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Introduction Sudden cardiac deaths in young people are devastating and personally tragic events, which fortunately occur uncommonly.1–7 Unsuspected genetic or congenital heart dis- eases, as well as blunt trauma and c ommotio cordis, have been recognized as causes of sudden cardiac deaths for >30 years.1–3,5,8,9 Considerable public debate has arisen in the lay and medical communities about establishing the most effective strategies for reducing or eliminating these events.6,10–25 For competitive athletes, much attention has been directed towards reducing head trauma and concussions in contact sports such as football,26–28 but also in devising prepartici- pation screening approaches for identifying potentially lethal cardiovascular diseases.6 In the process, a vast literature has been assem- bled, comprising both original data and a myriad of editorial commentaries.6

Although initially regarded as personal and family tragedies, the sudden deaths of young competitive athletes have become highly reported events over the past few

decades, achieving prominence in the public consciousness.1,5,6,10 Indeed, the sudden deaths of young people are counterintuitive and inconsistent with our expectations for sports competition. This discourse has been driven by the ubiquity of traditional and new social media, creating an exaggerated impres- sion of the incidence of these events that is disproportionate to the true effect that such deaths have on overall public health. Indeed, the strong influence of the media might have even fuelled the misconception that deaths are more common on athletic fields than they actually are, that these events might be largely limited to athletes, and that they are abso- lutely preventable by electro cardiographic screening.6,29 In this Perspectives article, we place many of these issues into the appro- priate context, with particular focus on the ethical considerations related to the prac- tice of limiting cardiovascular screening to c ompetitive athletes.

Historical context Interest in the preferential screening of young athlete populations (lately with electro cardiograms) has been justified on the assumption that sudden death owing to

underlying and unsuspected cardiovascular disease is largely explained by the physi- cally vigorous and stressful lifestyle to which young athletes are uniquely exposed by virtue of competition and systematic training regimens—that these deaths occur in athletes because they are athletes.6,30,31 However, the data supporting a strong link between com- petitive sports participation and the risk of sudden death remains incomplete.6,32–37 For example, sudden arrhythmic deaths were reported in 2014 to be most common at rest or during sleep.38

In the USA, a long-standing customary practice is to screen young people before they engage in sanctioned competitive sports in high school or college, using a personal and family history and physical examination, such as the 14 elements recom- mended by the AHA/ACC.6 This process has generally included all student athletes (at high school or college), independently of their level of achievement and performance. Indeed, Israel, Italy, and the USA are the only countries with systematic, broad-based screening of the athlete population.5,6,10,22,25

Mass population screening with the 12-lead electrocardiogram (including on a national basis) has been heavily promoted by Italian cardiologists,5,10,17–19 and by some in the US sports medicine community,16,31 despite the lack of both conclusive evidence and general agreement that adding electro- cardiograms to the screening examination substantially reduces cardiovascular mortality (Figure 1).6,23,25,37 Indeed, the Italian proposal has triggered a decade-long debate among cardiologists, paediatricians, and family prac- titioners about the merits of various cardio- vascular screening strategies.4,6,7,15–25,30 Many in the US cardiology community,1,4,7,20,21,23,24 including the AHA/ACC, regard mass electro cardiographic screen ing as excessive, if not inadvisable.6,39 This view is predicated on the considerable number of expected false-positiv e and false-negative test results, and the costs triggered by secondary ‘down- stream’ diagnostic testing (largely, but not necessarily, limited to echocardiography), which is wasteful of resources that could otherwise be used to promote improved pop ulation health.40 These factors, as well as other obstacles associated with limited resources, have led to the view that national

OPINION

Ethics of preparticipation cardiovascular screening for athletes Barry J. Maron, Richard A. Friedman and Arthur Caplan

Abstract | Preparticipation screening for unsuspected cardiovascular disease is a controversial topic in the medical and lay communities. Much attention has been directed towards young competitive athletes, particularly the proposed strategy of incorporating 12‑lead electrocardiograms into the screening process, even on a national or worldwide basis. However, sudden deaths of young athletes owing to genetic or congenital heart diseases have a low incidence in the general population. Furthermore, young people not engaged in competitive sports can harbour the same conditions that cause sudden death in athletes, which has gone largely unrecognized. Notably, sudden deaths from these diseases are numerically far more common in the much larger population of nonathletes. In this Perspectives article, we propose that an ethical dilemma has emerged, raising the important public‑health issue of whether young individuals should be arbitrarily excluded from potentially life‑ saving clinical screening evaluations because they do not engage in competitive sports programmes.

Maron, B. J. et al. Nat. Rev. Cardiol. 12, 375–378 (2015); published online 24 February 2015; doi:10.1038/nrcardio.2015.21

Competing interests The authors declare no competing interests.

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or mandated universal electrocardiographic screening is impractical and imprecise, if not potentially unethical when arbitrarily c onfined to athletes.6,32,33

Incidence and proportionality Most data on the incidence and causes of sudden death in young people come from the athlete community, because these events can be easily tabulated owing to their trad- itionally extensive exposure in the public domain.29 By contrast, sudden deaths occur- ring in nonathletes or participants in infor- mal recreational sports are not regularly identified publically. As a consequence, the highly-charged deaths of individual young athletes have come to dominate, or even overwhelm, larger and potentially more substantial public-health issues.40

Based on the considerable assembled data, sudden deaths as a result of cardio vascular disease in young athletes are among the least common causes of death in this age group (Figure 2).6,24 We wish to empha- size that these events are several hundred- fold less common than the major causes of death, such as motor vehicle accidents or suicide, and occur with a similar frequency to that of fatal lightning strikes (Figure 2). For example, athlete data from Minnesota, USA,4 Denmark,33,34 and the Veneto region of Italy 5 all indicate that the  absolute numbers of these sudden death events are in the range of one to two annually, with

an incidence in most studies of 1:80,000 to 1:200,000.6

Nationwide comparative data from Denmark32–36,40 and France41 show that cardio vascular-related sudden deaths occur uncommonly in competitive athletes, and less frequently than in either recreational sports participants or the general popula- tion. This finding was the basis for the deci- sion by Danish health authorities to reject the European proposal to screen all com- petitive athletes with electrocardiograms. Resources can be redirected to other, more effective societal initiatives to reduce sudden deaths in young people (athletes and non- athletes alike),40 such as prevention of suicide, reduction of illicit drug use and the number of motor vehicle accidents and fatal- ities, as well as increased use of automated external d efibrillators for out-of-hospital cardiac arrest.40

An ethical dilemma The current situation, in which the oppor- tunity to detect potentially lethal cardio- vascular diseases is confined to those students who engage in organized or sanc- tioned competitive athletic programmes, unavoidably raises an ethical dilemma. With this practice, students or others not involved in competitive sports are arbitrar- ily excluded from the potentially impor- tant (and possibly life-saving) benefits of screening. In effect, this practice confers

preferential attention on competitive ath- letes solely because of their vigorous lifestyle and often public prominence.42 However, substantially more young people partici- pate in recreational or noncompetitive ath- letic activities,43 but nevertheless are also at risk of sudden death owing to unsuspected cardiovascular disease.41,44 For example, 70% of high school students and 98% of college students do not participate in competitive athletics, but often engage in other sports- related activities at some level, which can be vigorous and intense.45–48

Genetic and congenital heart diseases, such as hypertrophic cardiomyopathy, congenital coronary artery anomalies, arrhyth mo genic right ventricular cardiomyopathy, and ion channelopathies, which can cause sudden deaths in young people, do not have a unique predilection for trained athletes. Conversely, these diseases occur in both athletes and non athletes alike, and can cause sudden death whether they occur on the field during competition, in a myriad of recreational sporting activities, or even when associated with seden tary lifestyle.6,41 Given that only a minority of students choose to be trained competitive athletes,45–48 the absolute number of sudden deaths expected in nonathletes nec- essarily exceeds—by at least eightfold—that in competitive athletes, because non athletes greatly out number students in organized and s anctioned sports programmes.

Well-meaning clinicians and advo- cacy groups have persistently been strong advocates for universal 12-lead electro- cardio graphic testing in young competitive athletes.5,10,15–19,31 In many European coun- tries, in which interest in electrocardiographic screening is greatest, the effort to identify potentially lethal cardiovascular disease has mostly been extended only to the small subgroups of elite or professional athletes at the highest level of performance. Therefore, after considering all viewpoints, we are com- pelled to pose this novel question: is it ethical to restrict cardiovascular screening to only those young people who elect to participate in competitive sports, and in the process deprive others who might be at similar or greater risk of sudden death from access to potentially life-saving clinical evaluations and testing? In 2015, is it appropriate for competitive young athletes to be p rivileged at the expense of other young people?

Future perspectives We wish to emphasize that we do not mean to suggest or justify abandoning long- standin g systematic screening of high school

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Figure 1 | Effect of preparticipation screening on cardiovascular mortality in competitive athletes.37 The graph shows annual athlete mortality per 100,000 person‑years in the Veneto region of Italy (history, physical examination, and 12‑lead electrocardiogram) and Minnesota, USA (history and physical examination only), with the two strategies compared over 21 years (1985–2005). No significant difference exists in mortality between the two populations with the different cardiovascular screening strategies. The Italian national preparticipation screening programme began in 1981. Reprinted from Maron, B. J. et al. Comparison of U.S. and Italian experiences with sudden cardiac death in young competitive athletes and implications for preparticipation screening strategies. Am. J. Cardiol. 104 (2), 276–280 © 2009, with permission from Elsevier.

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NATURE REVIEWS | CARDIOLOGY VOLUME 12 | JUNE 2015 | 377

and college student athletes or others in the USA.6 Indeed, history and physical exami- nation screening have been practised in the USA for >50 years, with proven efficacy in identifying many young individuals with potentially lethal cardiac disease.48 However, consideration should be given to more wide- spread availability of the personal and family history (and possibly physical examination) to those students not engaged in competi- tive sports, using the 14 target elements from the AHA/ACC to raise suspicion of cardio- vascular abnormalities.6 We concede that extending this approach to larger popula- tions of nonathletes would be an ambitious strategy, undoubtedly fraught with logistical

challenges. Nevertheless, a precedent for such a process in large populations does exist. Mandated under the School Health Law in Japan, general population cardio- vascular screening largely with history and physical examination has been performed systematically in thousands of children in the first, seventh, and tenth grades.49,50 However, the reported results are rudimen- tary and do not indicate whether mortality was reduced.

Conclusions In this Perspectives article, we recommend that the ongoing cardiovascular screening debate be refocused beyond the fairly small

population of competitive athletes to other, larger groups of active young people who might also be at risk of sudden premature death. In principle, little ethical justification exists for arbitrarily excluding such people from clinical evaluations that could diag- nose lethal cardiovascular diseases, either because of their decision to forgo partici- pation in competitive sports, or the lack of physical talent to perform in such activi- ties. We suggest devoting greater energy and resources to cardiovascular screening (without noninvasive testing), extended to larger segments of the youthful population beyond competitive athletes, as part of an expanded public-health policy.

Hypertrophic Cardiomyopathy Center, Minneapolis Heart Institute Foundation, Suite 620, 920 East 28th Street, Minneapolis, MN 55407, USA (B.J.M.). Cohen Children’s Medical Center of New York, 269‑01 76th Avenue, New York, NY 11040, USA (R.A.F.). Division of Medical Ethics, NYU Langone Medical Center, 455 1st Avenue, New York, NY 10016, USA (A.C.). Correspondence to: B.J.M. [email protected]

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2. Maron, B. J., Doerer, J. J., Haas, T. S., Tierney, D. M. & Mueller, F. O. Sudden deaths in young competitive athletes: analysis of 1866 deaths in the United States, 1980–2006. Circulation 119, 1085–1092 (2009).

3. Maron, B. J., et al. Sudden death in young competitive athletes: clinical, demographic, and pathological profiles. JAMA 276, 199–204 (1996).

4. Maron, B. J., Haas, T. S., Ahluwalia, A. & Rutten‑Ramos, S. C. Incidence of cardiovascular deaths in Minnesota high school athletes. Heart Rhythm 10, 374–377 (2013).

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

6. Maron, B. J. et al. Assessment of the 12‑lead electrocardiogram as a screening test for detection of cardiovascular disease in general healthy populations of young people (12–25 years of age). J. Am. Coll. Cardiol. 64, 1479–1514 (2014).

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0 1 2 3 Number of deaths per year (×103) 4 5 6 7 8 9 10 11 12 13

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NCAA athletes —CV (forensic)

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Minnesota high school athletes—CV

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Figure 2 | Causes of sudden death in young people (aged <25 years) in the USA.6 *Detectable by electrocardiographic screening. In Denmark, the risk of sudden death from CV disease in young competitive athletes is low (1.5 deaths per year). Abbreviations: CV, cardiovascular; NCAA, National Collegiate Athletic Association. Reprinted from Maron, B. J. et al. Assessment of the 12‑lead ECG as a screening test for detection of cardiovascular disease in healthy general populations of young people (12–25 years of age): a scientific statement from the American Heart Association and the American College of Cardiology. J. Am. Coll. Cardiol. 64 (14), 1479–1514 © 2014, with permission from Elsevier and the American College of Cardiology; and reprinted from Maron, B. J. et al. Assessment of the 12‑lead ECG as a screening test for detection of cardiovascular disease in healthy general populations of young people (12–25 years of age): a scientific statement from the American Heart Association and the American College of Cardiology. Circulation 130 (15), 1303–1334 (2014).

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Author contributions All the authors researched data for the article, contributed to discussion of content, and wrote, reviewed, and edited the manuscript before submission.

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