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Cited by 298Cardiovascular Effects of ExerciseCardiomyopathy and Myosin StudiesViral Infections and Immunology Research

Diverse patterns of myocardial fibrosis in lifelong, veteran endurance athletes

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Wilson, M., O'Hanlon, R., Prasad, S., Deighan, A., MacMillan, P., Oxborough, D., Godfrey, R., Smith, G. +4 more·2011·Journal of Applied Physiology
DOI 10.1152/japplphysiol.01280.2010PMC PMC3119133
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Abstract

This study examined the cardiac structure and function of a unique cohort of documented lifelong, competitive endurance veteran athletes (>50 yr). Twelve lifelong veteran male endurance athletes [mean ± SD (range) age: 56 ± 6 yr (50–67)], 20 age-matched veteran controls [60 ± 5 yr; (52–69)], and 17 younger male endurance athletes [31 ± 5 yr (26–40)] without significant comorbidities underwent cardiac magnetic resonance (CMR) imaging to assess cardiac morphology and function, as well as CMR imaging with late gadolinium enhancement (LGE) to assess myocardial fibrosis. Lifelong veteran athletes had smaller left (LV) and right ventricular (RV) end-diastolic and end-systolic volumes ( P < 0.05), but maintained LV and RV systolic function compared with young athletes. However, veteran athletes had a significantly larger absolute and indexed LV and RV end-diastolic and systolic volumes, intraventricular septum thickness during diastole, posterior wall thickness during diastole, and LV and RV stroke volumes ( P < 0.05), together with significantly reduced LV and RV ejection fractions ( P < 0.05), compared with veteran controls. In six (50%) of the veteran athletes, LGE of CMR indicated the presence of myocardial fibrosis (4 veteran athletes with LGE of nonspecific cause, 1 probable previous myocarditis, and 1 probable previous silent myocardial infarction). There was no LGE in the age-matched veteran controls or young athletes. The prevalence of LGE in veteran athletes was not associated with age, height, weight, or body surface area ( P > 0.05), but was significantly associated with the number of years spent training ( P < 0.001), number of competitive marathons ( P < 0.001), and ultraendurance (>50 miles) marathons ( P < 0.007) completed. An unexpectedly high prevalence of myocardial fibrosis (50%) was observed in healthy, asymptomatic, lifelong veteran male athletes, compared with zero cases in age-matched veteran controls and young athletes. These data suggest a link between lifelong endurance exercise and myocardial fibrosis that requires further investigation.

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  • DGE was observed in 6 of 12 elite veteran athletes but not in 17 young novice athletes or 20 older non-athletes.

    “More recently, Wilson et al. 18 observed DGE in 6 of 12 elite veteran athletes but not in 17 young novice athletes or 20 older non-athletes.”

    From Exercise-induced right ventricular dysfunction and structural remodelling in endurance athletes (2012) · cites this paper as [18]

    The Results report LGE in 6 of 12 veteran athletes and none in the 17 young athletes or 20 age-matched controls. But the Methods describe the young athletes as experienced endurance competitors with 11–31 years of training, not novices. The paper calls the imaging finding LGE rather than DGE. (LLM, conf=0.90)

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  • In a study of 12 veteran male endurance athletes assessed by cardiac MRI, half (6/12) demonstrated late gadolinium enhancement compared to sedentary controls, and years in training and number of competitive marathons predicted prevalence of LGE.

    “Similar findings of myocardial fibrosis were presented a few years later in another study involving 12 veteran male endurance athletes who were assessed by cardiac magnetic resonance imaging (MRI) [54]. Specifically, half of them (6/12 athletes) demonstrated late gadolinium enhancement (LGE) compared to sedentary controls. The number of years spent in training (p < 0.001) and the number of”

    From Atrial Fibrillation in Elite Athletes: A Comprehensive Review of the Literature (2024) · cites this paper as [54]

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References 30 · Cited by 298

Research works printed but not linked: 29

  1. [1]1. Anselme F. Association of idiopathic RVOT VT and AVNRT: anything else than chance? Europace 5: 221–223, 2003 [DOI] [PubMed] [Google Scholar]
  2. [2]2. Batterham AM, George KP, Whyte G, Sharma S, McKenna W. Scaling cardiac structural data by body dimensions: a review of theory, practice, and problems. Int J Sports Med 20: 495–502, 1999 [DOI] [PubMed] [Google Scholar]
  3. [3]3. Benito B, Gay-Jordi G, Serrano-Mollar A, Guasch E, Shi Y, Tardif JC, Brugada J, Nattel S, Mont L. Cardiac arrhythmogenic remodeling in a rat model of long-term intensive exercise training. Circulation 123: 13–22, 2011 [DOI] [PubMed] [Google Scholar]
  4. [4]4. Bouvier F, Saltin B, Nejat M, Jensen-Urstad M. Left ventricular function and perfusion in elderly endurance athletes. Med Sci Sports Exerc 33: 735–740, 2001 [DOI] [PubMed] [Google Scholar]
  5. [5]5. Breuckmann F, Mohlenkamp S, Nassenstein K, Lehmann N, Ladd S, Schmermund A, Sievers B, Schlosser T, Jockel KH, Heusch G, Erbel R, Barkhausen J. Myocardial late gadolinium enhancement: prevalence, pattern, and prognostic relevance in marathon runners. Radiology 251: 50–57, 2009 [DOI] [PubMed] [Google Scholar]
  6. [6]6. Cerqueira MD, Weissman NJ, Dilsizian V, Jacobs AK, Kaul S, Laskey WK, Pennell DJ, Rumberger JA, Ryan T, Verani MS. Standardized myocardial segmentation and nomenclature for tomographic imaging of the heart: a statement for healthcare professionals from the Cardiac Imaging Committee of the Council on Clinical Cardiology of the American Heart Association. Circulation 105: 539–542, 2002 [DOI] [PubMed] [Google Scholar]
  7. [7]7. Ector J, Ganame J, van der Merwe N, Adriaenssens B, Pison L, Willems R, Gewillig M, Heidbuchel H. Reduced right ventricular ejection fraction in endurance athletes presenting with ventricular arrhythmias: a quantitative angiographic assessment. Eur Heart J 28: 345–353, 2007 [DOI] [PubMed] [Google Scholar]
  8. [8]8. Grimsmo J, Grundvold I, Maehlum S, Arnesen H. Echocardiographic evaluation of aged male cross country skiers. Scand J Med Sci Sports. In press [DOI] [PubMed] [Google Scholar]
  9. [9]9. Jensen-Urstad K, Bouvier F, Saltin B, Jensen-Urstad M. High prevalence of arrhythmias in elderly male athletes with a lifelong history of regular strenuous exercise. Heart 79: 161–164, 1998 [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. [10]10. Kawara T, Derksen R, de Groot JR, Coronel R, Tasseron S, Linnenbank AC, Hauer RN, Kirkels H, Janse MJ, de Bakker JM. Activation delay after premature stimulation in chronically diseased human myocardium relates to the architecture of interstitial fibrosis. Circulation 104: 3069–3075, 2001 [DOI] [PubMed] [Google Scholar]
  11. [11]11. Kramer CM, Barkhausen J, Flamm SD, Kim RJ, Nagel E. Standardized cardiovascular magnetic resonance imaging (CMR) protocols, society for cardiovascular magnetic resonance: board of trustees task force on standardized protocols. J Cardiovasc Magn Reson 10: 35, 2008 [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. [12]12. Lakatta EG, Levy D. Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises. II. The aging heart in health: links to heart disease. Circulation 107: 346–354, 2003 [DOI] [PubMed] [Google Scholar]
  13. [13]13. Miki T, Yokota Y, Seo T, Yokoyama M. Echocardiographic findings in 104 professional cyclists with follow-up study. Am Heart J 127: 898–905, 1994 [DOI] [PubMed] [Google Scholar]
  14. [14]14. Mohlenkamp S, Lehmann N, Breuckmann F, Brocker-Preuss M, Nassenstein K, Halle M, Budde T, Mann K, Barkhausen J, Heusch G, Jockel KH, Erbel R. Running: the risk of coronary events. Prevalence and prognostic relevance of coronary atherosclerosis in marathon runners. Eur Heart J 29: 1903–1910, 2008 [DOI] [PubMed] [Google Scholar]
  15. [15]15. Mohlenkamp S, Schmermund A, Kroger K, Kerkhoff G, Brocker-Preuss M, Adams V, Hensel M, Kiefer D, Lehmann N, Moebus S, Leineweber K, Elsenbruch S, Barkhausen J, Halle M, Hambrecht R, Siegrist J, Mann K, Budde T, Jockel KH, Erbel R. Coronary atherosclerosis and cardiovascular risk in masters male marathon runners. Rationale and design of the “marathon study”. Herz 31: 575–585, 2006 [DOI] [PubMed] [Google Scholar]
  16. [16]16. Mont L, Elosua R, Brugada J. Endurance sport practice as a risk factor for atrial fibrillation and atrial flutter. Europace 11: 11–17, 2009 [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. [17]17. Nikitin NP, Witte KK, Ingle L, Clark AL, Farnsworth TA, Cleland JG. Longitudinal myocardial dysfunction in healthy older subjects as a manifestation of cardiac ageing. Age Ageing 34: 343–349, 2005 [DOI] [PubMed] [Google Scholar]
  18. [18]18. O'Hanlon R, Wilson M, Wage R, Smith G, Alpendurada FD, Wong J, Dahl A, Oxborough D, Godfrey R, Sharma S, Roughton M, George K, Pennell DJ, Whyte G, Prasad SK. Troponin release following endurance exercise: is inflammation the cause? A cardiovascular magnetic resonance study. J Cardiovasc Magn Reson 12: 38, 2010 [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. [19]19. Olivetti G, Melissari M, Capasso JM, Anversa P. Cardiomyopathy of the aging human heart. Myocyte loss and reactive cellular hypertrophy. Circ Res 68: 1560–1568, 1991 [DOI] [PubMed] [Google Scholar]
  20. [20]20. Roberts WO, Maron BJ. Evidence for decreasing occurrence of sudden cardiac death associated with the marathon. J Am Coll Cardiol 46: 1373–1374, 2005 [DOI] [PubMed] [Google Scholar]
  21. [21]21. Rowe WJ. A world record marathon runner with silent ischemia without coronary atherosclerosis. Chest 99: 1306–1308, 1991 [DOI] [PubMed] [Google Scholar]
  22. [22]22. Rowe WJ. Endurance exercise and injury to the heart. Sports Med 16: 73–79, 1993 [DOI] [PubMed] [Google Scholar]
  23. [23]23. Sandstede J, Lipke C, Beer M, Hofmann S, Pabst T, Kenn W, Neubauer S, Hahn D. Age- and gender-specific differences in left and right ventricular cardiac function and mass determined by cine magnetic resonance imaging. Eur Radiol 10: 438–442, 2000 [DOI] [PubMed] [Google Scholar]
  24. [24]24. Simonetti OP, Kim RJ, Fieno DS, Hillenbrand HB, Wu E, Bundy JM, Finn JP, Judd RM. An improved MR imaging technique for the visualization of myocardial infarction. Radiology 218: 215–223, 2001 [DOI] [PubMed] [Google Scholar]
  25. [25]25. Spiewak M, Malek LA, Misko J, Chojnowska L, Milosz B, Klopotowski M, Petryka J, Dabrowski M, Kepka C, Ruzyllo W. Comparison of different quantification methods of late gadolinium enhancement in patients with hypertrophic cardiomyopathy. Eur J Radiol 74: e149–e153, 2010 [DOI] [PubMed] [Google Scholar]
  26. [26]26. Tunstall Pedoe DS. Sudden death risk in older athletes: increasing the denominator. Br J Sports Med 38: 671–672, 2004 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. [27]27. Whyte G, Sheppard M, George K, Shave R, Wilson M, Prasad S, O'Hanlon R, Sharma S. Post-mortem evidence of idiopathic left ventricular hypertrophy and idiopathic interstitial myocardial fibrosis: is exercise the cause? Br J Sports Med 42: 304–305, 2008 [DOI] [PubMed] [Google Scholar]
  28. [28]28. Whyte GP, Sheppard M, George KP, Shave RE, Wilson M, Stephens N, Senior R, Sharma S. Arrhythmias and the athlete: mechanisms and clinical significance. Eur Heart J 28: 1399–1401; author reply 1401, 2007 [DOI] [PubMed] [Google Scholar]
  29. [29]29. Yared K, Wood MJ. Is marathon running hazardous to your cardiovascular health? The jury is still out. Radiology 251: 3–5, 2009 [DOI] [PubMed] [Google Scholar] Articles from Journal of Applied Physiology are provided here courtesy of American Physiological Society

Authors
Wilson, M., O'Hanlon, R., Prasad, S., Deighan, A., MacMillan, P., Oxborough, D., Godfrey, R., Smith, G., Maceira, A., Sharma, S., George, K., & Whyte, G.
Affiliations
  • Qatar Orthopaedic and Sports Medicine Hospital (QA)
  • Department of Cardiac Magnetic Resonance Imaging, Royal Brompton and Harefield National Health Service Trust, London, United Kingdom;
  • National Health Service (GB)
  • St Bartholomew's Hospital (GB)
  • Frenchay Hospital (GB)
  • University of Leeds (GB)
  • Brunel University of London (GB)
  • Hospital Universitari Arnau de Vilanova (ES)
  • St George's Hospital (GB)
  • Liverpool John Moores University (GB)
Corresponding author
Wilson, M.
ORCID
Venue
Journal of Applied Physiology
Publisher
American Physiological Society
Published
2011-06
Volume
110
Issue
6
Pages
1622-1626
ISSN
  • 0161-7567 (ISSN-L)
  • 8750-7587
  • 1522-1601
DOI
10.1152/japplphysiol.01280.2010
PMC
PMC3119133
OpenAlex
W2133563957
Cited by
298
References
30
Citations by year
2026: 8 · 2025: 9 · 2024: 29 · 2023: 7 · 2022: 15 · 2021: 20 · 2020: 35 · 2019: 12 · 2018: 25 · 2017: 20 · 2016: 20 · 2015: 23 · 2014: 28 · 2013: 14 · 2012: 17
FWCI
16.28
Type
journal article
Language
en
Open access
Locations
  • Journal of Applied Physiology (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Effects of Exercise
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiomyopathy and Myosin Studies
  • Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Viral Infections and Immunology Research
Keywords
myocardial fibrosis, older athletes, late gadolinium enhancement, cardiac magnetic resonance, cardiac structure and function, ejection fraction, marathon running, training duration, myocardial infarction, myocarditis, cardiac hypertrophy
MeSH terms
Adult, Age Factors, Aged, Aging, Analysis of Variance, Contrast Media, England, Fibrosis, Heart Diseases, Humans, Male, Middle Aged, Myocardium, Physical Endurance, Stroke Volume, Systole, Case-Control Studies, Ventricular Function, Left, Ventricular Function, Right, Magnetic Resonance Imaging, Cine, Athletes

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