The Spectrum of Coronary Artery Disease in Elite Endurance Athletes—A Long-Standing Debate: State-of-the-Art Review
Abstract
:1. Introduction
2. Materials and Methods
3. Exercise and Coronary Artery Disease, a Long-Standing Paradox
3.1. Benefits of PA and Cardiac Adaptation or “Maladaptation”
3.2. Coronary Artery Disease in Elite Athletes
3.3. Clinical and Prognostic Implications—A Long-Standing Debate
4. Features of Coronary Atherosclerosis in Endurance Athletes
4.1. Mechanisms of Atherosclerotic Progression
4.2. Coronary Artery Calcification and Plaque Characteristics in Athletes
4.3. Factors Impacting on Atherosclerotic Burden and Coronary Calcification
5. Special Subgroups of Coronary Anomalies and Lesions in Elite Athletes
5.1. Coronary Artery Anomalies
5.2. Coronary Artery Dissection
5.3. Myocardial Bridge
6. Management of Athletes with Suspected Coronary Artery Disease
6.1. Evaluation of Athletes at Risk
6.2. Management of Athletes with Coronary Artery Disease
6.3. Gaps in Evidence and Future Directions
7. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Visseren, F.L.J.; Mach, F.; Smulders, Y.M.; Carballo, D.; Koskinas, K.C.; Bäck, M.; Benetos, A.; Biffi, A.; Boavida, J.-M.; Capodanno, D.; et al. 2021 ESC Guidelines on Cardiovascular Disease Prevention in Clinical Practice. Eur. Heart J. 2021, 42, 3227–3337. [Google Scholar] [CrossRef]
- Lee, D.; Pate, R.R.; Lavie, C.J.; Sui, X.; Church, T.S.; Blair, S.N. Leisure-Time Running Reduces All-Cause and Cardiovascular Mortality Risk. J. Am. Coll. Cardiol. 2014, 64, 472–481. [Google Scholar] [CrossRef]
- Schnohr, P.; O’Keefe, J.H.; Marott, J.L.; Lange, P.; Jensen, G.B. Dose of Jogging and Long-Term Mortality. J. Am. Coll. Cardiol. 2015, 65, 411–419. [Google Scholar] [CrossRef] [PubMed]
- Tso, J.; Kim, J.H. Master Endurance Athletes and Cardiovascular Controversies. Curr. Sports Med. Rep. 2020, 19, 113–118. [Google Scholar] [CrossRef] [PubMed]
- Marijon, E.; Tafflet, M.; Celermajer, D.S.; Dumas, F.; Perier, M.-C.; Mustafic, H.; Toussaint, J.-F.; Desnos, M.; Rieu, M.; Benameur, N.; et al. Sports-Related Sudden Death in the General Population. Circulation 2011, 124, 672–681. [Google Scholar] [CrossRef]
- Bohm, P.; Scharhag, J.; Meyer, T. Data from a Nationwide Registry on Sports-Related Sudden Cardiac Deaths in Germany. Eur. J. Prev. Cardiol. 2016, 23, 649–656. [Google Scholar] [CrossRef]
- Arnson, Y.; Rozanski, A.; Gransar, H.; Hayes, S.W.; Friedman, J.D.; Thomson, L.E.J.; Berman, D.S. Impact of Exercise on the Relationship between CAC Scores and All-Cause Mortality. JACC Cardiovasc. Imaging 2017, 10, 1461–1468. [Google Scholar] [CrossRef]
- Mori, H.; Torii, S.; Kutyna, M.; Sakamoto, A.; Finn, A.V.; Virmani, R. Coronary Artery Calcification and Its Progression. JACC Cardiovasc. Imaging 2018, 11, 127–142. [Google Scholar] [CrossRef]
- Merghani, A.; Maestrini, V.; Rosmini, S.; Cox, A.T.; Dhutia, H.; Bastiaenan, R.; David, S.; Yeo, T.J.; Narain, R.; Malhotra, A.; et al. Prevalence of Subclinical Coronary Artery Disease in Masters Endurance Athletes with a Low Atherosclerotic Risk Profile. Circulation 2017, 136, 126–137. [Google Scholar] [CrossRef]
- Mohlenkamp, S.; Lehmann, N.; Breuckmann, F.; Brocker-Preuss, M.; Nassenstein, K.; Halle, M.; Budde, T.; Mann, K.; Barkhausen, J.; Heusch, G.; et al. Running: The Risk of Coronary Events: Prevalence and Prognostic Relevance of Coronary Atherosclerosis in Marathon Runners. Eur. Heart J. 2008, 29, 1903–1910. [Google Scholar] [CrossRef] [PubMed]
- Aengevaeren, V.L.; Mosterd, A.; Braber, T.L.; Prakken, N.H.J.; Doevendans, P.A.; Grobbee, D.E.; Thompson, P.D.; Eijsvogels, T.M.H.; Velthuis, B.K. Relationship between Lifelong Exercise Volume and Coronary Atherosclerosis in Athletes. Circulation 2017, 136, 138–148. [Google Scholar] [CrossRef]
- Radford, N.B.; DeFina, L.F.; Leonard, D.; Barlow, C.E.; Willis, B.L.; Gibbons, L.W.; Gilchrist, S.C.; Khera, A.; Levine, B.D. Cardiorespiratory Fitness, Coronary Artery Calcium, and Cardiovascular Disease Events in a Cohort of Generally Healthy Middle-Age Men: Results from the Cooper Center Longitudinal Study. Circulation 2018, 137, 1888–1895. [Google Scholar] [CrossRef]
- DeFina, L.F.; Radford, N.B.; Barlow, C.E.; Willis, B.L.; Leonard, D.; Haskell, W.L.; Farrell, S.W.; Pavlovic, A.; Abel, K.; Berry, J.D.; et al. Association of All-Cause and Cardiovascular Mortality with High Levels of Physical Activity and Concurrent Coronary Artery Calcification. JAMA Cardiol. 2019, 4, 174. [Google Scholar] [CrossRef] [PubMed]
- Wen, C.P.; Wai, J.P.M.; Tsai, M.K.; Yang, Y.C.; Cheng, T.Y.D.; Lee, M.-C.; Chan, H.T.; Tsao, C.K.; Tsai, S.P.; Wu, X. Minimum Amount of Physical Activity for Reduced Mortality and Extended Life Expectancy: A Prospective Cohort Study. Lancet 2011, 378, 1244–1253. [Google Scholar] [CrossRef] [PubMed]
- Benjamin, E.J.; Virani, S.S.; Callaway, C.W.; Chamberlain, A.M.; Chang, A.R.; Cheng, S.; Chiuve, S.E.; Cushman, M.; Delling, F.N.; Deo, R.; et al. Heart Disease and Stroke Statistics—2018 Update: A Report from the American Heart Association. Circulation 2018, 137, 12. [Google Scholar] [CrossRef]
- Pelliccia, A.; Sharma, S.; Gati, S.; Bäck, M.; Börjesson, M.; Caselli, S.; Collet, J.-P.; Corrado, D.; Drezner, J.A.; Halle, M.; et al. 2020 ESC Guidelines on Sports Cardiology and Exercise in Patients with Cardiovascular Disease. Eur. Heart J. 2021, 42, 17–96. [Google Scholar] [CrossRef] [PubMed]
- Lavie, C.J.; Arena, R.; Swift, D.L.; Johannsen, N.M.; Sui, X.; Lee, D.; Earnest, C.P.; Church, T.S.; O’Keefe, J.H.; Milani, R.V.; et al. Exercise and the Cardiovascular System: Clinical Science and Cardiovascular Outcomes. Circ. Res. 2015, 117, 207–219. [Google Scholar] [CrossRef] [PubMed]
- Pagan, L.U.; Gomes, M.J.; Okoshi, M.P. Endothelial Function and Physical Exercise. Arq. Bras. Cardiol. 2018, 111, 540–541. [Google Scholar] [CrossRef]
- Di Francescomarino, S.; Sciartilli, A.; Di Valerio, V.; Di Baldassarre, A.; Gallina, S. The Effect of Physical Exercise on Endothelial Function. Sports Med. 2009, 39, 797–812. [Google Scholar] [CrossRef] [PubMed]
- Clarke, P.M.; Walter, S.J.; Hayen, A.; Mallon, W.J.; Heijmans, J.; Studdert, D.M. Survival of the Fittest: Retrospective Cohort Study of the Longevity of Olympic Medallists in the Modern Era. BMJ 2012, 345, e8308. [Google Scholar] [CrossRef]
- Arbab-Zadeh, A.; Perhonen, M.; Howden, E.; Peshock, R.M.; Zhang, R.; Adams-Huet, B.; Haykowsky, M.J.; Levine, B.D. Cardiac Remodeling in Response to 1 Year of Intensive Endurance Training. Circulation 2014, 130, 2152–2161. [Google Scholar] [CrossRef]
- Bhella, P.S.; Hastings, J.L.; Fujimoto, N.; Shibata, S.; Carrick-Ranson, G.; Palmer, M.D.; Boyd, K.N.; Adams-Huet, B.; Levine, B.D. Impact of Lifelong Exercise “Dose” on Left Ventricular Compliance and Distensibility. J. Am. Coll. Cardiol. 2014, 64, 1257–1266. [Google Scholar] [CrossRef] [PubMed]
- Niebauer, J.; Börjesson, M.; Carre, F.; Caselli, S.; Palatini, P.; Quattrini, F.; Serratosa, L.; Adami, P.E.; Biffi, A.; Pressler, A.; et al. Recommendations for Participation in Competitive Sports of Athletes with Arterial Hypertension: A Position Statement from the Sports Cardiology Section of the European Association of Preventive Cardiology (EAPC). Eur. Heart J. 2018, 39, 3664–3671. [Google Scholar] [CrossRef]
- Levine, B.D.; Baggish, A.L.; Kovacs, R.J.; Link, M.S.; Maron, M.S.; Mitchell, J.H. Eligibility and Disqualification Recommendations for Competitive Athletes with Cardiovascular Abnormalities: Task Force 1: Classification of Sports: Dynamic, Static, and Impact. J. Am. Coll. Cardiol. 2015, 66, 2350–2355. [Google Scholar] [CrossRef] [PubMed]
- Vella, C.A.; Robergs, R.A. A Review of the Stroke Volume Response to Upright Exercise in Healthy Subjects. Br. J. Sports Med. 2005, 39, 190–195. [Google Scholar] [CrossRef]
- Jones, A.M.; Vanhatalo, A. The ‘Critical Power’ Concept: Applications to Sports Performance with a Focus on Intermittent High-Intensity Exercise. Sports Med. 2017, 47 (Suppl. S1), 65–78. [Google Scholar] [CrossRef]
- Gerche, A.L.; Heidbuchel, H. Can Intensive Exercise Harm the Heart?: You Can Get Too Much of a Good Thing. Circulation 2014, 130, 992–1002. [Google Scholar] [CrossRef]
- O’Keefe, E.L.; Torres-Acosta, N.; O’Keefe, J.H.; Lavie, C.J. Training for Longevity: The Reverse J-Curve for Exercise. Mo. Med. 2020, 117, 355–361. [Google Scholar] [PubMed]
- Graziano, F.; Juhasz, V.; Brunetti, G.; Cipriani, A.; Szabo, L.; Merkely, B.; Corrado, D.; D’Ascenzi, F.; Vago, H.; Zorzi, A. May Strenuous Endurance Sports Activity Damage the Cardiovascular System of Healthy Athletes? A Narrative Review. J. Cardiovasc. Dev. Dis. 2022, 9, 347. [Google Scholar] [CrossRef]
- Franklin, B.A.; Thompson, P.D.; Al-Zaiti, S.S.; Albert, C.M.; Hivert, M.-F.; Levine, B.D.; Lobelo, F.; Madan, K.; Sharrief, A.Z.; Eijsvogels, T.M.H.; et al. Exercise-Related Acute Cardiovascular Events and Potential Deleterious Adaptations Following Long-Term Exercise Training: Placing the Risks Into Perspective—An Update: A Scientific Statement from the American Heart Association. Circulation 2020, 141. [Google Scholar] [CrossRef]
- Chugh, S.S.; Weiss, J.B. Sudden Cardiac Death in the Older Athlete. J. Am. Coll. Cardiol. 2015, 65, 493–502. [Google Scholar] [CrossRef] [PubMed]
- Van Rosendael, A.R.; De Graaf, M.A.; Scholte, A.J. Cardiac Arrest during Vigorous Exercise: Coronary Plaque Rupture or Myocardial Ischaemia? Neth. Heart J. 2015, 23, 130–132. [Google Scholar] [CrossRef]
- Braber, T.L.; Mosterd, A.; Prakken, N.H.; Rienks, R.; Nathoe, H.M.; Mali, W.P.; Doevendans, P.A.; Backx, F.J.; Bots, M.L.; Grobbee, D.E.; et al. Occult Coronary Artery Disease in Middle-Aged Sportsmen with a Low Cardiovascular Risk Score: The Measuring Athlete’s Risk of Cardiovascular Events (MARC) Study. Eur. J. Prev. Cardiol. 2016, 23, 1677–1684. [Google Scholar] [CrossRef]
- Tsiflikas, I.; Thomas, C.; Fallmann, C.; Schabel, C.; Mangold, S.; Ketelsen, D.; Claussen, C.; Axmann, D.; Schroeder, S.; Burgstahler, C. Prevalence of Subclinical Coronary Artery Disease in Middle-Aged, Male Marathon Runners Detected by Cardiac CT. RöFo-Fortschritte Auf Dem Geb. Röntgenstrahlen Bildgeb. Verfahr. 2015, 187, 561–568. [Google Scholar] [CrossRef]
- Shapero, K.; Deluca, J.; Contursi, M.; Wasfy, M.; Weiner, R.B.; Lewis, G.D.; Hutter, A.; Baggish, A.L. Cardiovascular Risk and Disease Among Masters Endurance Athletes: Insights from the Boston MASTER (Masters Athletes Survey To Evaluate Risk) Initiative. Sports Med.-Open 2016, 2, 29. [Google Scholar] [CrossRef] [PubMed]
- Hou, Z.; Lu, B.; Gao, Y.; Jiang, S.; Wang, Y.; Li, W.; Budoff, M.J. Prognostic Value of Coronary CT Angiography and Calcium Score for Major Adverse Cardiac Events in Outpatients. JACC Cardiovasc. Imaging 2012, 5, 990–999. [Google Scholar] [CrossRef]
- Peng, A.W.; Mirbolouk, M.; Orimoloye, O.A.; Osei, A.D.; Dardari, Z.; Dzaye, O.; Budoff, M.J.; Shaw, L.; Miedema, M.D.; Rumberger, J.; et al. Long-Term All-Cause and Cause-Specific Mortality in Asymptomatic Patients with CAC ≥1000. JACC Cardiovasc. Imaging 2020, 13, 83–93. [Google Scholar] [CrossRef]
- Delaney, J.A.C.; Jensky, N.E.; Criqui, M.H.; Whitt-Glover, M.C.; Lima, J.A.C.; Allison, M.A. The Association between Physical Activity and Both Incident Coronary Artery Calcification and Ankle Brachial Index Progression: The Multi-Ethnic Study of Atherosclerosis. Atherosclerosis 2013, 230, 278–283. [Google Scholar] [CrossRef]
- Gao, J.-W.; Hao, Q.-Y.; Lu, L.-Y.; Han, J.-J.; Huang, F.-F.; Vuitton, D.A.; Wang, J.-F.; Zhang, S.-L.; Liu, P.-M. Associations of Long-Term Physical Activity Trajectories with Coronary Artery Calcium Progression and Cardiovascular Disease Events: Results from the CARDIA Study. Br. J. Sports Med. 2022, 56, 854–861. [Google Scholar] [CrossRef]
- German, C.A.; Fanning, J.; Singleton, M.J.; Shapiro, M.D.; Brubaker, P.H.; Bertoni, A.G.; Yeboah, J. Physical Activity, Coronary Artery Calcium, and Cardiovascular Outcomes in the Multi-Ethnic Study of Atherosclerosis (MESA). Med. Sci. Sports Exerc. 2022, 54, 800–806. [Google Scholar] [CrossRef]
- De Bosscher, R.; Dausin, C.; Claus, P.; Bogaert, J.; Dymarkowski, S.; Goetschalckx, K.; Ghekiere, O.; Van De Heyning, C.M.; Van Herck, P.; Paelinck, B.; et al. Lifelong Endurance Exercise and Its Relation with Coronary Atherosclerosis. Eur. Heart J. 2023, 44, 2388–2399. [Google Scholar] [CrossRef]
- Puchner, S.B.; Liu, T.; Mayrhofer, T.; Truong, Q.A.; Lee, H.; Fleg, J.L.; Nagurney, J.T.; Udelson, J.E.; Hoffmann, U.; Ferencik, M. High-Risk Plaque Detected on Coronary CT Angiography Predicts Acute Coronary Syndromes Independent of Significant Stenosis in Acute Chest Pain. J. Am. Coll. Cardiol. 2014, 64, 684–692. [Google Scholar] [CrossRef] [PubMed]
- Min, J.K.; Shaw, L.J.; Devereux, R.B.; Okin, P.M.; Weinsaft, J.W.; Russo, D.J.; Lippolis, N.J.; Berman, D.S.; Callister, T.Q. Prognostic Value of Multidetector Coronary Computed Tomographic Angiography for Prediction of All-Cause Mortality. J. Am. Coll. Cardiol. 2007, 50, 1161–1170. [Google Scholar] [CrossRef] [PubMed]
- Chiu, J.-J.; Chien, S. Effects of Disturbed Flow on Vascular Endothelium: Pathophysiological Basis and Clinical Perspectives. Physiol. Rev. 2011, 91, 327–387. [Google Scholar] [CrossRef]
- Wang, Y.-X.; Liu, H.-B.; Li, P.-S.; Yuan, W.-X.; Liu, B.; Liu, S.-T.; Qin, K.-R. ROS and NO Dynamics in Endothelial Cells Exposed to Exercise-Induced Wall Shear Stress. Cell. Mol. Bioeng. 2019, 12, 107–120. [Google Scholar] [CrossRef]
- Lavie, C.J.; Hecht, H.F.; Wisloff, U. Extreme Physical Activity May Increase Coronary Calcification, But Fitness Still Prevails. Mayo Clin. Proc. Innov. Qual. Outcomes 2019, 3, 103–105. [Google Scholar] [CrossRef]
- Puri, R.; Nicholls, S.J.; Shao, M.; Kataoka, Y.; Uno, K.; Kapadia, S.R.; Tuzcu, E.M.; Nissen, S.E. Impact of Statins on Serial Coronary Calcification during Atheroma Progression and Regression. J. Am. Coll. Cardiol. 2015, 65, 1273–1282. [Google Scholar] [CrossRef]
- Lin, J.; DeLuca, J.R.; Lu, M.T.; Ruehm, S.G.; Dudum, R.; Choi, B.; Lieberman, D.E.; Hoffman, U.; Baggish, A.L. Extreme Endurance Exercise and Progressive Coronary Artery Disease. J. Am. Coll. Cardiol. 2017, 70, 293–295. [Google Scholar] [CrossRef] [PubMed]
- Heusch, G.; Schulz, R.; Baumgart, D.; Haude, M.; Erbel, R. Coronary Microembolization. Prog. Cardiovasc. Dis. 2001, 44, 217–230. [Google Scholar] [CrossRef]
- Franck, G.; Even, G.; Gautier, A.; Salinas, M.; Loste, A.; Procopio, E.; Gaston, A.-T.; Morvan, M.; Dupont, S.; Deschildre, C.; et al. Haemodynamic Stress-Induced Breaches of the Arterial Intima Trigger Inflammation and Drive Atherogenesis. Eur. Heart J. 2019, 40, 928–937. [Google Scholar] [CrossRef]
- Gardinier, J.D.; Mohamed, F.; Kohn, D.H. PTH Signaling during Exercise Contributes to Bone Adaptation. J. Bone Miner. Res. 2015, 30, 1053–1063. [Google Scholar] [CrossRef]
- Bouassida, A.; Latiri, I.; Bouassida, S.; Zalleg, D.; Zaouali, M.; Feki, Y.; Gharbi, N.; Zbidi, A.; Tabka, Z. Parathyroid Hormone and Physical Exercise: A Brief Review. J. Sports Sci. Med. 2006, 5, 367–374. [Google Scholar] [PubMed]
- Raggi, P.; Genest, J.; Giles, J.T.; Rayner, K.J.; Dwivedi, G.; Beanlands, R.S.; Gupta, M. Role of Inflammation in the Pathogenesis of Atherosclerosis and Therapeutic Interventions. Atherosclerosis 2018, 276, 98–108. [Google Scholar] [CrossRef] [PubMed]
- Mody, N. Oxidative Stress Modulates Osteoblastic Differentiation of Vascular and Bone Cells. Free Radic. Biol. Med. 2001, 31, 509–519. [Google Scholar] [CrossRef]
- Kojda, G.; Hambrecht, R. Molecular Mechanisms of Vascular Adaptations to Exercise. Physical Activity as an Effective Antioxidant Therapy? Cardiovasc. Res. 2005, 67, 187–197. [Google Scholar] [CrossRef]
- Zhu, D.; Hadoke, P.W.F.; Wu, J.; Vesey, A.T.; Lerman, D.A.; Dweck, M.R.; Newby, D.E.; Smith, L.B.; MacRae, V.E. Ablation of the Androgen Receptor from Vascular Smooth Muscle Cells Demonstrates a Role for Testosterone in Vascular Calcification. Sci. Rep. 2016, 6, 24807. [Google Scholar] [CrossRef] [PubMed]
- Criqui, M.H.; Denenberg, J.O.; Ix, J.H.; McClelland, R.L.; Wassel, C.L.; Rifkin, D.E.; Carr, J.J.; Budoff, M.J.; Allison, M.A. Calcium Density of Coronary Artery Plaque and Risk of Incident Cardiovascular Events. JAMA 2014, 311, 271–278. [Google Scholar] [CrossRef] [PubMed]
- Pontone, G.; Rossi, A.; Guglielmo, M.; Dweck, M.R.; Gaemperli, O.; Nieman, K.; Pugliese, F.; Maurovich-Horvat, P.; Gimelli, A.; Cosyns, B.; et al. Clinical Applications of Cardiac Computed Tomography: A Consensus Paper of the European Association of Cardiovascular Imaging—Part I. Eur. Heart J.-Cardiovasc. Imaging 2022, 23, 299–314. [Google Scholar] [CrossRef]
- Agatston, A.S.; Janowitz, W.R.; Hildner, F.J.; Zusmer, N.R.; Viamonte, M.; Detrano, R. Quantification of Coronary Artery Calcium Using Ultrafast Computed Tomography. J. Am. Coll. Cardiol. 1990, 15, 827–832. [Google Scholar] [CrossRef]
- Sandfort, V.; Bluemke, D.A. CT Calcium Scoring. History, Current Status and Outlook. Diagn. Interv. Imaging 2017, 98, 3–10. [Google Scholar] [CrossRef]
- Perrone-Filardi, P.; Achenbach, S.; Mohlenkamp, S.; Reiner, Z.; Sambuceti, G.; Schuijf, J.D.; Van Der Wall, E.; Kaufmann, P.A.; Knuuti, J.; Schroeder, S.; et al. Cardiac Computed Tomography and Myocardial Perfusion Scintigraphy for Risk Stratification in Asymptomatic Individuals without Known Cardiovascular Disease: A Position Statement of the Working Group on Nuclear Cardiology and Cardiac CT of the European Society of Cardiology. Eur. Heart J. 2011, 32, 1986–1993. [Google Scholar] [CrossRef] [PubMed]
- Elias-Smale, S.E.; Proença, R.V.; Koller, M.T.; Kavousi, M.; Van Rooij, F.J.A.; Hunink, M.G.; Steyerberg, E.W.; Hofman, A.; Oudkerk, M.; Witteman, J.C.M. Coronary Calcium Score Improves Classification of Coronary Heart Disease Risk in the Elderly. J. Am. Coll. Cardiol. 2010, 56, 1407–1414. [Google Scholar] [CrossRef] [PubMed]
- Erbel, R.; Möhlenkamp, S.; Moebus, S.; Schmermund, A.; Lehmann, N.; Stang, A.; Dragano, N.; Grönemeyer, D.; Seibel, R.; Kälsch, H.; et al. Coronary Risk Stratification, Discrimination, and Reclassification Improvement Based on Quantification of Subclinical Coronary Atherosclerosis. J. Am. Coll. Cardiol. 2010, 56, 1397–1406. [Google Scholar] [CrossRef] [PubMed]
- McClelland, R.L.; Jorgensen, N.W.; Budoff, M.; Blaha, M.J.; Post, W.S.; Kronmal, R.A.; Bild, D.E.; Shea, S.; Liu, K.; Watson, K.E.; et al. 10-Year Coronary Heart Disease Risk Prediction Using Coronary Artery Calcium and Traditional Risk Factors. J. Am. Coll. Cardiol. 2015, 66, 1643–1653. [Google Scholar] [CrossRef] [PubMed]
- Demer, L.L.; Tintut, Y. Vascular Calcification: Pathobiology of a Multifaceted Disease. Circulation 2008, 117, 2938–2948. [Google Scholar] [CrossRef]
- Hoshino, T.; Chow, L.A.; Hsu, J.J.; Perlowski, A.A.; Abedin, M.; Tobis, J.; Tintut, Y.; Mal, A.K.; Klug, W.S.; Demer, L.L. Mechanical Stress Analysis of a Rigid Inclusion in Distensible Material: A Model of Atherosclerotic Calcification and Plaque Vulnerability. Am. J. Physiol.-Heart Circ. Physiol. 2009, 297, H802–H810. [Google Scholar] [CrossRef]
- Hsu, J.J.; Lim, J.; Tintut, Y.; Demer, L.L. Cell-Matrix Mechanics and Pattern Formation in Inflammatory Cardiovascular Calcification. Heart 2016, 102, 1710–1715. [Google Scholar] [CrossRef]
- Bernardini, F.; Gelfusa, M.; Celeski, M.; Coletti, F.; Nusca, A.; De Stefano, D.; Piccirillo, F.; Mangiacapra, F.; Gallo, P.; Cammalleri, V.; et al. Beyond the Calcium Score: What Additional Information from a CT Scan Can Assist in Cardiovascular Risk Assessment? Appl. Sci. 2022, 13, 241. [Google Scholar] [CrossRef]
- Roberts, W.O.; Schwartz, R.S.; Kraus, S.M.; Schwartz, J.G.; Peichel, G.; Garberich, R.F.; Lesser, J.R.; Oesterle, S.N.; Wickstrom, K.K.; Knickelbine, T.; et al. Long-Term Marathon Running Is Associated with Low Coronary Plaque Formation in Women. Med. Sci. Sports Exerc. 2017, 49, 641–645. [Google Scholar] [CrossRef]
- Aengevaeren, V.L.; Mosterd, A.; Sharma, S.; Braber, T.L.; Thompson, P.D.; Velthuis, B.K.; Eijsvogels, T.M.H. Coronary Atherosclerosis in Athletes. JACC Cardiovasc. Imaging 2019, 12, 1587–1589. [Google Scholar] [CrossRef]
- McClelland, R.L.; Chung, H.; Detrano, R.; Post, W.; Kronmal, R.A. Distribution of Coronary Artery Calcium by Race, Gender, and Age: Results from the Multi-Ethnic Study of Atherosclerosis (MESA). Circulation 2006, 113, 30–37. [Google Scholar] [CrossRef] [PubMed]
- Laddu, D.R.; Rana, J.S.; Murillo, R.; Sorel, M.E.; Quesenberry, C.P.; Allen, N.B.; Gabriel, K.P.; Carnethon, M.R.; Liu, K.; Reis, J.P.; et al. 25-Year Physical Activity Trajectories and Development of Subclinical Coronary Artery Disease as Measured by Coronary Artery Calcium: The Coronary Artery Risk Development in Young Adults (CARDIA) Study. Mayo Clin. Proc. 2017, 92, 1660–1670. [Google Scholar] [CrossRef] [PubMed]
- Peñalver, J.M.; Mosca, R.S.; Weitz, D.; Phoon, C.K. Anomalous Aortic Origin of Coronary Arteries from the Opposite Sinus: A Critical Appraisal of Risk. BMC Cardiovasc. Disord. 2012, 12, 83. [Google Scholar] [CrossRef] [PubMed]
- Gowd, B.; Thompson, P. Isolated Myocardial Bridging and Exercise-Related Cardiac Events. Int. J. Sports Med. 2014, 35, 1145–1150. [Google Scholar] [CrossRef] [PubMed]
- Kalaga, R.V.; Malik, A.; Thompson, P.D. Exercise-Related Spontaneous Coronary Artery Dissection: Case Report and Literature Review. Med. Sci. Sports Exerc. 2007, 39, 1218–1220. [Google Scholar] [CrossRef]
- Hill, S.F.; Sheppard, M.N. A Silent Cause of Sudden Cardiac Death Especially in Sport: Congenital Coronary Artery Anomalies. Br. J. Sports Med. 2014, 48, 1151–1156. [Google Scholar] [CrossRef]
- Basso, C.; Maron, B.J.; Corrado, D.; Thiene, G. Clinical Profile of Congenital Coronary Artery Anomalies with Origin from the Wrong Aortic Sinus Leading to Sudden Death in Young Competitive Athletes. J. Am. Coll. Cardiol. 2000, 35, 1493–1501. [Google Scholar] [CrossRef]
- Zeppilli, P.; Bianco, M.; Gervasi, S.F.; Cammarano, M.; Monti, R.; Sollazzo, F.; Modica, G.; Morra, L.; Nifosì, F.M.; Palmieri, V. Congenital Coronary Artery Anomalies in Sports Medicine. Why to Know Them. Clin. Cardiol. 2023, 46, 1038–1048. [Google Scholar] [CrossRef]
- Pelliccia, A.; Spataro, A.; Maron, B.J. Prospective Echocardiographic Screening for Coronary Artery Anomalies in 1,360 Elite Competitive Athletes. Am. J. Cardiol. 1993, 72, 978–979. [Google Scholar] [CrossRef]
- Cantinotti, M.; Giordano, R.; Assanta, N.; Koestenberger, M.; Franchi, E.; Marchese, P.; Clemente, A.; Kutty, S.; D’Ascenzi, F. Echocardiographic Screening of Anomalous Origin of Coronary Arteries in Athletes with a Focus on High Take-Off. Healthcare 2021, 9, 231. [Google Scholar] [CrossRef]
- Borjesson, M.; Dellborg, M.; Niebauer, J.; LaGerche, A.; Schmied, C.; Solberg, E.E.; Halle, M.; Adami, E.; Biffi, A.; Carré, F.; et al. Recommendations for Participation in Leisure Time or Competitive Sports in Athletes-Patients with Coronary Artery Disease: A Position Statement from the Sports Cardiology Section of the European Association of Preventive Cardiology (EAPC). Eur. Heart J. 2019, 40, 13–18. [Google Scholar] [CrossRef]
- Van Hare, G.F.; Ackerman, M.J.; Evangelista, J.K.; Kovacs, R.J.; Myerburg, R.J.; Shafer, K.M.; Warnes, C.A.; Washington, R.L. Eligibility and Disqualification Recommendations for Competitive Athletes with Cardiovascular Abnormalities: Task Force 4: Congenital Heart Disease: A Scientific Statement from the American Heart Association and American College of Cardiology. Circulation 2015, 132, e281–e291. [Google Scholar] [CrossRef] [PubMed]
- Hayes, S.N.; Tweet, M.S.; Adlam, D.; Kim, E.S.H.; Gulati, R.; Price, J.E.; Rose, C.H. Spontaneous Coronary Artery Dissection. J. Am. Coll. Cardiol. 2020, 76, 961–984. [Google Scholar] [CrossRef]
- Kaddoura, R.; Cader, F.A.; Ahmed, A.; Alasnag, M. Spontaneous Coronary Artery Dissection: An Overview. Postgrad. Med. J. 2023, 99, 1226–1236. [Google Scholar] [CrossRef]
- Tweet, M.S.; Hayes, S.N.; Pitta, S.R.; Simari, R.D.; Lerman, A.; Lennon, R.J.; Gersh, B.J.; Khambatta, S.; Best, P.J.M.; Rihal, C.S.; et al. Clinical Features, Management, and Prognosis of Spontaneous Coronary Artery Dissection. Circulation 2012, 126, 579–588. [Google Scholar] [CrossRef]
- Adlam, D.; Tweet, M.S.; Gulati, R.; Kotecha, D.; Rao, P.; Moss, A.J.; Hayes, S.N. Spontaneous Coronary Artery Dissection. JACC Cardiovasc. Interv. 2021, 14, 1743–1756. [Google Scholar] [CrossRef]
- Thompson, P.D.; Myerburg, R.J.; Levine, B.D.; Udelson, J.E.; Kovacs, R.J. Eligibility and Disqualification Recommendations for Competitive Athletes with Cardiovascular Abnormalities: Task Force 8: Coronary Artery Disease. J. Am. Coll. Cardiol. 2015, 66, 2406–2411. [Google Scholar] [CrossRef]
- Sternheim, D.; Power, D.A.; Samtani, R.; Kini, A.; Fuster, V.; Sharma, S. Myocardial Bridging: Diagnosis, Functional Assessment, and Management. J. Am. Coll. Cardiol. 2021, 78, 2196–2212. [Google Scholar] [CrossRef]
- Tarantini, G.; Migliore, F.; Cademartiri, F.; Fraccaro, C.; Iliceto, S. Left Anterior Descending Artery Myocardial Bridging. J. Am. Coll. Cardiol. 2016, 68, 2887–2899. [Google Scholar] [CrossRef] [PubMed]
- Lee, M.S.; Chen, C.-H. Myocardial Bridging: An Up-to-Date Review. J. Invasive Cardiol. 2015, 27, 521–528. [Google Scholar] [PubMed]
- Morrison, B.N.; McKinney, J.; Isserow, S.; Lithwick, D.; Taunton, J.; Nazzari, H.; De Souza, A.M.; Heilbron, B.; Cater, C.; MacDonald, M.; et al. Assessment of Cardiovascular Risk and Preparticipation Screening Protocols in Masters Athletes: The Masters Athlete Screening Study (MASS): A Cross-Sectional Study. BMJ Open Sport Exerc. Med. 2018, 4, e000370. [Google Scholar] [CrossRef]
- Börjesson, M.; Assanelli, D.; Carré, F.; Dugmore, D.; Panhuyzen-Goedkoop, N.M.; Seiler, C.; Senden, J.; Solberg, E.E. ESC Study Group of Sports Cardiology: Recommendations for Participation in Leisure-Time Physical Activity and Competitive Sports for Patients with Ischaemic Heart Disease. Eur. J. Cardiovasc. Prev. Rehabil. 2006, 13, 137–149. [Google Scholar] [CrossRef]
- Knuuti, J.; Wijns, W.; Saraste, A.; Capodanno, D.; Barbato, E.; Funck-Brentano, C.; Prescott, E.; Storey, R.F.; Deaton, C.; Cuisset, T.; et al. 2019 ESC Guidelines for the Diagnosis and Management of Chronic Coronary Syndromes. Eur. Heart J. 2020, 41, 407–477. [Google Scholar] [CrossRef]
- Keelan, P.C.; Bielak, L.F.; Ashai, K.; Jamjoum, L.S.; Denktas, A.E.; Rumberger, J.A.; Sheedy, I.P.F.; Peyser, P.A.; Schwartz, R.S. Long-Term Prognostic Value of Coronary Calcification Detected by Electron-Beam Computed Tomography in Patients Undergoing Coronary Angiography. Circulation 2001, 104, 412–417. [Google Scholar] [CrossRef]
- Patel, V.I.; Roy, S.K.; Budoff, M.J. Coronary Computed Tomography Angiography (CCTA) vs Functional Imaging in the Evaluation of Stable Ischemic Heart Disease. J. Invasive Cardiol. 2021, 33, E349–E354. [Google Scholar] [PubMed]
- Pellikka, P.A.; Nagueh, S.F.; Elhendy, A.A.; Kuehl, C.A.; Sawada, S.G. American Society of Echocardiography Recommendations for Performance, Interpretation, and Application of Stress Echocardiography. J. Am. Soc. Echocardiogr. 2007, 20, 1021–1041. [Google Scholar] [CrossRef]
- Dorbala, S.; Ananthasubramaniam, K.; Armstrong, I.S.; Chareonthaitawee, P.; DePuey, E.G.; Einstein, A.J.; Gropler, R.J.; Holly, T.A.; Mahmarian, J.J.; Park, M.-A.; et al. Single Photon Emission Computed Tomography (SPECT) Myocardial Perfusion Imaging Guidelines: Instrumentation, Acquisition, Processing, and Interpretation. J. Nucl. Cardiol. 2018, 25, 1784–1846. [Google Scholar] [CrossRef]
- Greenwood, J.P.; Maredia, N.; Younger, J.F.; Brown, J.M.; Nixon, J.; Everett, C.C.; Bijsterveld, P.; Ridgway, J.P.; Radjenovic, A.; Dickinson, C.J.; et al. Cardiovascular Magnetic Resonance and Single-Photon Emission Computed Tomography for Diagnosis of Coronary Heart Disease (CE-MARC): A Prospective Trial. Lancet 2012, 379, 453–460. [Google Scholar] [CrossRef] [PubMed]
- Wagner, A.; Mahrholdt, H.; Kim, R.J.; Judd, R.M. Use of Cardiac Magnetic Resonance to Assess Viability. Curr. Cardiol. Rep. 2005, 7, 59–64. [Google Scholar] [CrossRef]
- Sörensson, P.; Ekenbäck, C.; Lundin, M.; Agewall, S.; Bacsovics Brolin, E.; Caidahl, K.; Cederlund, K.; Collste, O.; Daniel, M.; Jensen, J.; et al. Early Comprehensive Cardiovascular Magnetic Resonance Imaging in Patients with Myocardial Infarction with Nonobstructive Coronary Arteries. JACC Cardiovasc. Imaging 2021, 14, 1774–1783. [Google Scholar] [CrossRef]
- Shave, R.; Baggish, A.; George, K.; Wood, M.; Scharhag, J.; Whyte, G.; Gaze, D.; Thompson, P.D. Exercise-Induced Cardiac Troponin Elevation. J. Am. Coll. Cardiol. 2010, 56, 169–176. [Google Scholar] [CrossRef] [PubMed]
- Celeski, M.; Segreti, A.; Piscione, M.; Monticelli, L.M.; Di Gioia, G.; Fossati, C.; Ussia, G.P.; Pigozzi, F.; Grigioni, F. The Current Paradigm of Cardiac Troponin Increase among Athletes. Monaldi Arch. Chest Dis. 2024. [Google Scholar] [CrossRef]
- Sana, F.; Isselbacher, E.M.; Singh, J.P.; Heist, E.K.; Pathik, B.; Armoundas, A.A. Wearable Devices for Ambulatory Cardiac Monitoring. J. Am. Coll. Cardiol. 2020, 75, 1582–1592. [Google Scholar] [CrossRef] [PubMed]
- Konstantinidis, D.; Iliakis, P.; Tatakis, F.; Thomopoulos, K.; Dimitriadis, K.; Tousoulis, D.; Tsioufis, K. Wearable Blood Pressure Measurement Devices and New Approaches in Hypertension Management: The Digital Era. J. Hum. Hypertens. 2022, 36, 945–951. [Google Scholar] [CrossRef] [PubMed]
- Hughes, A.; Shandhi, M.M.H.; Master, H.; Dunn, J.; Brittain, E. Wearable Devices in Cardiovascular Medicine. Circ. Res. 2023, 132, 652–670. [Google Scholar] [CrossRef] [PubMed]
- Maron, D.J.; Hochman, J.S.; Reynolds, H.R.; Bangalore, S.; O’Brien, S.M.; Boden, W.E.; Chaitman, B.R.; Senior, R.; López-Sendón, J.; Alexander, K.P.; et al. Initial Invasive or Conservative Strategy for Stable Coronary Disease. N. Engl. J. Med. 2020, 382, 1395–1407. [Google Scholar] [CrossRef]
- Hochman, J.S.; Anthopolos, R.; Reynolds, H.R.; Bangalore, S.; Xu, Y.; O’Brien, S.M.; Mavromichalis, S.; Chang, M.; Contreras, A.; Rosenberg, Y.; et al. Survival After Invasive or Conservative Management of Stable Coronary Disease. Circulation 2023, 147, 8–19. [Google Scholar] [CrossRef]
- Mancini, G.B.J.; Hartigan, P.M.; Shaw, L.J.; Berman, D.S.; Hayes, S.W.; Bates, E.R.; Maron, D.J.; Teo, K.; Sedlis, S.P.; Chaitman, B.R.; et al. Predicting Outcome in the COURAGE Trial (Clinical Outcomes Utilizing Revascularization and Aggressive Drug Evaluation). JACC Cardiovasc. Interv. 2014, 7, 195–201. [Google Scholar] [CrossRef]
- McKinney, J.; Moulson, N.; Morrison, B.N.; Phulka, J.S.; Yeung, P.; Isserow, S.; Wood, D.A. Do Athletes Play by Different Rules? Obstructive Coronary Artery Disease in Asymptomatic Competitive Masters Athletes: A Case Series. Eur. Heart J.-Case Rep. 2020, 4, 1–5. [Google Scholar] [CrossRef] [PubMed]
- Cook, C.M.; Ahmad, Y.; Howard, J.P.; Shun-Shin, M.J.; Sethi, A.; Clesham, G.J.; Tang, K.H.; Nijjer, S.S.; Kelly, P.A.; Davies, J.R.; et al. Impact of Percutaneous Revascularization on Exercise Hemodynamics in Patients with Stable Coronary Disease. J. Am. Coll. Cardiol. 2018, 72, 970–983. [Google Scholar] [CrossRef]
- Van Nunen, L.X.; Zimmermann, F.M.; Tonino, P.A.L.; Barbato, E.; Baumbach, A.; Engstrøm, T.; Klauss, V.; MacCarthy, P.A.; Manoharan, G.; Oldroyd, K.G.; et al. Fractional Flow Reserve versus Angiography for Guidance of PCI in Patients with Multivessel Coronary Artery Disease (FAME): 5-Year Follow-up of a Randomised Controlled Trial. Lancet 2015, 386, 1853–1860. [Google Scholar] [CrossRef]
- Xaplanteris, P.; Fournier, S.; Pijls, N.H.J.; Fearon, W.F.; Barbato, E.; Tonino, P.A.L.; Engstrøm, T.; Kääb, S.; Dambrink, J.-H.; Rioufol, G.; et al. Five-Year Outcomes with PCI Guided by Fractional Flow Reserve. N. Engl. J. Med. 2018, 379, 250–259. [Google Scholar] [CrossRef] [PubMed]
- Aengevaeren, V.L.; Mosterd, A.; Bakker, E.A.; Braber, T.L.; Nathoe, H.M.; Sharma, S.; Thompson, P.D.; Velthuis, B.K.; Eijsvogels, T.M.H. Exercise Volume Versus Intensity and the Progression of Coronary Atherosclerosis in Middle-Aged and Older Athletes: Findings from the MARC-2 Study. Circulation 2023, 147, 993–1003. [Google Scholar] [CrossRef] [PubMed]
- Parker, J.L.; Oltman, C.L.; Muller, J.M.; Myers, P.R.; Adams, H.R.; Laughlin, M.H. Effects of Exercise Training on Regulation of Tone in Coronary Arteries and Arterioles. Med. Sci. Sports Exerc. 1994, 26, 1252–1261. [Google Scholar] [CrossRef]
- Haskell, W.L.; Sims, C.; Myll, J.; Bortz, W.M.; St Goar, F.G.; Alderman, E.L. Coronary Artery Size and Dilating Capacity in Ultradistance Runners. Circulation 1993, 87, 1076–1082. [Google Scholar] [CrossRef]
- Yonetsu, T.; Jang, I.-K. Advances in Intravascular Imaging: New Insights into the Vulnerable Plaque from Imaging Studies. Korean Circ. J. 2018, 48, 1–15. [Google Scholar] [CrossRef]
Guidelines 1 | Settings | Competitive Sports Allowed if | Competitive Sports Not Recommended if |
---|---|---|---|
ESC | Clinically manifest CAD in the setting of CCS | - Preserved LVEF, no abnormalities on a maximal exercise test or functional imaging test, no high-risk coronary lesions | - High-risk coronary lesions 2 not eligible for revascularization - LVEF ≤ 50% - Inducible myocardial ischemia or NSVT/frequent PVC |
Asymptomatic CAD 3 | - Disease progression during serial evaluations - Positive maximal exercise test or functional imaging test | - No inducible myocardial ischemia on functional imaging or conventional exercise stress | |
Acute coronary syndrome | - After 8–12 weeks of cardiac rehabilitation and 3–6 months of structured outpatient exercise programs - Normal exercise test with 12-lead ECG recording or CPET before returning to sport competition | - First 3–6 months after the event - Persistent inducible myocardial ischemia or Symptoms after successful revascularization | |
Post-revascularization | - After 3–6 months, if negative stress testing, normal LVEF, and no symptoms | - Ischemia that cannot be treated despite adequate therapy | |
ACC/AHA | Clinically manifest CAD in the setting of CCS | - LVEF > 50%, asymptomatic, no inducible ischemia or electrical instability | - Patients non-fulfilling 1 or more criteria: LVEF > 50%, asymptomatic, no inducible ischemia or electrical instability |
Asymptomatic CAD 4 | X | X | |
Acute coronary syndrome | - After 3 months of the event - No symptoms and no inducible myocardial ischemia | -Increasing frequency or worsening symptoms of myocardial ischemia - First 120 days after ACS | |
Post-revascularization | - After 3 months following PCI - No symptoms and no inducible myocardial ischemia | -Increasing frequency or worsening symptoms of myocardial ischemia - First 120 days after ACS |
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Celeski, M.; Di Gioia, G.; Nusca, A.; Segreti, A.; Squeo, M.R.; Lemme, E.; Mango, F.; Ferrera, A.; Ussia, G.P.; Grigioni, F. The Spectrum of Coronary Artery Disease in Elite Endurance Athletes—A Long-Standing Debate: State-of-the-Art Review. J. Clin. Med. 2024, 13, 5144. https://doi.org/10.3390/jcm13175144
Celeski M, Di Gioia G, Nusca A, Segreti A, Squeo MR, Lemme E, Mango F, Ferrera A, Ussia GP, Grigioni F. The Spectrum of Coronary Artery Disease in Elite Endurance Athletes—A Long-Standing Debate: State-of-the-Art Review. Journal of Clinical Medicine. 2024; 13(17):5144. https://doi.org/10.3390/jcm13175144
Chicago/Turabian StyleCeleski, Mihail, Giuseppe Di Gioia, Annunziata Nusca, Andrea Segreti, Maria Rosaria Squeo, Erika Lemme, Federica Mango, Armando Ferrera, Gian Paolo Ussia, and Francesco Grigioni. 2024. "The Spectrum of Coronary Artery Disease in Elite Endurance Athletes—A Long-Standing Debate: State-of-the-Art Review" Journal of Clinical Medicine 13, no. 17: 5144. https://doi.org/10.3390/jcm13175144