EXERCISE, SUDDEN DEATH
The sudden death of a competitive athlete is a personal tragedy with great impact on the lay and medical communities(26). Sudden deaths in athletes are usually caused by previously unsuspected cardiovascular disease(1,3,6,11,17,23,31,37,41,42,45,57,59,60,61,62,63,65,67). Such an event often assumes a high public profile because of the generally held perception that trained athletes constitute the healthiest segment of our society. The death of a well-known elite athlete often emphasizes this visibility (26,33). Athletic field catastrophes strike to the core of our sensibilities and often galvanize us. They also inevitably raise a number of practical and ethical issues.
This statement is a response to these considerations and represents the consensus of a panel appointed by the American Heart Association Science Advisory and Co-ordinating Committee. The panel comprised cardiovascular specialists, other physicians with extensive clinical experience with athletes of all ages, and a legal expert. The panel 1) assessed the benefits and limitations of preparticipation screening for early detection of cardiovascular abnormalities in competitive athletes; 2) addressed cost-efficiency and feasibility issues as well as the medical and legal implications of screening; and 3) developed consensus recommendations and guidelines for the most prudent, practical, and effective screening procedures and strategies (the recommendations are listed at the end of this statement). This endeavor seems particularly relevant and timely, given the large number of competitive athletes in this country, recent public health initiatives on physical activity and exercise, and the staging of the 1996 Olympic Games in the United States.
Definitions and Background
The competitive athlete has been described as one who participates in an organized team or individual sport requiring systematic training and regular competition against others while placing a high premium on athletic excellence and achievement (37). The purpose of screening, as described here, is to provide medical clearance for participation in competitive sports through routine and systematic evaluations intended to identify clinically relevant and preexisting cardiovascular abnormalities and thereby reduce the risks associated with organized sports. However, detection of a possible cardiovascular abnormality on a standard screening examination is only the first tier of recognition; referral to a specialist for further diagnostic investigation will probably be required. When a definitive cardiovascular diagnosis is made, the consensus panel guidelines of the 26th Bethesda Conference (34) should be used to formulate recommendations for continued participation or disqualification from competitive sports.
The current guidelines focus primarily on the potential for population-based screening of high school and collegiate athletes rather than individual clinical assessments of athletes and apply to competitors of all ages and both genders. These recommendations may also be extrapolated to athletes in youth, middle school, and masters or professional sports, and in some instances to participants in intense recreational sports or those engaged in careers concerned with public safety (e.g., firefighters, police officers, and airline pilots). It is also recognized that overall preparticipation screening goes well beyond the considerations described here, which are limited to the cardiovascular system.
These recommendations are predicated on the probability that intense athletic training is likely to increase the risk for sudden cardiac death (or disease progression) in trained athletes with clinically important underlying structural heart disease, although at present it is not possible to quantify that risk. Certainly the vast majority of young athletes who die suddenly do so during athletic training or competition(1,41,42,63). Finally, early detection of clinically significant cardiovascular disease through preparticipation screening will in many instances permit timely therapeutic interventions that may prolong life.
Causes of Sudden Death
A variety of cardiovascular abnormalities represent the most common causes of sudden death in competitive athletes(1,3,6,11,17,23,31,33,37,41,42,45,57,59,60,61,62,63,65,67). The precise lesions responsible for athletic field catastrophes differ considerably with regard to age. For example, in youthful athletes (younger than 35 yr) the vast majority of sudden deaths are due to several congenital cardiac malformations (Fig. 1). Hypertrophic cardiomyopathy is the predominant abnormality occurring in about one third of cases (41,42,63). The next most frequent cause is congenital coronary anomalies, particularly anomalous origin of the left main coronary artery from the right sinus of Valsalva(2,55). These deaths occur most commonly in team sports such as basketball and football, which have the highest levels of participation.
Older athletes (35 yr and older) represent a different athletic population because they do not primarily participate in organized team sports but instead focus on individual endeavors such as long-distance running. The vast majority of deaths in middle-aged athletes are caused by atherosclerotic coronary artery disease (59,60,65,67).
Because this statement focuses on the cardiovascular evaluation of athletes, other related medical problems that may cause sudden death, such as cerebral aneurysm, sickle cell trait (19), nonpenetrating blunt chest impact (39), and bronchial asthma are not considered here. Issues related to drug screening also are not considered here, although it is known that ingestion of agents such as cocaine may have severe adverse cardiovascular consequences (16,66). Screening for systemic hypertension, although not regarded as an important cause of sudden unexpected death in young athletes (18), has been addressed.
Prevalence and Scope of the Problem
The design of a screening strategy must take into account the fact that sudden cardiac death in athletes is an infrequent event and that only a small proportion of participants in organized sports in the United States is at risk(5,63).
Indeed, each of the lesions known to be responsible for sudden death in young athletes occurs infrequently in the general population, ranging from the relatively common, such as hypertrophic cardiomyopathy (1:500)(32), to the very rare, such as coronary artery anomalies, arrhythmogenic right ventricular dysplasia, long QT syndrome, or Marfan syndrome, for which reliable estimates of frequency are lacking. Therefore, it is reasonable to estimate that congenital malformations relevant to athletic screening probably account for a combined prevalence of approximately 0.2% in athletic populations.
The large reservoir of competitive athletes in the United States constitutes a major obstacle to screening strategies. There are approximately 4 million competitive high school-age athletes (grades 9-12) in addition to smaller numbers of collegiate (500,000) and professional (5000) athletes. This does not include an unspecified number of youth, middle school, and masters level competitors, for which reliable numbers are not available.
Although the prevalence of athletic field deaths nationally is not known with certainty, it appears to be in the range of 1:100,000 to 1:300,000 high school-age athletes and is disproportionately higher in males(42,63). Among older athletes, available estimates(40,59) suggest that the frequency of sudden cardiac death due principally to coronary artery disease may exceed that of younger athletes (1:15,000 joggers and 1:50,000 marathon runners). Considering such a relatively low prevalence, the heightened awareness and intense interest in sudden death in athletes, often fueled by the news media, are perhaps disproportionate to its actual numerical impact as a public health problem.
There is general consensus that within a benevolent society there is a responsibility on the part of physicians to initiate prudent efforts to identify life-threatening diseases in athletes to minimize cardiovascular risk associated with sport. Specifically, there also appears to be an implicit ethical (and possibly legal) obligation on the part of educational institutions (e.g., high schools and colleges) to implement cost-efficient strategies to ensure that their athletes are not subject to unacceptable medical risks. Despite sufficient resources, it is recognized that there may not be a high motivation among professional teams or athletes to implement cardiovascular screening. This may be due to the economic pressures inherent in such a sports environment, for which athletic participation is a vocation and financial remuneration is often substantial.
The extent to which preparticipation screening efforts can be supported at any level of competitive athletics is mitigated by cost-efficiency considerations, practical limitations, and the awareness that it is not possible to achieve a zero-risk circumstance in competitive sports(30). Indeed, there is often an implied acceptance of risk on the part of athletes. As a society we permit or condone many athletic activities known to have intrinsic risks that cannot be controlled absolutely-e.g., automobile racing or mountain climbing, as well as more traditional competitive sports such as football, in which the possibility of serious traumatic injury exists.
It is important to clearly acknowledge those limitations associated with preparticipation screening in order to 1) inform the public, which might otherwise harbor important misconceptions about the principles and efficacy of athletic screening, and 2) offer appropriate guidance to physicians and healthcare workers responsible for screening.
Although educational institutions and professional sports organizations must use reasonable care in conducting their athletic programs, currently there is no clear legal precedent regarding their duty to require or conduct preparticipation screening of athletes to detect medically significant abnormalities. In the absence of binding requirements established by law or by athletic governing bodies, most institutions and teams rely on their team physician or other medical personnel to determine appropriate medical screening procedures.
A physician who has medically cleared an athlete to participate in competitive sports is not necessarily legally liable for an injury or death caused by an undiscovered cardiovascular condition. Malpractice liability for failure to discover a latent asymptomatic cardiovascular condition requires proof that a physician deviated from customary or accepted medical practice in his or her specialty in performing preparticipation screening of athletes and that use of established diagnostic criteria and methods would have disclosed the medical abnormality.
The law permits the medical profession to establish the appropriate nature and scope of preparticipation screening of athletes based on its collective medical judgment. This necessarily involves the development of reliable diagnostic procedures in light of cost-benefit and feasibility factors. The current guidelines for cardiovascular preparticipation screening of athletes constitute some evidence of the proper medical standard of care; they will establish the legal standard of care if generally accepted or customarily followed by physicians (47) or relied upon by courts in determining the nature and scope of the legal responsibility borne by sponsors of competitive athletes in determining medical fitness.
Current Customary Practice
Currently there are no universally accepted standards for the screening of high school and college athletes, nor are there approved certification procedures for healthcare professionals who perform screening examinations. Some form of medical clearance by a physician or other trained healthcare worker, usually consisting of a history and physical examination, appears to be customary for high school athletes. Standards may be mandated by state legislatures or left to the individual state high school athletic associations or school districts. However, there is no uniform agreement among the states as to the precise format of preparticipation medical clearances; in fact, 11 states do not have a standard medical form, and five do not even require an examination. Some forms are specific, whereas others require only the signature of a physician to clear an athlete to compete in organized sports. In a substantial minority of states, nonphysician healthcare workers are allowed to perform preparticipation screening: chiropractors (10 states) and advanced nurse practitioners or physician assistants (with or without physician supervision, 15 states). Appropriate models of the preparticipation examination have been developed by a number of medical organizations and investigators (7,8,14,56).
Expectations of Standard Screening
Preparticipation screening by history and physical examination alone(without noninvasive testing) is not sufficient to guarantee detection of many critical cardiovascular abnormalities in large populations of young trained athletes. Indeed, hemodynamically significant congenital aortic valve stenosis is probably the lesion most likely to be reliably detected during routine screening because of its characteristically loud heart murmur. Detection of hypertrophic cardiomyopathy by standard screening is unreliable because most patients have the nonobstructive form of this disease, characteristically expressed by only a soft heart murmur or none at all(28,29,34,70). Furthermore, most athletes with hypertrophic cardiomyopathy do not experience syncope or have a family history of premature sudden death due to the disease(35,42).
The standard personal history conveys a generally low specificity for detection of many cardiovascular abnormalities that lead to sudden cardiac death in young athletes, particularly those associated with symptoms such as chest pain or impaired consciousness. In older athletes, however, a personal history of coronary risk factors and a family history of premature ischemic heart disease can be useful for identifying those individuals at risk.
Effectiveness and Limitations of Noninvasive Screening Tests
The addition of noninvasive diagnostic tests to the screening process in young athletes clearly has the potential to enhance detection of certain cardiovascular defects. For example, the two-dimensional echocardiogram is the principal diagnostic tool for clinical recognition of hypertrophic cardiomyopathy, demonstrating otherwise unexplained asymmetric left ventricular wall thickening, the sine qua non of this disease(20,28,29,34,70). Screening for hypertrophic cardiomyopathy with DNA testing for a variety of known mutations in genes encoding proteins of the sarcomere is not yet practical or feasible for large populations, given the substantial genetic heterogeneity of the disease (13,58,68).
Echocardiography can also be expected to detect other relevant abnormalities associated with sudden death in young athletes, such as valvular heart disease, aortic root dilatation, and left ventricular dysfunction (with myocarditis and dilated cardiomyopathy). However, even such diagnostic testing cannot itself guarantee identification of all important lesions, and some diseases may not be detectable with any screening method. For example, identification of many congenital coronary artery anomalies usually requires a sophisticated laboratory examination that includes coronary arteriography, although in selected young athletes it is possible with echocardiography to raise a strong suspicion (or even identify) anomalies such as the left main coronary artery from the right sinus of Valsalva(12,36). Arrhythmogenic right ventricular dysplasia usually cannot be reliably diagnosed solely with echocardiography and electrocardiography; the best available noninvasive test for this disease is magnetic resonance imaging, which is both expensive and not universally available (46,53).
Cost-efficiency issues are important when assessing the feasibility of screening large athletic populations(9,10,49,55,69); however, in the vast majority of instances adequate financial and personnel resources are inadequate for such endeavors. In situations in which the full expense of testing is the responsibility of administrative bodies such as schools, universities, or professional teams, the costs are probably prohibitive, ranging from $400 to $2000 per echocardiographic study (average $600). For example, if the occurrence of hypertrophic cardiomyopathy in a young athletic population is assumed to be 1:500 (32), even at $500 per study it would theoretically cost $250,000 to detect even one previously undiagnosed case.
Screening protocols that incorporate noninvasive testing at greatly reduced costs have been described (49,69); however, these efforts have been in unique circumstances involving donated equipment and professional time for all but technician-related costs. Some investigators have suggested an inexpensive shortened-format echocardiogram for population screening, limited to parasternal views and lasting about 2 min(49,69). Nevertheless, such public service projects based largely on volunteer efforts usually cannot be sustained because of changing priorities for the use of available resources and therefore are unlikely to be implemented on a scale necessary to provide effective screening of all high school and collegiate athletes.
Another important limitation of screening with two-dimensional echocardiography is the potential for false-positive or false-negative results. False-positive results may arise from assignment of borderline values for left ventricular wall thicknesses (or particularly large values for cavity size) that require formulation of a differential diagnosis between the normal physiological adaptations of an athlete's heart(12,25,51) and pathological conditions such as hypertrophic cardiomyopathy or other cardiomyopathies(38). Indeed, such clinical dilemmas (which cannot be definitively resolved in some athletes) generate heavy emotional, financial, and medical burdens for the athlete, family, team, and institution by virtue of the uncertainty created and the requirement for additional testing. False-negative results may occur because the phenotypic expression of hypertrophic cardiomyopathy may not be evident or complete until adolescence(43). Consequently, in selected young athletes (younger than 15 yr) with hypertrophic cardiomyopathy, left ventricular hypertrophy may be absent or mild and echocardiographic findings not diagnostic of that disease (43).
The 12-lead electrocardiogram (ECG) has been proposed as a more practical and cost-efficient alternative to routine echocardiography for population-based screening (21,27). Indeed, the ECG is abnormal in about 95% of patients with hypertrophic cardiomyopathy(44), is frequently abnormal in other potentially lethal lesions such as coronary anomalies (55), and will usually identify the important but uncommon long QT syndrome(48,64). However, recent data indicate that a certain proportion of genetically affected relatives in families with long QT syndrome may have little or no phenotypic expression on the ECG(64).
In preparticipation screening the ECG compares unfavorably with the echocardiogram because of its lack of imaging capability for recognition of structural cardiovascular malformations. The ECG also has a relatively low specificity as a screening test in athletic populations because of the high frequency of electrocardiographic alterations that are associated with the normal physiological adaptations of an athlete's heart to training(71). In screening large populations of older trained athletes, routine use of exercise testing to detect coronary artery disease is limited by its low specificity and pretest probability(4).
To date there have been relatively few published reports of cardiovascular screening efforts in large athletic populations(10,21,22,27,49,54,69). Most of these studies have implemented noninvasive testing (i.e., conventional or limited echocardiogram or 12-lead ECG) in high school or collegiate athletes. The populations screened have ranged in size from 250 to 2000 athletes, who were usually studied over at 1-yr period. In general, few definitive examples of potentially lethal cardiovascular abnormalities were detected. These results are largely consistent with the experience in Italy, where a systematic national program for preparticipation evaluation of athletes (often involving echocardiography) has been in place for more than 30 yr (52).
Perspectives on Race and Gender
Sudden cardiac death in young athletes is a source of concern in the African-American community. While preliminary data suggest that hypertrophic cardiomyopathy is an important cause of sudden death in young African-American competitive athletes (42), reports from selected hospital-based referral populations with hypertrophic cardiomyopathy have rarely included African-Americans. It is possible that this circumstance reflects the limited access of certain high-risk individuals (particularly the poor and disenfranchised) to health care and specifically to athletic screening. Indeed, the likelihood that a disease such as hypertrophic cardiomyopathy will be clinically detected may be different between African-American and white athletes.
Sudden death on the athletic field is uncommon in young women (about 15% of all such deaths). The lower death rate may be explained by lower participation rates of women, different training demands, or cardiac adaptation(50). Hypertrophic cardiomyopathy is also less commonly recognized clinically in women(20,28,29,34,44,70). These observations also suggest the possibility that a measure of protection from sudden death is attributable in some way to gender. Nevertheless, available data do not provide a compelling justification to construct specific screening algorithms based on gender, race, or demographic subgrouping.
The American Heart Association recommends that some form of preparticipation cardiovascular screening for high school and collegiate athletes is justifiable and compelling, based on ethical, legal, and medical grounds. Noninvasive testing can enhance the diagnostic power of the standard history and physical examination; however, it is not prudent to recommend routine use of such tests as 12-lead electrocardiography, echocardiography, or graded exercise testing for detection of cardiovascular disease in large populations of young or older athletes. This recommendation is based on both practical and cost-efficiency considerations, given the large number of competitive athletes in the United States, the relatively low frequency with which the cardiovascular lesions responsible for these deaths occur, and the low rate of sudden cardiac death in the athletic community. This viewpoint, however, is not intended to actively discourage all efforts at population screening that may be proposed by individual investigators. Nevertheless, there is concern that the widespread use of noninvasive testing in athletic populations could result in many false-positive test results, creating unnecessary anxiety among substantial numbers of athletes and their families, as well as unjustified exclusion from life insurance coverage and athletic competition. Indeed, in such a circumstance with a low incidence of disease in the community, a great likelihood exists that the number of false-positive results would exceed that of true-positive results(4).
Consequently, we conclude that a complete and careful personal and family history and physical examination designed to identify (or raise suspicion of) those cardiovascular lesions known to cause sudden death or disease progression in young athletes is the best available and most practical approach to screening populations of competitive sports participants, regardless of age. Such cardiovascular screening is an obtainable objective and should be mandatory for all athletes. We recommend that both a history and a physical examination be performed before participation in organized high school (grades 9 through 12) and collegiate sports. Screening should then be repeated every 2 yr. In intervening years an interim history should be obtained. Indeed, this recommendation is consistent with procedures that are customary for most high school and collegiate athletes in the United States.
However, it is important to point out that official recommendations or requirements by athletic governing bodies regarding the nature and scope of preparticipation medical evaluations of athletes are not standardized among the states, nor can they necessarily be viewed as medically sufficient in many instances. Therefore, because of this heterogeneity in the design and content of preparticipation examinations, we also recommend developing a national standard for preparticipation medical evaluations. Adherence to uniformly applicable guidelines would have a substantial and cost-effective impact on the health of student athletes by enhancing the safety of athletic activities.
Despite the limitations of the history and physical examination in detecting coronary artery disease in older athletes (over 35 yr), a personal history of coronary risk factors or a family history of premature ischemic heart disease may be useful for identifying that disease with screening and therefore should be performed before initiating competitive exercise. In addition, it is prudent to selectively perform medically supervised exercise stress testing in men older than 40 (and women older than 50) who wish to engage in regular physical training and competitive sports if the examining physician suspects occult coronary artery disease on the basis of risk factors, whether multiple (two or more, other than age and gender), or single but markedly abnormal. Older athletes should also be warned specifically about prodromal cardiovascular symptoms such as exertional chest pain.
These guidelines should not promulgate a false sense of security on the part of medical practitioners or the general public because the standard history and physical examination intrinsically lack the capability to reliably identify many potentially lethal cardiovascular abnormalities. Indeed, it is an unrealistic expectation that large-scale standard athletic screening can reliably exclude most important cardiac lesions.
Preparticipation sports examinations are at present performed by various paid or volunteer physicians or non-physician healthcare workers with different training and experience. Examiners may be associated with or administratively independent of an institution, school, or team.
Consequently, we strongly recommend that athletic screening be performed by a healthcare worker with the requisite training, medical skills, and background to reliably obtain a detailed cardiovascular history, perform a physical examination, and recognize heart disease. While it is preferable that such an individual be a licensed physician, this may not always be feasible, and under certain circumstances it may be acceptable for an appropriately trained registered nurse or physician assistant to perform the screening examination. In states in which nonphysician healthcare workers(including chiropractors) are permitted to perform preparticipation screening, it will be necessary to establish a formal certification process to demonstrate expertise in performing cardiovascular examinations.
Specifically, athletic screening evaluations should include a complete medical history and physical examination, including brachial artery blood pressure measurement. This examination should be conducted in an environment conducive to optimal cardiac auscultation, whether performed in a private office or as part of a school program. The evaluation should also emphasize certain elements critical to the detection of cardiovascular diseases known to be associated with morbidity or sudden cardiac death in athletes.
The cardiovascular history should include key questions designed to determine 1) prior occurrence of exertional chest pain/discomfort or syncope/near-syncope as well as excessive, unexpected, and unexplained shortness of breath or fatigue associated with exercise; 2) past detection of a heart murmur or increased systemic blood pressure; and 3) family history of premature death (sudden or otherwise), or significant disability from cardiovascular disease in close relative(s) younger than 50 yr old or specific knowledge of the occurrence of certain conditions (e.g., hypertrophic cardiomyopathy, dilated cardiomyopathy, long QT syndrome, Marfan syndrome, or clinically important arrhythmias). These recommendations are offered with the awareness that the accuracy of some responses elicited from young athletes may depend on their level of compliance and historical knowledge. Indeed, parents should be responsible for completing the history forms for high school athletes.
The cardiovascular physical examination should emphasize (but not necessarily be limited to) 1) precordial ausculation in both the supine and standing positions to identify, in particular, heart murmurs consistent with dynamic left ventricular outflow obstruction; 2) assessment of the femoral artery pulses to exclude coarctation of the aorta; 3) recognition of the physical stigmata of Marfan syndrome; and 4) brachial blood pressure measurement in the sitting position.
As noted previously, when cardiovascular abnormalities are identified or suspected, the athlete should be referred to a cardiovascular specialist for further evaluation and/or confirmation. Definitively identified cardiovascular abnormalities should be judged with respect to the 26th Bethesda Conference consensus panel guidelines for the final determination of eligibility for future athletic competition (34).
Figure 1-Causes of sudden cardiac death in young competitive athletes (median age 17), based on systematic tracking of 158 athletes in the United States, primarily from 1985 to 1995. Ao indicates aorta; LAD, left anterior descending coronary artery; AS, aortic stenosis; C-M, cardiomyopathy; ARVD, arrhythmogenic right ventricular dysplasia; MVP, mitral valve prolapse; CAD, coronary artery disease; HCM, hypertrophic cardiomyopathy; 173, increased. Adapted from Maron et al.
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A statement for health professionals from the Sudden Death Committee and Congenital Cardiac Defects Committee, American Heart Association.
Writing Group: Barry J. Maron, Chair, Paul D. Thompson, James C. Puffer, Christopher A. McGrew, William B. Strong, Pamela S. Douglas, Luther T. Clark, Matthew J. Mitten, Michael H. Crawford, Dianne L. Atkins, David J. Driscoll, Andrew E. Epstein.
The American Academy of Pediatrics Section on Cardiology supports the recommendations of this statement. Endorsed by the Board of Trustees of the American College of Cardiology.
Endorsed by the Board of Trustees of the American College of Sports Medicine.