CAS  PubMed  Google Scholar 

  • Drezner JA, Ackerman MJ, Anderson J et al (2013) Electrocardiographic interpretation in athletes: the ‘Seattle criteria’. Br J Sports Med 47:122–124

    Article  PubMed  Google Scholar 

  • Ector J, Ganame J, van der Merwe N et al (2007) Reduced right ventricular ejection fraction in endurance athletes presenting with ventricular arrhythmias: a quantitative angiographic assessment. Eur Heart J 28:345–353

    Article  PubMed  Google Scholar 

  • Fanton L, Belhani D, Vaillant F et al (2009) Heart lesions associated with anabolic steroid abuse: comparison of post-mortem findings in athletes and norethandrolone-induced lesions in rabbits. Exp Toxicol Pathol 61:317–323

    Article  CAS  PubMed  Google Scholar 

  • Ferrer M, Encabo A, Marin J et al (1994) Chronic treatment with the anabolic steroid, nandrolone, inhibits vasodilator responses in rabbit aorta. Eur J Pharmacol 252:233–241

    Article  CAS  PubMed  Google Scholar 

  • Fineschi V, Riezzo I, Centini F et al (2007) Sudden cardiac death during anabolic steroid abuse: morphologic and toxicologic findings in two fatal cases of bodybuilders. Int J Legal Med 121:48–53

    Article  PubMed  Google Scholar 

  • Fisker Hag AM, Pedersen SF, Kjaer A (2008) Gene expression of LOX-1, VCAM-1, and ICAM-1 in pre-atherosclerotic mice. Biochem Biophys Res Commun 377:689–693

    Article  CAS  PubMed  Google Scholar 

  • Flotats A, Carrio I, Agostini D et al (2010) Proposal for standardization of 123I-metaiodobenzylguanidine (MIBG) cardiac sympathetic imaging by the EANM Cardiovascular Committee and the European Council of Nuclear Cardiology. Eur J Nucl Med Mol Imaging 37:1802–1812

    Article  PubMed  Google Scholar 

  • Fontana K, Oliveira HC, Leonardo MB et al (2008) Adverse effect of the anabolic-androgenic steroid mesterolone on cardiac remodelling and lipoprotein profile is attenuated by aerobicz exercise training. Int J Exp Pathol 89:358–366

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Freed LA, Levy D, Levine RA et al (1999) Prevalence and clinical outcome of mitral-valve prolapse. N Engl J Med 341:1–7

    Article  CAS  PubMed  Google Scholar 

  • Friedrich MG, Sechtem U, Schulz-Menger J et al (2009) Cardiovascular magnetic resonance in myocarditis: a JACC White Paper. J Am Coll Cardiol 53:1475–1487

    Article  PubMed Central  PubMed  Google Scholar 

  • Gawaz M, Langer H, May AE (2005) Platelets in inflammation and atherogenesis. J Clin Invest 115:3378–3384

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Germano G, Kiat H, Kavanagh PB et al (1995) Automatic quantification of ejection fraction from gated myocardial perfusion SPECT. J Nucl Med 36:2138–2147

    CAS  PubMed  Google Scholar 

  • Ghadri JR, Fiechter M, Veraguth K et al (2012) Coronary calcium score as an adjunct to nuclear myocardial perfusion imaging for risk stratification before noncardiac surgery. J Nucl Med 53:1081–1086

    Article  PubMed  Google Scholar 

  • Gimelli A, Landi P, Marraccini P et al (2008) Left ventricular ejection fraction measurements: accuracy and prognostic implications in a large population of patients with known or suspected ischemic heart disease. Int J Cardiovasc Imaging 24:793–801

    Article  PubMed  Google Scholar 

  • Goldberger JJ, Cain ME, Hohnloser SH et al (2008) American Heart Association/American College of Cardiology Foundation/Heart Rhythm Society Scientific Statement on Noninvasive Risk Stratification Techniques for Identifying Patients at Risk for Sudden Cardiac Death. A scientific statement from the American Heart Association Council on Clinical Cardiology Committee on Electrocardiography and Arrhythmias and Council on Epidemiology and Prevention. J Am Coll Cardiol 52:1179–1199

    Article  PubMed  Google Scholar 

  • Golestani R, Slart RH, Dullaart RP et al (2012) Adverse cardiovascular effects of anabolic steroids: pathophysiology imaging. Eur J Clin Invest 42:795–803

    Article  CAS  PubMed  Google Scholar 

  • Graham MR, Grace FM, Boobier W et al (2006) Homocysteine induced cardiovascular events: a consequence of long term anabolic-androgenic steroid (AAS) abuse. Br J Sports Med 40:644–648

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Grigioni F, Enriquez-Sarano M, Ling LH et al (1999) Sudden death in mitral regurgitation due to flail leaflet. J Am Coll Cardiol 34:2078–2085

    Article  CAS  PubMed  Google Scholar 

  • Gurtner HP, Walser P, Fassler B (1975) Normal values for pulmonary hemodynamics at rest and during exercise in man. Prog Respir Res 9:295–315

    Article  Google Scholar 

  • Hartgens F, Kuipers H (2004) Effects of androgenic-anabolic steroids in athletes. Sports Med 34:513–554

    Article  PubMed  Google Scholar 

  • Hartgens F, Rietjens G, Keizer HA et al (2004) Effects of androgenic-anabolic steroids on apolipoproteins and lipoprotein (a). Br J Sports Med 38:253–259

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hayek E, Gring CN, Griffin BP (2005) Mitral valve prolapse. Lancet 365:507–518

    Article  PubMed  Google Scholar 

  • Hendel RC, Cerqueira M, Douglas PS et al (2010) A multicenter assessment of the use of single-photon emission computed tomography myocardial perfusion imaging with appropriateness criteria. J Am Coll Cardiol 55:156–162

    Article  PubMed  Google Scholar 

  • Ibrahim el-SH (2012) Imaging sequences in cardiovascular magnetic resonance: current role, evolving applications, and technical challenges. Int J Cardiovasc Imaging 28:2027–2047

    Google Scholar 

  • James OG, Christensen JD, Wong TZ et al (2011) Utility of FDG PET/CT in inflammatory cardiovascular disease. Radiographics 31:1271–1286

    Article  PubMed  Google Scholar 

  • John AS, Dill T, Brandt RR et al (2003) Magnetic resonance to assess the aortic valve area in aortic stenosis: how does it compare to current diagnostic standards? J Am Coll Cardiol 42:519–526

    Article  PubMed  Google Scholar 

  • Kajander S, Joutsiniemi E, Saraste M et al (2010) Cardiac positron emission tomography/computed tomography imaging accurately detects anatomically and functionally significant coronary artery disease. Circulation 122:603–613

    Article  CAS  PubMed  Google Scholar 

  • Kapur A, Latus KA, Davies G et al (2002) A comparison of three radionuclide myocardial perfusion tracers in clinical practice: the ROBUST study. Eur J Nucl Med Mol Imaging 29:1608–1616

    Article  CAS  PubMed  Google Scholar 

  • Kaufmann PA, Di Carli MF (2009) Hybrid SPECT/CT and PET/CT imaging: the next step in noninvasive cardiac imaging. Semin Nucl Med 39:341–347

    Article  PubMed  Google Scholar 

  • Kelesidis I, Travin MI (2012) Use of cardiac radionuclide imaging to identify patients at risk for arrhythmic sudden cardiac death. J Nucl Cardiol 19:142–152

    Article  PubMed  Google Scholar 

  • Koh AS, Flores JL, Keng FY et al (2011) Evaluation of the American College of Cardiology Foundation/American Society of Nuclear Cardiology appropriateness criteria for SPECT myocardial perfusion imaging in an Asian tertiary cardiac center. J Nucl Cardiol 18:324–330

    Article  PubMed  Google Scholar 

  • La Gerche A, Heidbuchel H, Burns AT et al (2011) Disproportionate exercise load and remodeling of the athlete’s right ventricle. Med Sci Sports Exerc 43:974–981

    Article  PubMed  Google Scholar 

  • La Gerche A, Burns AT, Mooney DJ et al (2012) Exercise-induced right ventricular dysfunction and structural remodelling in endurance athletes. Eur Heart J 33:998–1006

    Article  PubMed  CAS  Google Scholar 

  • Laaksonen MS, Kalliokoski KK, Luotolahti M et al (2007) Myocardial perfusion during exercise in endurance-trained and untrained humans. Am J Physiol Regul Integr Comp Physiol 293:R837–R843

    Article  CAS  PubMed  Google Scholar 

  • Laitinen I, Saraste A, Weidl E et al (2009) Evaluation of alphavbeta3 integrin-targeted positron emission tomography tracer 18F-galacto-RGD for imaging of vascular inflammation in atherosclerotic mice. Circ Cardiovasc Imaging 2:331–338

    Article  PubMed  Google Scholar 

  • Lane HA, Grace F, Smith JC et al (2006) Impaired vasoreactivity in bodybuilders using androgenic anabolic steroids. Eur J Clin Invest 36:483–488

    Article  CAS  PubMed  Google Scholar 

  • Lefroy DC, de Silva R, Choudhury L et al (1993) Diffuse reduction of myocardial beta-adrenoceptors in hypertrophic cardiomyopathy: a study with positron emission tomography. J Am Coll Cardiol 22:1653–1660

    Article  CAS  PubMed  Google Scholar 

  • Lerch H, Bartenstein P, Wichter T et al (1993) Sympathetic innervation of the left ventricle is impaired in arrhythmogenic right ventricular disease. Eur J Nucl Med 20:207–212

    Article  CAS  PubMed  Google Scholar 

  • Lotze U, Kober A, Kaepplinger S et al (1999) Cardiac sympathetic activity as measured by myocardial 123-I-metaiodobenzylguanidine uptake and heart rate variability in idiopathic dilated cardiomyopathy. Am J Cardiol 83:1548–1551

    Article  CAS  PubMed  Google Scholar 

  • Lotze U, Kaepplinger S, Kober A et al (2001) Recovery of the cardiac adrenergic nervous system after long-term beta-blocker therapy in idiopathic dilated cardiomyopathy: assessment by increase in myocardial 123I-metaiodobenzylguanidine uptake. J Nucl Med 42:49–54

    CAS  PubMed  Google Scholar 

  • Luijkx T, Velthuis BK, Backx FJ et al (2013) Anabolic androgenic steroid use is associated with ventricular dysfunction on cardiac MRI in strength trained athletes. Int J Cardiol 167:664–668

    Article  PubMed  Google Scholar 

  • Magnani JW, Dec GW (2006) Myocarditis: current trends in diagnosis and treatment. Circulation 113:876–890

    Article  PubMed  Google Scholar 

  • Majmudar MD, Nahrendorf M (2012) Cardiovascular molecular imaging: the road ahead. J Nucl Med 53:673–676

    Article  PubMed Central  PubMed  Google Scholar 

  • Margari ZJ, Anastasiou-Nana MI, Terrovitis J et al (2003) Indium-111 monoclonal antimyosin cardiac scintigraphy in suspected acute myocarditis: evolution and diagnostic impact. Int J Cardiol 90:239–245

    Article  PubMed  Google Scholar 

  • Maron BJ (1986) Structural features of the athlete heart as defined by echocardiography. J Am Coll Cardiol 7:190–203

    Article  CAS  PubMed  Google Scholar 

  • Maron BJ (1998) Cardiovascular risks to young persons on the athletic field. Ann Intern Med 129:379–386

    Article  CAS  PubMed  Google Scholar 

  • Maron BJ, Roberts WC, McAllister HA et al (1980) Sudden death in young athletes. Circulation 62:218–229

    Article  CAS  PubMed  Google Scholar 

  • Maron BJ, Pelliccia A, Spirito P (1995) Cardiac disease in young trained athletes. Insights into methods for distinguishing athlete’s heart from structural heart disease, with particular emphasis on hypertrophic cardiomyopathy. Circulation 91:1596–1601

    Article  CAS  PubMed  Google Scholar 

  • Maron BJ, McKenna WJ, Danielson GK et al (2003) American College of Cardiology/European Society of Cardiology clinical expert consensus document on hypertrophic cardiomyopathy. A report of the American College of Cardiology Foundation Task Force on Clinical Expert Consensus Documents and the European Society of Cardiology Committee for Practice Guidelines. J Am Coll Cardiol 42:1687–1713

    Article  PubMed  Google Scholar 

  • Maron BJ, Thompson PD, Ackerman MJ et al (2007) Recommendations and considerations related to preparticipation screening for cardiovascular abnormalities in competitive athletes: 2007 update: a scientific statement from the American Heart Association Council on Nutrition, Physical Activity, and Metabolism: endorsed by the American College of Cardiology Foundation. Circulation 115:1643–455

    Article  PubMed  Google Scholar 

  • Maron BJ, Doerer JJ, Haas TS et al (2009) Sudden deaths in young competitive athletes: analysis of 1866 deaths in the United States, 1980–2006. Circulation 119:1085–1092

    Article  PubMed  Google Scholar 

  • Matsuda K, Ruff A, Morinelli TA et al (1994) Testosterone increases thromboxane A2 receptor density and responsiveness in rat aortas and platelets. Am J Physiol 267:H887–H893

    CAS  PubMed  Google Scholar 

  • Matsuo S, Nakamura Y, Takahashi M et al (2001) Cardiac sympathetic dysfunction in an athlete’s heart detected by 123I-metaiodobenzylguanidine scintigraphy. Jpn Circ J 65:371–374

    Article  CAS  PubMed  Google Scholar 

  • McCrohon JA, Moon JC, Prasad SK et al (2003) Differentiation of heart failure related to dilated cardiomyopathy and coronary artery disease using gadolinium-enhanced cardiovascular magnetic resonance. Circulation 108:54–59

    Article  CAS  PubMed  Google Scholar 

  • Medei E, Marocolo M, Rodrigues DC et al (2010) Chronic treatment with anabolic steroids induces ventricular repolarization disturbances: cellular, ionic and molecular mechanism. J Mol Cell Cardiol 49:165–175

    Article  CAS  PubMed  Google Scholar 

  • Miyagawa M, Anton M, Wagner B et al (2005) Non-invasive imaging of cardiac transgene expression with PET: comparison of the human sodium/iodide symporter gene and HSV1-tk as the reporter gene. Eur J Nucl Med Mol Imaging 32:1108–1114

    Article  PubMed  Google Scholar 

  • Mohiaddin RH, Amanuma M, Kilner PJ et al (1991) MR phase-shift velocity mapping of mitral and pulmonary venous flow. J Comput Assist Tomogr 15:237–243

    Article  CAS  PubMed  Google Scholar 

  • Mudd JO, Kass DA (2008) Tackling heart failure in the twenty-first century. Nature 451:919–928

    Article  CAS  PubMed  Google Scholar 

  • Nagueh SF, Mahmarian JJ (2006) Noninvasive cardiac imaging in patients with hypertrophic cardiomyopathy. J Am Coll Cardiol 48:2410–2422

    Article  PubMed  Google Scholar 

  • Nahrendorf M, Jaffer FA, Kelly KA et al (2006) Noninvasive vascular cell adhesion molecule-1 imaging identifies inflammatory activation of cells in atherosclerosis. Circulation 114:1504–1511

    Article  CAS  PubMed  Google Scholar 

  • Nahrendorf M, Keliher E, Panizzi P et al (2009) 18F-4V for PET/CT imaging of VCAM-1 expression in atherosclerosis. JACC Cardiovasc Imaging 2:1213–1222

    Article  PubMed Central  PubMed  Google Scholar 

  • Nava A, Bauce B, Basso C et al (2000) Clinical profile and long-term follow-up of 37 families with arrhythmogenic right ventricular cardiomyopathy. J Am Coll Cardiol 36:2226–2233

    Article  CAS  PubMed  Google Scholar 

  • Ong PJ, Patrizi G, Chong WC et al (2000) Testosterone enhances flow-mediated brachial artery reactivity in men with coronary artery disease. Am J Cardiol 85:269–272

    Article  CAS  PubMed  Google Scholar 

  • Pelliccia A, Maron BJ, Spataro A et al (1991) The upper limit of physiologic cardiac hypertrophy in highly trained elite athletes. N Engl J Med 324:295–301

    Article  CAS  PubMed  Google Scholar 

  • Pelliccia A, Spataro A, Caselli G et al (1993) Absence of left ventricular wall thickening in athletes engaged in intense power training. Am J Cardiol 72:1048–1054

    Article  CAS  PubMed  Google Scholar 

  • Pelliccia A, Culasso F, Di Paolo FM et al (1999) Physiologic left ventricular cavity dilatation in elite athletes. Ann Intern Med 130:23–31

    Article  CAS  PubMed  Google Scholar 

  • Pereira-Junior PP, Chaves EA, Costa-E-Sousa RH et al (2006) Cardiac autonomic dysfunction in rats chronically treated with anabolic steroid. Eur J Appl Physiol 96:487–494

    Article  CAS  PubMed  Google Scholar 

  • Petersen SE, Selvanayagam JB, Francis JM et al (2005) Differentiation of athlete’s heart from pathological forms of cardiac hypertrophy by means of geometric indices derived from cardiovascular magnetic resonance. J Cardiovasc Magn Reson 7:551–558

    Article  PubMed  Google Scholar 

  • Pinamonti B, Alberti E, Cigalotto A et al (1988) Echocardiographic findings in myocarditis. Am J Cardiol 62:285–291

    Article  CAS  PubMed  Google Scholar 

  • Prakken NH, Velthuis BK, Teske AJ et al (2010) Cardiac MRI reference values for athletes and nonathletes corrected for body surface area, training hours/week and sex. Eur J Cardiovasc Prev Rehabil 17:198–203

    Article  PubMed  Google Scholar 

  • Prakken NH, Cramer MJ, Teske AJ et al (2011) The effect of age in the cardiac MRI evaluation of the athlete’s heart. Int J Cardiol 149:68–73

    Article  PubMed  Google Scholar 

  • Prior DL, La Gerche A (2012) The athlete’s heart. Heart 98:947–955

    Article  PubMed  Google Scholar 

  • Rispler S, Aronson D, Abadi S et al (2011) Integrated SPECT/CT for assessment of haemodynamically significant coronary artery lesions in patients with acute coronary syndrome. Eur J Nucl Med Mol Imaging 38:1917–1925

    Article  PubMed  Google Scholar 

  • Rocha FL, Carmo EC, Roque FR et al (2007) Anabolic steroids induce cardiac renin-angiotensin system and impair the beneficial effects of aerobic training in rats. Am J Physiol Heart Circ Physiol 293:H3575–H3583

    Article  CAS  PubMed  Google Scholar 

  • Rybczynska AA, Elsinga PH, Sijbesma JW et al (2009) Steroid hormones affect binding of the sigma ligand 11C-SA4503 in tumour cells and tumour-bearing rats. Eur J Nucl Med Mol Imaging 36:1167–1175

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sader MA, Griffiths KA, Skilton MR et al (2003) Physiological testosterone replacement and arterial endothelial function in men. Clin Endocrinol (Oxf) 59:62–67

    Article  CAS  Google Scholar 

  • Schafers M, Dutka D, Rhodes CG et al (1998) Myocardial presynaptic and postsynaptic autonomic dysfunction in hypertrophic cardiomyopathy. Circ Res 82:57–62

    Article  CAS  PubMed  Google Scholar 

  • Schattke S, Wagner M, Hattasch R et al (2012) Single beat 3D echocardiography for the assessment of right ventricular dimension and function after endurance exercise: intraindividual comparison with magnetic resonance imaging. Cardiovasc Ultrasound 10:6

    Article  PubMed Central  PubMed  Google Scholar 

  • Schindler TH, Facta AD, Prior JO et al (2006) PET-measured heterogeneity in longitudinal myocardial blood flow in response to sympathetic and pharmacologic stress as a non-invasive probe of epicardial vasomotor dysfunction. Eur J Nucl Med Mol Imaging 33:1140–1149

    Article  PubMed  Google Scholar 

  • Sen-Chowdhry S, Prasad SK, Syrris P et al (2006) Cardiovascular magnetic resonance in arrhythmogenic right ventricular cardiomyopathy revisited: comparison with task force criteria and genotype. J Am Coll Cardiol 48:2132–2140

    Article  PubMed  Google Scholar 

  • Skouri HN, Dec GW, Friedrich MG et al (2006) Noninvasive imaging in myocarditis. J Am Coll Cardiol 48:2085–2093

    Article  PubMed  Google Scholar 

  • Slart RH, Bax JJ, de Jong RM et al (2004) Comparison of gated PET with MRI for evaluation of left ventricular function in patients with coronary artery disease. J Nucl Med 45:176–182

    PubMed  Google Scholar 

  • Slart RH, Bax JJ, De Boer J et al (2005) Comparison of (99m)Tc-sestamibi/(18)FDG DISA SPECT with PET for the detection of viability in patients with coronary artery disease and left ventricular dysfunction. Eur J Nucl Med Mol Imaging 32:972–979

    Article  PubMed  Google Scholar 

  • Slart RH, Bax JJ, van Veldhuisen DJ (2006) Prediction of functional recovery after revascularisation in patients with chronic ischaemic left ventricular dysfunction: head-to-head comparison (99m)Tc-sestamibi/(18)FDG DISA SPECT and (13)N-ammonia/(18)F-FDG PET. Eur J Nucl Med Mol Imaging 33:716–723

    Article  PubMed  Google Scholar 

  • Slart RH, Zeebregts CJ, Hillege HL et al (2011) Myocardial perfusion reserve after a PET-driven revascularization procedure: a strong prognostic factor. J Nucl Med 52:873–879

    Article  PubMed  Google Scholar 

  • Sorensen J, Valind S, Andersson LG (2010) Simultaneous quantification of myocardial perfusion, oxidative metabolism, cardiac efficiency and pump function at rest and during supine bicycle exercise using 1–11C-acetate PET–a pilot study. Clin Physiol Funct Imaging 30:279–284

    Article  PubMed  Google Scholar 

  • Spirito P, Pelliccia A, Proschan MA et al (1994) Morphology of the “athlete’s heart” assessed by echocardiography in 947 elite athletes representing 27 sports. Am J Cardiol 74:802–806

    Article  CAS  PubMed  Google Scholar 

  • Stacy MR, Maxfield MW, Sinusas AJ (2012) Targeted molecular imaging of angiogenesis in PET and SPECT: a review. Yale J Biol Med 85:75–86

    PubMed Central  PubMed  Google Scholar 

  • Stergiopoulos K, Brennan JJ, Mathews R et al (2008) Anabolic steroids, acute myocardial infarction and polycythemia: a case report and review of the literature. Vasc Health Risk Manag 4:1475–1480

    PubMed Central  PubMed  Google Scholar 

  • Tabas I, Williams KJ, Boren J (2007) Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation 116:1832–1844

    Article  CAS  PubMed  Google Scholar 

  • Terai H, Shimizu M, Ino H et al (2003a) Cardiac sympathetic nerve activity in patients with hypertrophic cardiomyopathy with malignant ventricular tachyarrhythmias. J Nucl Cardiol 10:304–310

    Article  PubMed  Google Scholar 

  • Terai H, Shimizu M, Ino H et al (2003b) Changes in cardiac sympathetic nerve innervation and activity in pathophysiologic transition from typical to end-stage hypertrophic cardiomyopathy. J Nucl Med 44:1612–1617

    PubMed  Google Scholar 

  • Thiene G, Basso C (2001) Arrhythmogenic right ventricular cardiomyopathy: an update. Cardiovasc Pathol 10:109–117

    Article  CAS  PubMed  Google Scholar 

  • Tio RA, Dabeshlim A, Siebelink HM et al (2009a) Comparison between the prognostic value of left ventricular function and myocardial perfusion reserve in patients with ischemic heart disease. J Nucl Med 50:214–219

    Article  PubMed  Google Scholar 

  • Tio RA, Slart RH, de Boer RA et al (2009b) Reduced regional myocardial perfusion reserve is associated with impaired contractile performance in idiopathic dilated cardiomyopathy. Neth Heart J 17:470–474

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Toraa M, Pouillard F, Merlet P et al (1999) Cardiac hypertrophy and coronary reserve in endurance athletes. Can J Appl Physiol 24:87–95

    CAS  PubMed  Google Scholar 

  • Towbin JA, Bowles NE (2002) The failing heart. Nature 415:227–233

    Article  CAS  PubMed  Google Scholar 

  • Urhausen A, Albers T, Kindermann W (2004) Are the cardiac effects of anabolic steroid abuse in strength athletes reversible? Heart 90:496–501

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • van Amsterdam J, Opperhuizen A, Hartgens F (2010) Adverse health effects of anabolic-androgenic steroids. Regul Toxicol Pharmacol 57:117–123

    Article  PubMed  CAS  Google Scholar 

  • van den Borne SW, Isobe S, Verjans JW et al (2008) Molecular imaging of interstitial alterations in remodeling myocardium after myocardial infarction. J Am Coll Cardiol 52:2017–2028

    Article  PubMed  CAS  Google Scholar 

  • van der Vleuten PA, Slart RHJA, Tio RA et al (2005) The feasibility of repeated left ventricular ejection fraction analysis with sequential single-dose radionuclide ventriculography. Nucl Med Commun 26:711–715

    Article  PubMed  Google Scholar 

  • Vanhoenacker PK, Heijenbrok-Kal MH, Van HR et al (2007) Diagnostic performance of multidetector CT angiography for assessment of coronary artery disease: meta-analysis. Radiology 244:419–428

    Article  PubMed  Google Scholar 

  • Verjans JW, Lovhaug D, Narula N et al (2008) Noninvasive imaging of angiotensin receptors after myocardial infarction. JACC Cardiovasc Imaging 1:354–362

    Article  PubMed Central  PubMed  Google Scholar 

  • Vriens PW, Blankenberg FG, Stoot JH et al (1998) The use of technetium Tc 99m annexin V for in vivo imaging of apoptosis during cardiac allograft rejection. J Thorac Cardiovasc Surg 116:844–853

    Article  CAS  PubMed  Google Scholar 

  • Whitsel EA, Boyko EJ, Matsumoto AM et al (2001) Intramuscular testosterone esters and plasma lipids in hypogonadal men: a meta-analysis. Am J Med 111:261–269

    Article  CAS  PubMed  Google Scholar 

  • Wilson M, O’Hanlon R, Prasad S et al (2011) Diverse patterns of myocardial fibrosis in lifelong, veteran endurance athletes. J Appl Physiol 110:1622–1626

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wu FC, von Eckardstein A (2003) Androgens and coronary artery disease. Endocr Rev 24:183–217

    Article  CAS  PubMed  Google Scholar 

  • Zaugg M, Jamali NZ, Lucchinetti E et al (2001) Anabolic-androgenic steroids induce apoptotic cell death in adult rat ventricular myocytes. J Cell Physiol 187:90–95

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Xiong Z, Wu Y et al (2006) Quantitative PET imaging of tumor integrin alphavbeta3 expression with 18F-FRGD2. J Nucl Med 47:113–121

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao C, Shuke N, Okizaki A et al (2003) Comparison of myocardial fatty acid metabolism with left ventricular function and perfusion in cardiomyopathies: by 123I-BMIPP SPECT and 99mTc-tetrofosmin electrocardiographically gated SPECT. Ann Nucl Med 17:541–548

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departments of Nuclear Medicine and Molecular Imaging, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands

    Riemer H. J. A. Slart

  2. Division Cardiology, Thorax Center, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands

    René A. Tio & Wybe Nieuwland

Authors
  1. Riemer H. J. A. Slart
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. René A. Tio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wybe Nieuwland
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Riemer H. J. A. Slart .

Editor information

Editors and Affiliations

  1. Department of Nuclear Medicine and Molecular Imaging, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands

    Andor W.J.M. Glaudemans

  2. Department of Nuclear Medicine and Molecular Imaging, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands

    Rudi A.J.O. Dierckx

  3. Department of Radiology, Antwerp University Hospital, Edegem, Belgium

    Jan L.M.A. Gielen

  4. Exercise and Health, Center for Sports Medicine, University Center for Sport, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands

    Johannes (Hans) Zwerver

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Slart, R.H.J.A., Tio, R.A., Nieuwland, W. (2015). The Heart as a Special Muscle in Athletes and Anabolic–Androgenic Steroids (Ab)use. In: Glaudemans, A., Dierckx, R., Gielen, J., Zwerver, J. (eds) Nuclear Medicine and Radiologic Imaging in Sports Injuries. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-46491-5_44

Download citation

  • DOI: https://doi.org/10.1007/978-3-662-46491-5_44

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-662-46490-8

  • Online ISBN: 978-3-662-46491-5

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation