The Heart of the Female Athlete
Female sports participation has increased enormously since passage of Title IX in 1972, and women now participate in almost equal numbers as men from the high school level through the Olympics.1-3 Over these same decades, sports cardiology has emerged as a clinical field to serve the needs of highly active individuals and athletes. Though historically female athletes have been underrepresented in the body of research that informs sports cardiology practice, more recently several studies have embraced gender as an important biologic variable. We will review the impact of gender on key issues within sports cardiology and identify areas relevant to the female athlete in need of further investigation.
Recognizing Exercise-Induced Cardiac Adaptations in the Female Athlete
Exercise training induces a myriad of physiologic adaptations in the cardiovascular system. Differentiating what findings on cardiac studies (i.e., electrocardiogram [ECG], imaging) constitute exercise-induced adaptation versus cardiac disease is critical when female athletes present for clinical evaluation.
Female and male athletes have different prevalence of both normal, training-related ECG findings and of abnormal, potentially pathologic ECG patterns (Table 1). Specifically, normal variants including elevated QRS voltage, incomplete right bundle branch block and normal early repolarization are less common in female athletes than males.4-8 Whereas inferior and lateral T-wave inversions (TWI) are more prevalent in male athletes, anterior TWI are more prevalent in females and are less commonly associated with structural cardiac disease than TWI in other distributions.9,9-11 Independent of athletic remodeling, females have longer corrected QT (QTc) intervals than males. This is reflected in the consensus guidelines for athlete ECG interpretation, which stipulate a higher cutoff for normal QTc for females than males.12,13 Male and female athletes are not otherwise treated differently in these ECG interpretation guidelines despite differing in their ECG manifestation of athletic remodeling and in their pre-test probability of certain cardiac diseases (see below). We await data on whether these new guidelines perform differently in males and females when the ECG is used in the pre-participation exam.
Exercise-induced cardiac remodeling as manifest on cardiac imaging also differs based on gender. Female athletes have smaller absolute biventricular chamber size, left ventricular (LV) mass and wall thickness than male athletes.14,15 Consistent with prior work, a recent study that evaluated elite white athletes found that no females had LV wall thickness >12 mm (vs. 2.5% of males) and comparatively few females (7%) had LV end-diastolic dimension >54mm (vs. 47% of males).7 Though such absolute cutoffs for normality may be appealing, their application is fraught with several issues. First, the most accurate way to adjust measured heart size for body size remains unclear. For example, though LV and right ventricular (RV) size when normalized to body surface area (BSA) are actually larger in female than male athletes,7,16 this difference is attenuated or even reverses when normalized to lean body mass using allometric scaling.17 Second, the degree of expected exercise-induced cardiac remodeling within genders also varies based on sport type and ethnicity. For example, whether an LV wall thickness of 12 mm falls into a true clinical gray zone depends on whether the athlete is a white female long-distance runner with small body habitus or a black female thrower with larger body habitus because black ethnicity and high-static component "strength" sports are both associated with greater LV wall thickness.18,15 Overall, clinical interpretation of cardiac imaging in athletes necessitates an individualized approach that integrates gender along with body size, ethnicity and sport type. Whether reported differences in the degree and geometry of cardiac remodeling in males and female athletes reflect fundamentally different biological adaptation to exercise is unclear future work evaluating the underlying mechanisms of exercise-induced cardiac remodeling must identify whether gender serves as a modifier.
Identifying Cardiac Disease in the Female Athlete
When female athletes have cardiac findings on clinical evaluation that do not appear entirely consistent with physiologic remodeling, the most crucial diseases to exclude are those associated with sudden cardiac death (SCD). Women have slightly lower phenotypic prevalence of hypertrophic cardiomyopathy and arrhythmogenic right ventricular cardiomyopathy, which are diseases that may overlap structurally with exercise-induced remodeling and are among the most common causes of SCD in young athletes. Interestingly, even accounting for this differing prevalence of disease, the rate of SCD is consistently and disproportionally lower in female than male athletes (Table 2).19-26 This discordance suggests that those female athletes with structural cardiac disease may be less likely to suffer SCD than male athletes with the same conditions. Whether this apparent protection is attributable to differences in phenotypic expression of genetically mediated cardiac disease, to modification of arrhythmic risk by hormonal milieu or to other factors remains to be determined.27
Conversely, female athletes are more likely than males to harbor specific occult medical issues that either may present with symptoms that falsely suggest cardiovascular origin or may have associated cardiovascular manifestations (e.g., iron deficiency anemia, pregnancy, autoimmune disease, thyroid disease, fibromuscular dysplasia). The optimal comprehensive care for the female athlete presenting for evaluation includes a heightened awareness and appropriate testing for these conditions.
The Impact of Long-Term Exercise in the Female Athlete
Recently the question of whether long term exposure to high doses of exercise may be harmful has garnered a large amount of interest. This has been driven by the observation in several large epidemiologic studies that the most voluminous exercisers have slightly higher, though statistically insignificant, risk of mortality than those who exercise moderately (the so-called "reverse J-shaped curve").28-33 When mortality risk was stratified by gender in the largest of these studies, the shape of the exercise dose response curve in men and women was slightly different: whereas it retained the reverse-J shape in men, the plot was more curvilinear in women--meaning the most active women had similar mortality as those performing less activity (Figure 1).28 It is important to emphasize that, statistically, the data in men and women alike suggest that high doses of exercise appear similarly beneficial as moderate doses.28 However, the question of whether there may be a gender-based difference in risk at the extreme end of exercise dose is interesting because female athletes may also be at lower risk of developing forms of cardiac disease that have been posited as links between high amounts of exercise and excess cardiovascular disease risk.
Specifically, a subset of masters endurance athletes, all male, have been found to have ventricular fibrosis as demonstrated by late gadolinium enhancement (LGE) on cardiac magnetic resonance imaging.34-37 The cause of this fibrosis is unclear but may be ventricular overload, coronary disease or prior myocarditis. More recently, in a cohort that included an equal number of male and female masters triathletes, a sizable percentage of the men (17%) but none of the women were found to have LGE.38 These women competed in shorter distance events and were less fit than the men. Future work is needed to identify whether these results were due to different competitive levels between the groups or other gender-based biological mechanisms.
A similar narrative exists for the risk of coronary artery calcification and plaque in masters athletes. The initial studies examining this concept in males found a higher prevalence of CAD in athletes than controls despite adjustment for traditional risk factors.36,39 Though such cross-sectional work does not prove that exercise is causative, exercise-mediated mechanisms for plaque deposition have been proposed including turbulent coronary flow and altered calcium homeostasis. Recently, Merghani et al. compared the prevalence of CAD in masters endurance athletes, including 30% women, versus sedentary controls. Whereas male athletes had more CAD than controls, female athletes had a similar burden as sedentary females. The women in this study were, on average, close to menopause. It is possible that the absence of increased CAD in female athletes may be because CAD in women typically occurs later, after the menopausal fall in estrogen levels.40 How estrogen status may protect women from any interaction between high exposure to exercise and plaque formation remains unclear.
Finally, numerous observational studies have demonstrated that high doses of exercise are associated with more atrial fibrillation (AF).41 There are conflicting data on whether the added risk of high dose exercise applies equally to men and women. A recent prospective study suggested that AF risk in women followed the same pattern as in men, specifically that risk in the most active women was higher than those who were moderately active and similar to those who were inactive.42 However, a larger meta-analysis that included almost 150,000 women found that AF risk continued to decline across the spectrum of exercise dose.43 Overall, future studies that target masters female endurance athletes including those at an older age are needed in order to identify if highly active women are partially immune to the processes that drive ventricular fibrosis, CAD and AF or perhaps only temporarily protected by hormonal status until after menopause. Fortunately, the number of such women available for this research is posed to increase as more young women begin sports and then continue exercise habits into later life.
- International Olympic Committee. Factsheet: Women in the Olympic Movement Update June 2016. International Olympic Committee, Lausanne, Switzerland 2016.
- Irick E. NCAA Sports Sponsorship and Participation Rates Report. Indianapolis, IN: National Collegiate Athletic Association, 2017.
- 2016-17 High School Athletics Participation Survey. The National Federation of State High School Associations, 2017.
- Wasfy MM, DeLuca J, Wang F, et al. ECG findings in competitive rowers: normative data and the prevalence of abnormalities using contemporary screening recommendations. Br J Sports Med 2015;49:200-6.
- Pelliccia A, Maron BJ, Culasso F, et al. Clinical significance of abnormal electrocardiographic patterns in trained athletes. Circulation 2000;102:278-84.
- Storstein L, Bjørnstad H, Hals O, Meen HD. Electrocardiographic findings according to sex in athletes and controls. Cardiology 1991;79:227-36.
- Finocchiaro G, Dhutia H, D'Silva A, et al. Effect of sex and sporting discipline on LV adaptation to exercise. JACC Cardiovasc Imaging 2017;10:965-72.
- Brosnan M, La Gerche A, Kalman J, et al. Comparison of frequency of significant electrocardiographic abnormalities in endurance versus nonendurance athletes. Am J Cardiol 2014;113:1567-73.
- Malhotra A, Dhutia H, Gati S, et al. Anterior T-wave inversion in young white athletes and nonathletes: prevalence and significance. J Am Coll Cardiol 2017;69:1-9.
- Papadakis M, Basavarajaiah S, Rawlins J, et al. Prevalence and significance of T-wave inversions in predominantly Caucasian adolescent athletes. Eur Heart J 2009;30:1728-35.
- Sheikh N, Papadakis M, Schnell F, et al. Clinical profile of athletes with hypertrophic cardiomyopathy. Circ Cardiovasc Imaging 2015;8:e003454.
- Drezner JA, Sharma S, Baggish A, et al. Internatational criteria for electrocardiographic interpretation in athletes: consensus statement. Br J Sports Med 2017;51:704-31.
- Pickham D, Zarafshar S, Sani D, Kumar N, Froelicher V. Comparison of three ECG criteria for athlete pre-participation screening. J Electrocardiol 2014;47:769-74.
- D'Ascenzi F, Pisicchio C, Caselli S, Di Paolo FM, Spataro A, Pelliccia A. RV remodeling in Olympic athletes. JACC Cardiovasc Imaging 2017;10:385-93.
- Baggish AL, Wang F, Weiner RB, et al. Training-specific changes in cardiac structure and function: a prospective and longitudinal assessment of competitive athletes. J Appl Physiol 2008;104:1121-8.
- D'Ascenzi F, Pisicchio C, Caselli S, Di Paolo FM, Spataro A, Pelliccia A. RV remodeling in Olympic athletes. JACC Cardiovasc Imaging 2017;10:385-93.
- Giraldeau G, Kobayashi Y, Finocchiaro G, et al. Gender differences in ventricular remodeling and function in college athletes, insights from lean body mass scaling and deformation imaging. Am J Cardiol 2015;116:1610-6.
- Rawlins J, Carre F, Kervio G, et al. Ethnic differences in physiological cardiac adaptation to intense physical exercise in highly trained female athletes. Circulation 2010;121:1078-85.
- Harmon KG, Asif IM, Maleszewski JJ, et al. Incidence and etiology of sudden cardiac arrest and death in high school athletes in the United States. Mayo Clin Proc 2016;91:1493-502.
- Toresdahl BG, Rao Al, Harmon KG, Drezner JA. Incidence of sudden cardiac arrest in high school student athletes on school campus. Heart Rhythm 2014;11:1190-4.
- Harmon KG, Asif IM, Maleszewski JJ, et al. Incidence, cause, and comparative frequency of sudden cardiac death in National Collegiate Athletic Association athletes: a decade in review. Circulation 2015;132:10-9.
- Maron BJ, Haas TS, Murphy CJ, Ahluwalia A, Rutten-Ramos S. Incidence and causes of sudden death in U.S. college athletes. J Am Coll Cardiol 2014;63:1636-43.
- Kim HJ, Malhotra R, Chiampas G, et al. Cardiac arrest during long-distance running races. N Engl J Med 2012;366:130-40.
- Mathews SC, Narotsky DL, Bernholt DL, et al. Mortality among marathon runners in the United States, 2000-2009. Am J Sports Med 2012;40:1495-500.
- Roberts WO, Roberts DM, Lunos S. Marathon related cardiac arrest risk differences in men and women. Br J Sports Med 2013;47:168-71.
- Harris KM, Creswell LL, Haas TS, et al. Death and cardiac arrest in U.S. triathlon participants, 1985 to 2016: a case series. Ann Intern Med 2017;167:529-35.
- Furholz M, Radtke T, Roten L, et al. Training-related modulations of the autonomic nervous system in endurance athletes: is female gender cardioprotective? Eur J Appl Physiol 2013;113:631-40.
- Arem H, Moore SC, Patel A, et al. Leisure time physical activity and mortality: a detailed pooled analysis of the dose-response relationship. JAMA Intern Med 2015;175:959-67.
- Lee DC, Pate RR, Lavie CJ, Sui X, Church TS, Blair SN. Leisure-time running reduces all-cause and cardiovascular mortality risk. J Am Coll Cardiol 2014;64:472-81.
- Paffenbarger RS, Hyde RT, Wing AL, Hsieh CC. Physical activity, all-cause mortality, and longevity of college alumni. N Engl J Med 1986;314:605-13.
- Lee IM, Hsieh CC, Paffenbarger RS. Exercise intensity and longevity in men. The Harvard Alumni Health Study. JAMA 1995;273:1179-84.
- Sundquist K, Qvist J, Sundquist J, Johansson SE. Frequent and occasional physical activity in the elderly: a 12-year follow-up study of mortality. Am J Prev Med 2004;27:22-7.
- Janssen I, Joliffe CJ. Influence of physical activity on mortality in elderly with coronary artery disease. Med Sci Sports Exerc 2006;38:418-7.
- La Gerche A, Burns AT, Mooney DJ, et al. Exercise-induced right ventricular dysfunction and structural remodelling in endurance athletes. Eur Heart J 2012;33:998-1006.
- Breuckmann F, Mohlenkamp S, Nassenstein K, et al. Myocardial late gadolinium enhancement: prevalence, pattern, and prognostic relevance in marathon runners. Radiology 2009;251:50-7.
- Möhlenkamp S, Lehmann N, Breuckmann F, et al. Running: the risk of coronary events: prevalence and prognostic relevance of coronary atherosclerosis in marathon runners. Eur Heart J 2008;29:1903-10.
- Wilson M, O'Hanlon R, Prasad S, et al. Diverse patterns of myocardial fibrosis in lifelong, veteran endurance athletes. J Appl Physiol 2011;110:1622-6.
- Tahir E, Starekova J, Muellerleile K, et al. Myocardial fibrosis in competitive triathletes detected by contrast-enhanced CMR correlates with exercise-induced hypertension and competition history. JACC Cardiovasc Imaging 2017. [Epub ahead of print]
- Aengevaeren VL, Mosterd A, Braber TL, et al. Relationship between lifelong exercise volume and coronary atherosclerosis in athletes. Circulation 2017;136:138-48.
- Barrett-Connor E. Sex differences in coronary heart disease. Why are women so superior? The 1995 Ancel Keys Lecture. Circulation 1997;95:252-64.
- Estes NAM, Madias C. Atrial fibrillation in athletes: a lesson in the virtue of moderation. JACC Clin Electrophysiol 2017;3:921-8.
- Morseth B, Graff-Iversen S, Jacobsen BK, et al. Physical activity, resting heart rate, and atrial fibrillaiton: the Tromso Study. Eur Heart J 2016;37:2307-13.
- Mohanty S, Mohanty P, Tamaki M, et al. Differential association of exercise intensity with risk of atrial fibrillation in men and women: evidence from meta-analysis. J Cardiovasc Electrophysiol 2016;27:1021-9.
Clinical Topics: Arrhythmias and Clinical EP, Diabetes and Cardiometabolic Disease, Heart Failure and Cardiomyopathies, Noninvasive Imaging, Prevention, Sports and Exercise Cardiology, Atherosclerotic Disease (CAD/PAD), EP Basic Science, Genetic Arrhythmic Conditions, SCD/Ventricular Arrhythmias, Atrial Fibrillation/Supraventricular Arrhythmias, Magnetic Resonance Imaging, Exercise, Sports and Exercise and Imaging
Keywords: Accidental Falls, Adaptation, Biological, Adaptation, Physiological, Anemia, Iron-Deficiency, Arrhythmogenic Right Ventricular Dysplasia, Athletes, Atrial Fibrillation, Autoimmune Diseases, Biological Products, Body Size, Body Surface Area, Bundle-Branch Block, Calcium, Cardiomyopathy, Hypertrophic, Coronary Artery Disease, Cross-Sectional Studies, Death, Sudden, Cardiac, Electrocardiography, Epidemiologic Studies, Estrogens, Exercise, Fibromuscular Dysplasia, Gadolinium, Homeostasis, Magnetic Resonance Imaging, Menopause, Myocarditis, Plaque, Atherosclerotic, Pregnancy, Risk Factors, Sports, Thyroid Diseases
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