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RISK PROFILES AND CARDIOVASCULAR PREPARTICIPATION SCREENING OF COMPETITIVE ATHLETES
THE ATHLETE’S HEART AND CARDIOVASCULAR DISEASE
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RISK PROFILES AND CARDIOVASCULAR PREPARTICIPATION SCREENING OF COMPETITIVE ATHLETES Barry J. Maron, MD
Sudden deaths of competitive athletes are personal tragedies with great impact on the lay and medical communitiesz7that are usually due to a variety of previously unsuspected cardiovascular diseases.* Such events often assume a high public profile because of the generally held perception that trained athletes constitute the healthiest segment of society, with the deaths of well-known elite 34 athletes often exaggerating this vi~ibility.~~, Although these athletic field catastrophes strike to the core of sensibilities and often galvanize society, they also inevitably raise a number of practical and ethical issues. In response to these considerations, an American Heart Association consensus panel was composed of a number of cardiovascular specialists and other physician experts having extensive clinical experience with athletes of all ages as well as a legal
The present text is reproduced with some adaptation from Maron BJ, Thompson PD, Puffer JC, et al: American Heart Association Medical/Scientific Statement: Cardiovascular preparticipation screening of competitive athletes. Circulation 94:850-856, 1996; with permission of the American Heart Association. *References 1, 3, 6, 11, 17, 24, 32, 36, 42, 47, 61, 6347, 69, 71.
expert. This 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 medicolegal implications of screening; and (3) developed consensus recommendations and guidelines for the most prudent, practical, and effective screening procedures and strategies. It seems particularly relevant to reproduce those concepts here given the large number of competitive athletes in the United States and public health initiatives on physical activity and exercise. DEFINITIONS AND BACKGROUND
This discussion focuses on the competitive athlete, previously 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 a ~ h i e v e m e n tThe . ~ ~ 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
From the Cardiovascular Research Division, Minneapolis Heart Institute Foundation, Minneapolis, Minnesota
CARDIOLOGY CLINICS VOLUME 15 * NUMBER 3 * AUGUST 1997
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thereby reduce the risks associated with organized sports. Raising the possibility of a cardiovascular abnormality on a standard screening examination is, however, only the first tier of recognition, after which referral to a specialist for further diagnostic investigation is probably required. When a definitive cardiovascular diagnosis is made, the consensus panel guidelines of Bethesda Conference #2637 should be used to formulate recommendations for continued participation or disqualification from competitive sports. The present guidelines focus primarily on the potential for population-based screening of high school and collegiate student athletes rather than individual clinical assessments of athletes and are designed to apply to competitors of all ages and both genders. Also, these recommendations may be extrapolated to athletes in youth, middle-school, masters, or professional sports and in some instances to participants in intense recreational sporting activities. It is also recognized that overall preparticipation screening goes well beyond the considerations described here, which are limited to the cardiovascular system, and involves many other organ systems and medical issues. 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 presently 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, although a minority of deaths occur independent of exercise.41,42, 67 Finally, the early detection of clinically significant cardiovascular disease through preparticipation screening in many instances permits timely therapeutic interventions that may prolong life. CAUSES OF SUDDEN DEATH IN ATHLETES
A variety of cardiovascular abnormalities represent the most common causes of sudden death in competitive athletes.* The precise lesions responsible for athletic field catastrophes differ considerably with regard to age. For example, in youthful athletes (<35 years of age), the vast majority are due to a variety *References 1, 3, 6, 11, 17, 24, 32, 41, 42, 47, 61, 6347, 69, 71.
of largely congenital cardiac malformations 42, 67 Virtually any disease capable of (Fig. l).41, causing sudden death in young people potentially may do so in young competitive athletes. Although these cardiovascular diseases may be relatively common in young athletes dying suddenly, each is uncommon in the general population. Also, the lesions responsible for sudden death do not occur with the same frequency, with most responsible for only 5% or less of all deaths (see Fig. 1). The single most common cardiovascular abnormality among the causes of sudden death in young athletes is hypertrophic cardiomyopathy, usually in the nonobstructive form30,41, 42, 67 and with a prevalence in the range of 35% (see Fig. 1).Hypertrophic cardiomyopathy is a primary and familial cardiac malformation with heterogeneous expression, complex pathophysiology, and diverse clinical course for which several disease-causing mutations in four genes encoding proteins of the cardiac sarcomere have been reported.60Hypertrophic cardiomyopathy is a relatively uncommon malformation occurring in about 0.2% of the general populati~n.~~ The next most frequent cause of sudden death is a variety of congenital coronary anomalies, particularly anomalous origin of the left main coronary artery from the right (anterior) sinus of Valsalva.2,58 Less common causes are myocarditis, dilated cardiomyopathy, Marfan’s syndrome with aortic rupture, arrhythmogenic right ventricular dysplasia, sarcoidosis, mitral valve prolapse, aortic valve stenosis, atherosclerotic coronary artery disease, long QT syndrome, and possibly intramural (tunneled) coronary arteries. These deaths occur most commonly in intense team sports, such as basketball and football, which also have the highest levels of participation. Older athletes (> age 35) represent a different athletic population because they do not participate primarily in organized team sports but rather focus on individual endeavors, such as long distance running. Furthermore, the vast majority of deaths in middle-aged athletes are due to atherosclerotic coronary artery disease63,64, 69, 71 and only rarely to congenital diseases such as hypertrophic cardiomyopathy or coronary artery anomalies. Because this discussion focuses on the cardiovascular evaluation of athletes, other related medical problems that may occasionally cause sudden death in the young, such as cerebral aneurysm, sickle cell trait,19nonpene-
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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, from 1985 to 1995. Ao = Aorta; ARVD = arrhythmogenic right ventricular dysplasia; LAD = left anterior descending; AS = aortic stenosis; MVP = mitral valve prolapse; CAD = coronary artery disease; HCM = hypertrophic cardiomyopathy. (Adapted from Maron BJ, Shirani J, Poliac L, et al: Sudden death in young competitive athletes: Clinical demographic and pathological profiles. JAMA 276:199-204, 1996; with permission.)
trating blunt chest impact,39 or bronchial asthma, have been excluded from the present considerations. Also, issues related to drug screening are not discussed here, although it is known that the ingestion of agents such as cocaine may have important adverse cardiovascular consequences.16,20, 70 Screening for systemic hypertension, although not regarded as an important cause of sudden unexpected death in young athletes,18has been addressed. PREVALENCE AND SCOPE OF THE PROBLEM
Relevant to the design of any screening strategy is the fact that sudden cardiac death in athletes is a devastating but rather infrequent event, and only a small proportion of participants in organized sports in the United 67 ~ Each States are at r i ~ k . ~ , ~ ,of the lesions known to be responsible for sudden death in young athletes occurs infrequently in the general population, ranging from the relatively common (e.g., hypertrophic cardiomyopathy) to the apparently very rare (e.g., cor-
onary artery anomalies, arrhythmogenic right ventricular dysplasia, long QT syndrome, or Marfan’s syndrome), for which reliable estimates of frequency are lacking. It is reasonable to estimate that congenital malformations relevant to athletic screening may account for a combined prevalence of only 0.3% or less in general athletic populations. The large reservoir of competitive athletes in the United States constitutes another major obstacle to screening strategies. At present, there are approximately 5 million competitive athletes at the high school level (grades 9 through 12), in addition to lesser 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 whom reliable numbers are not presently available. Although the national prevalence of athletic field deaths owing to cardiovascular disease is not known with certainty, it appears to be in the approximate range of 1 in 50,000 to 1 in 100,000 athletes of high school age, although disproportionately higher in males.44 In older athletes, available esti-
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mates40,64 suggest the frequency of sudden cardiac death, principally owing to coronary artery disease (1 in 15,000 joggers and 1 in 50,000 marathon runners), may exceed somewhat that in younger athletes. Considering such a relatively low prevalence, the heightened awareness and intense interest in sudden deaths in athletes, often fueled by the news media, is perhaps disproportionate to their actual numerical impact as a public health problem. ETHICAL CONSIDERATIONS IN SCREENING
There is a general consensus that within a benevolent society, a responsibility exists on the part of physicians to initiate prudent efforts for the identification of life-threatening diseases in athletes, for the purpose of minimizing the 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-effective strategies to ensure that their student athletes are not subject to unacceptable and unavoidable medical risks. Despite sufficient resources, it is recognized that a high motivation to implement cardiovascular screening may not presently exist on the part of professional teams or athletes because of the economic pressures inherent in such a sports environment for which athletic participation represents a vocation and remuneration for services 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.31 There is often implied acceptance of risk on the part of athletes; society permits or condones 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 acknowledge the limitations associated with preparticipation screening to (1) create an informed public that might otherwise harbor important misconceptions regarding the principles and efficacy of athletic screening and (2) offer appropriate
guidance to physicians and health care workers responsible for screening. LEGAL CONSIDERATIONS
Although educational institutions and professional teams must use reasonable care in conducting their athletic programs, there currently is no clear legal precedent regarding their duty to require or conduct preparticipation screening of athletes for the purpose of detecting medically significant abnormalities. At present, no lawsuits have apparently been brought forward alleging negligence in the failure either to perform cardiovascular screening or to diagnose cardiac disease in young competitive athletes. In the absence of binding requirements established by state law or athletic governing bodies, most institutions and teams presently rely on their team physician or other medical personnel to determine the appropriate medical screening procedures. At present, 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 undetected 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 utilization of established diagnostic criteria and techniques would have disclosed the subject’s medical condition. The law permits the medical profession to establish the appropriate nature and scope of preparticipation screening of athletes based on the exercise of its collective medical judgment. This necessarily involves the development of reliable diagnostic procedures in light of cost-benefit and feasibility factors. The present guidelines for cardiovascular preparticipation screening of athletes are some evidence of the proper medical standard of care; they establish the legal standard of care if generally accepted or customarily followed by physicians49 or relied on by courts in determining the nature and scope of the legal responsibility borne by sponsors of competitive athletes in determining their medical fitness. CURRENT CUSTOMARY PRACTICE
Currently, there are no universally accepted standards for the screening of high
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school and college athletes, and there are no approved certification procedures for health care professionals who perform such screening examinations. Some form of medical clearance by a physician or other trained health care worker, usually consisting of a history and physical examination, presently appears most customary for high school athletes. Standards may be mandated by state legislative action or left to the individual state high school athletic associations or school districts. There is no uniform agreement among the states, however, as to the precise format of preparticipation medical evaluations and clearances; in fact, not all states require this process or have a recommended standard medical form. Some of. the available forms are specific, whereas others require only the signature of a physician to provide clearance for the athlete to compete in organized sports. In a substantial minority of states, nonphysician health care workers are sanctioned to perform preparticipation screening, including chiropractors (in 11 states) and advanced nurse-practitioners or physician’s assistants, with or without physician supervision, (in 16 states). Useful models for the preparticipation examination have been developed by a number of medical organizations or investigators.7,8,14.59 EXPECTATIONS OF STANDARD SCREENING PROCEDURES
Preparticipation screening by history and physical examination alone (without noninvasive testing) does not have sufficient power to guarantee detection of many critical cardiovascular abnormalities in large populations of young trained athletes. 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 the standard screening examination is unreliable because most patients have the nonobstructive form of this disease, characteristically expressed by no or only a soft heart murmur.25, 30, 60, 74 Furthermore, most athletes with hypertrophic cardiomyopathy do not experience syncope or have a family history of premature sudden death as a result of their disease.28,42 The standard personal history conveys a generally low specificity for the detection of 297
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many cardiovascular abnormalities that lead to sudden cardiac death in young athletes, particularly when symptoms such as chest pain or impaired consciousness are involved. 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 at-risk individuals. EFFECTIVENESS AND LIMITATIONS OF NONINVASIVE SCREENING TESTS
In young athletes, the addition of noninvasive diagnostic tests to the screening process clearly has the potential to enhance the detection of certain cardiovascular defects. For example, the two-dimensional echocardiogram is the principal diagnostic tool for clinical recognition of hypertrophic cardiomyopathy by demonstrating otherwise unexplained asymmetric left ventricular wall thickening, the sine qua non of this disease.21,25, 29, 74 Comprehensive and routine screening for hypertrophic cardiomyopathy with genetic testing for a variety of known mutations is not yet practical or feasible for large populations, given the substantial genetic heterogeneity of the disease and the expensive and time-intensive 60, 72 methodologies in~olved.’~, Echocardiography could also be expected to detect other relevant abnormalities associated with sudden death in young athletes, such as valvular heart disease (e.g., mitral valve prolapse), aortic root dilation, and left ventricular dysfunction (in myocarditis or dilated cardiomyopathy). Even such diagnostic testing cannot itself, however, guarantee identification of all important lesions, and some diseases may be beyond detection with any screening methodology. For example, identification of many congenital coronary artery anomalies usually requires sophisticated laboratory examination, including coronary arteriography, although it is possible in selected young athletes to raise a strong suspicion of (or even identify) anomalies such as left main coronary artery from the right sinus 28, 35 Arof Valsalva with echocardiography.12, rhythmogenic right ventricular dysplasia usually cannot be reliably diagnosed solely with echocardiography and electrocardiogram (ECG); the best available noninvasive test for this disease appears to be magnetic resonance imaging, which is both expensive and not universally available.48,56
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Cost-efficiency issues are important when assessing the feasibility of applying expensive testing to the screening of large athletic populations’, 51, 57, 73 (in the vast majority of instances, adequate financial and personnel resources are lacking for such endeavors). In those situations in which the full (i.e., unreduced) expense of testing would be the responsibility of administrative bodies such as a school, university, or team, the costs are probably prohibitive, ranging from about $400 to $2000 per echocardiographic study (average about $600). For example, if the occurrence of hypertrophic cardiomyopathy in a young athletic population is assumed to be as common as 1 in 500,33 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 cost have been describeds1,73; however, these efforts have been in unique circumstances in which equipment was donated and professional expenses were waived for all but technicianrelated costs. Some investigators have suggested an inexpensive shortened-format echocardiogram for population screening (limited to parasternal views, about 2 minutes in duration).”, 73 Nevertheless, such public service projects, based largely on volunteerism, usually cannot be sustained on a consistent basis because priorities in the utilization of available resources may change and therefore are unlikely to be implemented on a scale necessary to provide effective screening to all high school and collegiate athletes. Another important limitation of screening with two-dimensional echocardiography is the potential for false-positive or false-negative test results. False-positive results may arise from the assignment of borderline Values for left ventricular wall thicknesses (or particularly large values for cavity size), which require formulation of a differential diagnosis between the normal physiologic adaptations of athlete’s heart*s,26, 5s and pathologic conditions such as hypertrophic cardiomyopathy or other cardiomy~pathies.~~ Such clinical dilemmas (which may not always be definitively resolvable in individual 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 screening results may occur when encountering athletes with hypertrophic cardiomyopathy at a point of in-
complete phenotypic expression during adol e ~ c e n c e .Consequently, ~~ in selected young athletes with hypertrophic cardiomyopathy (< age 16), left ventricular hypertrophy may be absent or mild and therefore the echocardiographic findings not yet diagnostic of that disease.43 The 12-lead ECG has been proposed as a more practical and cost-efficient alternative to routine echocardiography for populationbased screening.22,2y The ECG is abnormal in about 95% of patients with hypertrophic cardiomyopathy,46may be abnormal in other potentially lethal lesions such as the coronary anomalies? 24, 28 and usually identifies the important (but uncommon) long QT syndrome.sO, Data indicate, however, that a certain proportion of genetically affected relatives in families with long QT syndrome may have little or no phenotypic expression on ECG.68 In preparticipation screening, the ECG suffers in comparison to the echocardiogram by its lack of imaging capability for recognition of structural cardiovascular malformations. Also the ECG has relatively low specificity as a screening test in athletic populations because of the high frequency with which ECG alterations occur in association with the normal physiologic adaptations of the athlete’s heart to training.7s Elite athletes not infrequently demonstrate distinctly abnormal ECG patterns consistent with pathologic conditions,52 even in the absence of structural heart disease and without evidence of a morphologic adaptation to training. In screening large populations of older trained athletes, the routine application of exercise testing to detect coronary artery disease is limited by its low specificity and pretest pr~bability.~ To date, there have been relatively few published reports of cardiovascular screening efforts in large athletic populations.’”,14,22, 23, 29, 4 5 , sl, 57 Most of these studies have implemented noninvasive testing (i.e., conventional or limited echocardiographic examination or 12-lead ECG) in young high school or collegiate athletes. The populations screened have ranged in size from 250 to 2000 athletes, usually studied over a 1-year period. In general, these reports are consistent by virtue of describing the detection of few definitive examples of potentially lethal cardiovascular abnormalities. This is also largely consistent with the experience in Italy, where a systematic national program for the preparticipation evaluation of athletes (often involving echo-
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cardiography) has been in place for more than 30 years.53 PERSPECTIVES ON RACE AND GENDER
Hypertrophic cardiomyopathy is an important cause of sudden death in young African-American athletes.', 42 The substantial occurrence of hypertrophic cardiomyopathy-related sudden death in young African-American male athletes contrasts sharply with the infrequent reporting of AfricanAmerican patients with hypertrophic cardiomyopathy in hospital-based populations. Therefore, in African-Americans, hypertrophic cardiomyopathy is most frequently encountered when it results in sudden and unexpected death during competitive athletics. These data emphasize the disproportionate access to subspecialty health care between the African-American and white communities in the United States, which makes it less likely for young African-American men to receive a relatively sophisticated cardiovascular diagnosis such as hypertrophic cardiomyopathy compared to their white counterparts. Consequently, it appears that African-American athletes with hypertrophic cardiomyopathy are less likely to be disqualified from competition, in accordance with the recommendations of Bethesda Conference #26,37 to reduce their risk for sudden death. Sudden death on the athletic field is uncommon in young women4* (comprising about 10% to 15% of all such deaths), which may be explained not only on the basis of lower participation rates or less severe training demands and cardiac adaptation54 in some instances, but also because hypertrophic cardiomyopathy is less commonly recognized clinically in women.25,30, 46, 74 This observation also suggests 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. SCREENING RECOMMENDATIONS Advisability
The 1996 American Heart Association recommendations state that some form of pre-
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participation cardiovascular screening for high school and college student athletes is justifiable and compelling based on ethical, legal, and medical Noninvasive testing can enhance the diagnostic power of the standard history and physical examination; however, it is not prudent to recommend the routine use of tests such as 12-lead ECG, echocardiography, or graded exercise testing for the detection of cardiovascular disease in large populations of youthful or older athletes. This view 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 is not, however, intended to discourage all efforts at population screening that may be proposed by individual investigators. Nevertheless, there is concern that the widespread application of noninvasive testing to athletic populations could result in many false-positive results, creating unnecessary anxiety among substantial numbers of athletes and their families as well as unjustified exclusion from competition. 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^.^ Consequently, it appears that a complete and careful personal and family history and physical examination designed to identify (or raise suspicion of) 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. It is recommended that both a history and a physical cardiovascular examination be performed before the initial engagement in organized high school (grades 9 through 12) and collegiate sports and subsequently repeated every 2 years. In intervening years, an interim history should be obtained. For young competitive athletes, this recommendation is consistent with procedures that are customary for most high school and college athletes in the United States. Official recommendations or requirements by athletic governing bodies regarding the nature and scope of preparticipation medical
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evaluations of athletes are not standardized among the states, and they necessarily cannot be viewed as medically sufficient in many instances. Therefore, because of this heterogeneity in the design and content of preparticipation examinations, it is also recommended that a systematic national standard for preparticipation medical evaluations be developed. Adherence to uniformly applicable guidelines would have a substantial impact on the health of student athletes, in a costeffective manner, by enhancing the safety of their athletic activities. For older athletes (>35 years of age), despite the limitations of the history and physical examination in detecting coronary artery disease, a personal history of coronary risk factors or familial occurrence of premature ischemic heart disease may be useful for identification of that disease in a screening setting and therefore should be performed before initiating competitive exercise. In addition, it is prudent to perform medically supervised exercise stress testing selectively in men over age 40 (women over age 50) who wish to engage in habitual physical training and competitive sports should the examining physician suspect occult coronary artery disease on the basis of risk factors, either 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. The present guidelines should not promulgate a false sense of security on the part of medical practitioners or the general public. The standard history and physical examination intrinsically lacks the power to identify reliably many potentially lethal cardiovascular abnormalities. It is, therefore, an unrealistic expectation that large-scale standard athletic screening examinations can exclude most important cardiac lesions. Methodology
Preparticipation sports examinations are presently performed by a variety of individuals, including paid or volunteer physicians or nonphysician health care workers with variable training and experience. Examiners may be associated with, or administratively independent of, the concerned institution, school, or team.
Consequently, athletic screening should be performed by an appropriately trained health care worker with the requisite training, medical skills, and background to perform reliably a detailed cardiovascular history and physical examination and to recognize heart disease. Although 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 health care workers (including chiropractors) are permitted to perform preparticipation screening, it is necessary to establish a formal certification process to demonstrate expertise in performing cardiovascular examinations. Specifically, athletic screening evaluations should comprise a complete medical history and physical examination, including brachial artery blood pressure measurement. This examination should be conducted in a physical environment conducive to optimal cardiac auscultation, whether performed individually in a private office or in a station-format 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 from the athlete: (1) prior occurrence of exertional chest pain or discomfort or syncope (or nearsyncope) as well as excessive, unexpected, and unexplained shortness of breath or fatigue associated with exercise; (2) past recognition of a heart murmur or increased systemic blood pressure; and (3) family history of premature death (sudden or otherwise) or morbidity from cardiovascular disease in close relative(s) younger than age 50 or specific knowledge of the occurrence of certain conditions in family members (e.g., hypertrophic cardiomyopathy, dilated cardiomyopathy, long QT syndrome, Marfan's syndrome, or clinically important arrhythmias). These recommendations are offered recognizing that the accuracy of some responses elicited from young athletes may depend on their level of compliance and historical knowledge. Parents should be responsible for completing the history form of high school athletes. The cardiovascular physical examination should emphasize (but not necessarily be lim-
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ited to (1) precordial auscultation in both the supine and the standing positions to identify, in particular, heart murmurs consistent with 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’s 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 specialist for further evaluation and confirmation. Definitively identified cardiovascular abnormalities should be judged with respect to the Bethesda Conference #26 consensus panel guidelines regarding the final determination of eligibility for future athletic c ~ m p e t i t i o n . ~ ~
References 1. Burke AP, Farb V, Virmani R, et al: Sports-related and non-sports-related sudden cardiac death in young adults. Am Heart J 121:568-575, 1991 2. Cheitlin MD, De Castro CM, McAllister H A Sudden death as a complication of anomalous left coronary origin from the anterior sinus of Valsalva: A not-sominor congenital anomaly. Circulation 50:780-787, 1974 3. Corrado D, Thiene G, Nava A, et al: Sudden death in young competitive athletes: Clinicopathologic correlations in 22 cases. Am J Med 89:588-596, 1990 4. Diamond GA, Forrester JS: Analysis of probability as an aid in the clinical diagnosis of coronary artery disease. N Engl J Med 300:1350-1358, 1979 5. Driscoll DJ, Edwards ED: Sudden unexpected death in children and adolescents. J Am Coll Cardiol 5:118B-l21B, 1985 6. Drory Y, Turetz Y, Hiss Y, et al: Sudden unexpected death in persons (40 years of age. Am J Cardiol 68:1388-1392, 1991 7. DuRant RH, Seymore C, Linder C, et al: The preparticipation examination of athletes: Comparison of single and multiple examiners. Am J Dis Child 139:657661, 1985 8. Dyment PG (ed): Sports Medicine: Health Care for Young Athletes, ed 2. Elk Grove Village, IL, American Academy of Pediatrics, 1991 9. Epstein SE, Maron BJ: Sudden death and the competitive athlete: Perspectives on preparticipation screening studies. J Am Coll Cardiol 7220-230, 1986 10. Feinstein RA, Colvin E, Oh MK: Echocardiographic screening as part of a preparticipation examination. Clin J Sports Med 3:149-152,1993 11. Furlanello F, Bettini R, Cozzi F, et al: Ventricular arrhythmias and sudden death in athletes. Ann NY Acad Sci 427253-279,1984 12. Gaither NS, Rogan KM, Stajduhar K, et al: Anomalous origin and course of coronary arteries in adults: Identification and improved imaging utilizing transesophageal echocardiography. Am Heart J 1226975, 1991 13. Geisterfer-Lowrance AAT, Kass S, Tanigawa G, et al:
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death in competitive athletes. J Am Coll Cardiol 7:204-214, 1986 33. Maron BJ, Gardin JM, Flack JM, et al: Assessment of the prevalence of hypertrophic cardiomyopathy in a general population of young adults: Echocardiographic analysis of 4111 subjects in the CARDIA Study. Circulation 92:785-789, 1995 34. Maron BJ, Garson A: Arrhythmias and sudden cardiac death in elite athletes. Cardiol Rev 2:26-32, 1994 35. Maron BJ, Leon BJ, Swain JA, et al: Prospective identification by two-dimensional echocardiography of anomalous origin of the left main coronary artery from the right sinus of Valsalva. Am J Cardiol 68:140-142, 1991 36. Maron BJ, Mitchell JH: Revised eligibility recommendations for competitive athletes with cardiovascular abnormalities [introduction to Bethesda Conference #26.] J Am Coll Cardiol 24:848-850, 1994 37. Maron BJ, Mitchell JH: 26th Bethesda Conference: Recommendations for determining eligibility for competition in athletes with cardiovascular abnormalities. J Am Coll Cardiol 24:845-899, 1994 38. Maron BJ, Pelliccia A, Spirito P: Cardiac disease in young trained athletes: Insights into methods for distinguishing athlete’s heart form structural heart disease with particular emphasis on hypertrophic cardiomyopathy. Circulation 91:1596-1601, 1995 39. Maron BJ, Poliac L, Kaplan JA, et al: Blunt impact to the chest leading to sudden death from cardiac arrest during sports activities. N Engl J Med 333:337-342, 1995 40. Maron BJ, Poliac JC, Roberts WO: Risk for sudden cardiac death associated with marathon running. Am J Cardiol 799340-841, 1997 41. Maron BJ, Roberts WC, McAllister HA, et al: Sudden death in young athletes. Circulation 62:218-229, 1980 42. Maron BJ, Shirani J, Poliac LC, et al: Sudden death in young competitive athletes: Clinical, demographic and pathological profiles. JAMA 276:199-204, 1996 43. Maron BJ, Spirito P, Wesley YE, et al: Development and progression of left ventricular hypertrophy in children with hypertrophic cardiomyopathy. N Engl 1 Med 315:610414, 1986 44 Maron BJ, Stead D, Aeppli D: Prevalence of sudden cardiac death during competitive sports activities in interscholastic athletes in Minnesota. Circulation 94:I388, 1996 45. Maron BJ, Thompson PD, Puffer JC, et al: Cardiovascular preparticipation screening of competitive athletes. Circulation 945350456, 1996 46. Maron BJ, Wolfson JK, Cird E, et al: Relation of electrocardiographic abnormalities and patterns of left ventricular hypertrophy identified by two-dimensional echocardiography in patients with hypertrophic cardiomyopathy. Am J Cardiol 51:189-194, 1983 47. McCaffrey FM, Braden DS, Strong WB: Sudden cardiac death in young athletes: A review. Am J Dis Child 145:177-183, 1991 48. McKenna WJ, Thiene G, Nava A, et al: Diagnosis of arrhythmogenic right ventricular dysplasia/cardiomyopathy. Br Heart J 71:215-218, 1994 49. Mitten MJ: Team physicians and competitive athletes: Allocating legal responsibility for athletic injuries. U Pitt Law Rev 55:129-169, 1993 50. Moss AJ, Schwartz PJ, Crampton RS, et al: The long QT syndrome: Prospective longitudinal study of 32u8 families. Circulation 84:1136-1144, 1991 51. Murry PM, Cantwell JD, Heith DL, et al: The role of
limited echocardiography in screening athletes. Am
J Cardiol 76:849-850, 1995 52. Pelliccia A, Cullasso F, Di Paolo FM, et al: Clinical significance of abnormal electrocardiographic patterns in elite athletes: The impact of gender and cardiac morphologic adaptations to training [abstr]. Circulation 945-326, 1996 53. Pelliccia A, Maron BJ: Preparticipation cardiovascular evaluation of the competitive athlete: Perspectives from the 30 year Italian experience. Am J Cardiol 75~827-831,1995 54. Pelliccia A, Maron BJ, Culasso F, et al: The athlete’s heart in women: Echocardiographic characterization of 600 highly trained and elite female athletes. JAMA 276~211-215,1996 55. Pelliccia A, Maron BJ, Spataro A, et al: The upper limit of physiologic cardiac hypertrophy in highly trained elite athletes. N Engl J Med 324:295-301, 1991 56. Ricci C, Longo R, Pagnan L, et al: Magnetic resonance imaging in right ventricular dysplasia. Am J Cardiol 70~1589-1595,1992 57. Risser WL, Hoffman HM, Gordon BG Jr, et al: A cost-benefit analysis of preparticipation sports examination of adolescent athletes. J School Health 55:270273, 1985 58. Roberts WC: Congenital coronary arterial anomalies unassociated with major anomalies of the heart or great vessels. In Roberts WC (ed): Adult Congenital Heart Disease. Philadelphia, FA Davis, 1987, p 583 59. Smith DM, Kovan JR, Rich BSE, et al: Preparticipation Physical Evaluation, ed 2. Minneapolis, Phys Sports Med, 1997 60. Spirito P, Seidman CE, McKenna WJ, et al: The management of hypertrophic cardiomyopathy. N Engl J Med 336:775-785,1997 61. Thiene G, Nava A, Corrado D. et al: Rieht ventricular cardiomyopathy and sudden death in young people. N Engl J Med 318:129-133, 1988 62 Thierfelder L, Watkins H, MacRae C, et al: a-Tropomyosin and cardiac troponin T mutations cause familial hypertrophic cardiomyopathy: A disease of the sarcomere. Cell 77701-712, 1994 63 Thompson PD, Funk EJ, Carleton RA, et al: Incidence of death during jogging in Rhode Island from 1975 through 1980. JAMA 2472535-2538, 1982 64. Thompson PD, Stem MP, Williams P, et al: Death during jogging or running: A study of 18 cases. JAMA 242:1265-1267, 1979 65, Topaz 0, Edwards JE: Pathologic features of sudden death in children, adolescents and young adults. Chest 87476482, 1985 66. Tsung SH, Huang TY, Chang HH: Sudden death in young athletes. Arch Pathol Lab Med 106:168-170, 1982 67. van Camp SP, Bloor CM, Mueller FO, et al: Nontraumatic sports death in high school and college athletes. Med Sci Sports Exerc 27641447, 1995 68. Vincent GM, Timothy KW, Leppert M, et al: The spectrum of symptoms and QT intervals in carriers of the gene for the long-QT syndrome. N Engl J Med 327846-852, 1992 69. Virmani R, Robinowitz M, McAllister HA Jr: Nontraumatic death in joggers: A series of 30 patients at autopsy. Am J Med 72:874-882, 1982 70. Virmani R, Robinowitz M, Smialek JE, et al: Cardiovascular effects of cocaine: An autopsy study of 40 patients. Am Heart J 115:1068-1076, 1988 71. Waller BF, Roberts WC: Sudden death while running in conditioned runners aged 40 years or over. Am J Cardiol 45:1292-1300, 1980
RISK PROFILES AND PREPARTICIPATIONSCREENING OF COMPETITIVE ATHLETES 72. Watkins H, Comer D, Thierfelder L, et a1 Mutations in the cardiac myosin binding protein-C gene on chromosome 11 cause familial hypertrophic cardiomyopathy. Nat Genet 11:434437, 1995 73. Weidenbener EJ, Krauss MD, Waller BF, et al: Incorporation of screening echocardiography in the preparticipation exam. Clin J Sports Med 5236-89, 1995
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74. Wigle ED, Sasson Z, Henderson MA, et al: Hypertrophic cardiomyopathy: The importance of the site and extent of hypertrophy-a review. Prog Cardiovasc Dis '28143,1985 75. Zehender M, Meinertz T, Keul J, et al: ECG variants and cardiac arrhythmias in athletes: Clinical relevance and prognostic importance. Am Heart J 119:1378-1391, 1990
Address reprint requests to Barry J. Maron, MD Minneapolis Heart Institute Foundation 920 East 28th Street, Suite 40 Minneapolis, MN 55407
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RISK PROFILES AND CARDIOVASCULAR PREPARTICIPATION SCREENING OF COMPETITIVE ATHLETES Barry J. Maron, MD
Sudden deaths of competitive athletes are personal tragedies with great impact on the lay and medical communitiesz7that are usually due to a variety of previously unsuspected cardiovascular diseases.* Such events often assume a high public profile because of the generally held perception that trained athletes constitute the healthiest segment of society, with the deaths of well-known elite 34 athletes often exaggerating this vi~ibility.~~, Although these athletic field catastrophes strike to the core of sensibilities and often galvanize society, they also inevitably raise a number of practical and ethical issues. In response to these considerations, an American Heart Association consensus panel was composed of a number of cardiovascular specialists and other physician experts having extensive clinical experience with athletes of all ages as well as a legal
The present text is reproduced with some adaptation from Maron BJ, Thompson PD, Puffer JC, et al: American Heart Association Medical/Scientific Statement: Cardiovascular preparticipation screening of competitive athletes. Circulation 94:850-856, 1996; with permission of the American Heart Association. *References 1, 3, 6, 11, 17, 24, 32, 36, 42, 47, 61, 6347, 69, 71.
expert. This 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 medicolegal implications of screening; and (3) developed consensus recommendations and guidelines for the most prudent, practical, and effective screening procedures and strategies. It seems particularly relevant to reproduce those concepts here given the large number of competitive athletes in the United States and public health initiatives on physical activity and exercise. DEFINITIONS AND BACKGROUND
This discussion focuses on the competitive athlete, previously 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 a ~ h i e v e m e n tThe . ~ ~ 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
From the Cardiovascular Research Division, Minneapolis Heart Institute Foundation, Minneapolis, Minnesota
CARDIOLOGY CLINICS VOLUME 15 * NUMBER 3 * AUGUST 1997
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thereby reduce the risks associated with organized sports. Raising the possibility of a cardiovascular abnormality on a standard screening examination is, however, only the first tier of recognition, after which referral to a specialist for further diagnostic investigation is probably required. When a definitive cardiovascular diagnosis is made, the consensus panel guidelines of Bethesda Conference #2637 should be used to formulate recommendations for continued participation or disqualification from competitive sports. The present guidelines focus primarily on the potential for population-based screening of high school and collegiate student athletes rather than individual clinical assessments of athletes and are designed to apply to competitors of all ages and both genders. Also, these recommendations may be extrapolated to athletes in youth, middle-school, masters, or professional sports and in some instances to participants in intense recreational sporting activities. It is also recognized that overall preparticipation screening goes well beyond the considerations described here, which are limited to the cardiovascular system, and involves many other organ systems and medical issues. 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 presently 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, although a minority of deaths occur independent of exercise.41,42, 67 Finally, the early detection of clinically significant cardiovascular disease through preparticipation screening in many instances permits timely therapeutic interventions that may prolong life. CAUSES OF SUDDEN DEATH IN ATHLETES
A variety of cardiovascular abnormalities represent the most common causes of sudden death in competitive athletes.* The precise lesions responsible for athletic field catastrophes differ considerably with regard to age. For example, in youthful athletes (<35 years of age), the vast majority are due to a variety *References 1, 3, 6, 11, 17, 24, 32, 41, 42, 47, 61, 6347, 69, 71.
of largely congenital cardiac malformations 42, 67 Virtually any disease capable of (Fig. l).41, causing sudden death in young people potentially may do so in young competitive athletes. Although these cardiovascular diseases may be relatively common in young athletes dying suddenly, each is uncommon in the general population. Also, the lesions responsible for sudden death do not occur with the same frequency, with most responsible for only 5% or less of all deaths (see Fig. 1). The single most common cardiovascular abnormality among the causes of sudden death in young athletes is hypertrophic cardiomyopathy, usually in the nonobstructive form30,41, 42, 67 and with a prevalence in the range of 35% (see Fig. 1).Hypertrophic cardiomyopathy is a primary and familial cardiac malformation with heterogeneous expression, complex pathophysiology, and diverse clinical course for which several disease-causing mutations in four genes encoding proteins of the cardiac sarcomere have been reported.60Hypertrophic cardiomyopathy is a relatively uncommon malformation occurring in about 0.2% of the general populati~n.~~ The next most frequent cause of sudden death is a variety of congenital coronary anomalies, particularly anomalous origin of the left main coronary artery from the right (anterior) sinus of Valsalva.2,58 Less common causes are myocarditis, dilated cardiomyopathy, Marfan’s syndrome with aortic rupture, arrhythmogenic right ventricular dysplasia, sarcoidosis, mitral valve prolapse, aortic valve stenosis, atherosclerotic coronary artery disease, long QT syndrome, and possibly intramural (tunneled) coronary arteries. These deaths occur most commonly in intense team sports, such as basketball and football, which also have the highest levels of participation. Older athletes (> age 35) represent a different athletic population because they do not participate primarily in organized team sports but rather focus on individual endeavors, such as long distance running. Furthermore, the vast majority of deaths in middle-aged athletes are due to atherosclerotic coronary artery disease63,64, 69, 71 and only rarely to congenital diseases such as hypertrophic cardiomyopathy or coronary artery anomalies. Because this discussion focuses on the cardiovascular evaluation of athletes, other related medical problems that may occasionally cause sudden death in the young, such as cerebral aneurysm, sickle cell trait,19nonpene-
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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, from 1985 to 1995. Ao = Aorta; ARVD = arrhythmogenic right ventricular dysplasia; LAD = left anterior descending; AS = aortic stenosis; MVP = mitral valve prolapse; CAD = coronary artery disease; HCM = hypertrophic cardiomyopathy. (Adapted from Maron BJ, Shirani J, Poliac L, et al: Sudden death in young competitive athletes: Clinical demographic and pathological profiles. JAMA 276:199-204, 1996; with permission.)
trating blunt chest impact,39 or bronchial asthma, have been excluded from the present considerations. Also, issues related to drug screening are not discussed here, although it is known that the ingestion of agents such as cocaine may have important adverse cardiovascular consequences.16,20, 70 Screening for systemic hypertension, although not regarded as an important cause of sudden unexpected death in young athletes,18has been addressed. PREVALENCE AND SCOPE OF THE PROBLEM
Relevant to the design of any screening strategy is the fact that sudden cardiac death in athletes is a devastating but rather infrequent event, and only a small proportion of participants in organized sports in the United 67 ~ Each States are at r i ~ k . ~ , ~ ,of the lesions known to be responsible for sudden death in young athletes occurs infrequently in the general population, ranging from the relatively common (e.g., hypertrophic cardiomyopathy) to the apparently very rare (e.g., cor-
onary artery anomalies, arrhythmogenic right ventricular dysplasia, long QT syndrome, or Marfan’s syndrome), for which reliable estimates of frequency are lacking. It is reasonable to estimate that congenital malformations relevant to athletic screening may account for a combined prevalence of only 0.3% or less in general athletic populations. The large reservoir of competitive athletes in the United States constitutes another major obstacle to screening strategies. At present, there are approximately 5 million competitive athletes at the high school level (grades 9 through 12), in addition to lesser 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 whom reliable numbers are not presently available. Although the national prevalence of athletic field deaths owing to cardiovascular disease is not known with certainty, it appears to be in the approximate range of 1 in 50,000 to 1 in 100,000 athletes of high school age, although disproportionately higher in males.44 In older athletes, available esti-
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mates40,64 suggest the frequency of sudden cardiac death, principally owing to coronary artery disease (1 in 15,000 joggers and 1 in 50,000 marathon runners), may exceed somewhat that in younger athletes. Considering such a relatively low prevalence, the heightened awareness and intense interest in sudden deaths in athletes, often fueled by the news media, is perhaps disproportionate to their actual numerical impact as a public health problem. ETHICAL CONSIDERATIONS IN SCREENING
There is a general consensus that within a benevolent society, a responsibility exists on the part of physicians to initiate prudent efforts for the identification of life-threatening diseases in athletes, for the purpose of minimizing the 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-effective strategies to ensure that their student athletes are not subject to unacceptable and unavoidable medical risks. Despite sufficient resources, it is recognized that a high motivation to implement cardiovascular screening may not presently exist on the part of professional teams or athletes because of the economic pressures inherent in such a sports environment for which athletic participation represents a vocation and remuneration for services 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.31 There is often implied acceptance of risk on the part of athletes; society permits or condones 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 acknowledge the limitations associated with preparticipation screening to (1) create an informed public that might otherwise harbor important misconceptions regarding the principles and efficacy of athletic screening and (2) offer appropriate
guidance to physicians and health care workers responsible for screening. LEGAL CONSIDERATIONS
Although educational institutions and professional teams must use reasonable care in conducting their athletic programs, there currently is no clear legal precedent regarding their duty to require or conduct preparticipation screening of athletes for the purpose of detecting medically significant abnormalities. At present, no lawsuits have apparently been brought forward alleging negligence in the failure either to perform cardiovascular screening or to diagnose cardiac disease in young competitive athletes. In the absence of binding requirements established by state law or athletic governing bodies, most institutions and teams presently rely on their team physician or other medical personnel to determine the appropriate medical screening procedures. At present, 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 undetected 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 utilization of established diagnostic criteria and techniques would have disclosed the subject’s medical condition. The law permits the medical profession to establish the appropriate nature and scope of preparticipation screening of athletes based on the exercise of its collective medical judgment. This necessarily involves the development of reliable diagnostic procedures in light of cost-benefit and feasibility factors. The present guidelines for cardiovascular preparticipation screening of athletes are some evidence of the proper medical standard of care; they establish the legal standard of care if generally accepted or customarily followed by physicians49 or relied on by courts in determining the nature and scope of the legal responsibility borne by sponsors of competitive athletes in determining their medical fitness. CURRENT CUSTOMARY PRACTICE
Currently, there are no universally accepted standards for the screening of high
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school and college athletes, and there are no approved certification procedures for health care professionals who perform such screening examinations. Some form of medical clearance by a physician or other trained health care worker, usually consisting of a history and physical examination, presently appears most customary for high school athletes. Standards may be mandated by state legislative action or left to the individual state high school athletic associations or school districts. There is no uniform agreement among the states, however, as to the precise format of preparticipation medical evaluations and clearances; in fact, not all states require this process or have a recommended standard medical form. Some of. the available forms are specific, whereas others require only the signature of a physician to provide clearance for the athlete to compete in organized sports. In a substantial minority of states, nonphysician health care workers are sanctioned to perform preparticipation screening, including chiropractors (in 11 states) and advanced nurse-practitioners or physician’s assistants, with or without physician supervision, (in 16 states). Useful models for the preparticipation examination have been developed by a number of medical organizations or investigators.7,8,14.59 EXPECTATIONS OF STANDARD SCREENING PROCEDURES
Preparticipation screening by history and physical examination alone (without noninvasive testing) does not have sufficient power to guarantee detection of many critical cardiovascular abnormalities in large populations of young trained athletes. 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 the standard screening examination is unreliable because most patients have the nonobstructive form of this disease, characteristically expressed by no or only a soft heart murmur.25, 30, 60, 74 Furthermore, most athletes with hypertrophic cardiomyopathy do not experience syncope or have a family history of premature sudden death as a result of their disease.28,42 The standard personal history conveys a generally low specificity for the detection of 297
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many cardiovascular abnormalities that lead to sudden cardiac death in young athletes, particularly when symptoms such as chest pain or impaired consciousness are involved. 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 at-risk individuals. EFFECTIVENESS AND LIMITATIONS OF NONINVASIVE SCREENING TESTS
In young athletes, the addition of noninvasive diagnostic tests to the screening process clearly has the potential to enhance the detection of certain cardiovascular defects. For example, the two-dimensional echocardiogram is the principal diagnostic tool for clinical recognition of hypertrophic cardiomyopathy by demonstrating otherwise unexplained asymmetric left ventricular wall thickening, the sine qua non of this disease.21,25, 29, 74 Comprehensive and routine screening for hypertrophic cardiomyopathy with genetic testing for a variety of known mutations is not yet practical or feasible for large populations, given the substantial genetic heterogeneity of the disease and the expensive and time-intensive 60, 72 methodologies in~olved.’~, Echocardiography could also be expected to detect other relevant abnormalities associated with sudden death in young athletes, such as valvular heart disease (e.g., mitral valve prolapse), aortic root dilation, and left ventricular dysfunction (in myocarditis or dilated cardiomyopathy). Even such diagnostic testing cannot itself, however, guarantee identification of all important lesions, and some diseases may be beyond detection with any screening methodology. For example, identification of many congenital coronary artery anomalies usually requires sophisticated laboratory examination, including coronary arteriography, although it is possible in selected young athletes to raise a strong suspicion of (or even identify) anomalies such as left main coronary artery from the right sinus 28, 35 Arof Valsalva with echocardiography.12, rhythmogenic right ventricular dysplasia usually cannot be reliably diagnosed solely with echocardiography and electrocardiogram (ECG); the best available noninvasive test for this disease appears to be magnetic resonance imaging, which is both expensive and not universally available.48,56
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Cost-efficiency issues are important when assessing the feasibility of applying expensive testing to the screening of large athletic populations’, 51, 57, 73 (in the vast majority of instances, adequate financial and personnel resources are lacking for such endeavors). In those situations in which the full (i.e., unreduced) expense of testing would be the responsibility of administrative bodies such as a school, university, or team, the costs are probably prohibitive, ranging from about $400 to $2000 per echocardiographic study (average about $600). For example, if the occurrence of hypertrophic cardiomyopathy in a young athletic population is assumed to be as common as 1 in 500,33 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 cost have been describeds1,73; however, these efforts have been in unique circumstances in which equipment was donated and professional expenses were waived for all but technicianrelated costs. Some investigators have suggested an inexpensive shortened-format echocardiogram for population screening (limited to parasternal views, about 2 minutes in duration).”, 73 Nevertheless, such public service projects, based largely on volunteerism, usually cannot be sustained on a consistent basis because priorities in the utilization of available resources may change and therefore are unlikely to be implemented on a scale necessary to provide effective screening to all high school and collegiate athletes. Another important limitation of screening with two-dimensional echocardiography is the potential for false-positive or false-negative test results. False-positive results may arise from the assignment of borderline Values for left ventricular wall thicknesses (or particularly large values for cavity size), which require formulation of a differential diagnosis between the normal physiologic adaptations of athlete’s heart*s,26, 5s and pathologic conditions such as hypertrophic cardiomyopathy or other cardiomy~pathies.~~ Such clinical dilemmas (which may not always be definitively resolvable in individual 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 screening results may occur when encountering athletes with hypertrophic cardiomyopathy at a point of in-
complete phenotypic expression during adol e ~ c e n c e .Consequently, ~~ in selected young athletes with hypertrophic cardiomyopathy (< age 16), left ventricular hypertrophy may be absent or mild and therefore the echocardiographic findings not yet diagnostic of that disease.43 The 12-lead ECG has been proposed as a more practical and cost-efficient alternative to routine echocardiography for populationbased screening.22,2y The ECG is abnormal in about 95% of patients with hypertrophic cardiomyopathy,46may be abnormal in other potentially lethal lesions such as the coronary anomalies? 24, 28 and usually identifies the important (but uncommon) long QT syndrome.sO, Data indicate, however, that a certain proportion of genetically affected relatives in families with long QT syndrome may have little or no phenotypic expression on ECG.68 In preparticipation screening, the ECG suffers in comparison to the echocardiogram by its lack of imaging capability for recognition of structural cardiovascular malformations. Also the ECG has relatively low specificity as a screening test in athletic populations because of the high frequency with which ECG alterations occur in association with the normal physiologic adaptations of the athlete’s heart to training.7s Elite athletes not infrequently demonstrate distinctly abnormal ECG patterns consistent with pathologic conditions,52 even in the absence of structural heart disease and without evidence of a morphologic adaptation to training. In screening large populations of older trained athletes, the routine application of exercise testing to detect coronary artery disease is limited by its low specificity and pretest pr~bability.~ To date, there have been relatively few published reports of cardiovascular screening efforts in large athletic populations.’”,14,22, 23, 29, 4 5 , sl, 57 Most of these studies have implemented noninvasive testing (i.e., conventional or limited echocardiographic examination or 12-lead ECG) in young high school or collegiate athletes. The populations screened have ranged in size from 250 to 2000 athletes, usually studied over a 1-year period. In general, these reports are consistent by virtue of describing the detection of few definitive examples of potentially lethal cardiovascular abnormalities. This is also largely consistent with the experience in Italy, where a systematic national program for the preparticipation evaluation of athletes (often involving echo-
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cardiography) has been in place for more than 30 years.53 PERSPECTIVES ON RACE AND GENDER
Hypertrophic cardiomyopathy is an important cause of sudden death in young African-American athletes.', 42 The substantial occurrence of hypertrophic cardiomyopathy-related sudden death in young African-American male athletes contrasts sharply with the infrequent reporting of AfricanAmerican patients with hypertrophic cardiomyopathy in hospital-based populations. Therefore, in African-Americans, hypertrophic cardiomyopathy is most frequently encountered when it results in sudden and unexpected death during competitive athletics. These data emphasize the disproportionate access to subspecialty health care between the African-American and white communities in the United States, which makes it less likely for young African-American men to receive a relatively sophisticated cardiovascular diagnosis such as hypertrophic cardiomyopathy compared to their white counterparts. Consequently, it appears that African-American athletes with hypertrophic cardiomyopathy are less likely to be disqualified from competition, in accordance with the recommendations of Bethesda Conference #26,37 to reduce their risk for sudden death. Sudden death on the athletic field is uncommon in young women4* (comprising about 10% to 15% of all such deaths), which may be explained not only on the basis of lower participation rates or less severe training demands and cardiac adaptation54 in some instances, but also because hypertrophic cardiomyopathy is less commonly recognized clinically in women.25,30, 46, 74 This observation also suggests 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. SCREENING RECOMMENDATIONS Advisability
The 1996 American Heart Association recommendations state that some form of pre-
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participation cardiovascular screening for high school and college student athletes is justifiable and compelling based on ethical, legal, and medical Noninvasive testing can enhance the diagnostic power of the standard history and physical examination; however, it is not prudent to recommend the routine use of tests such as 12-lead ECG, echocardiography, or graded exercise testing for the detection of cardiovascular disease in large populations of youthful or older athletes. This view 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 is not, however, intended to discourage all efforts at population screening that may be proposed by individual investigators. Nevertheless, there is concern that the widespread application of noninvasive testing to athletic populations could result in many false-positive results, creating unnecessary anxiety among substantial numbers of athletes and their families as well as unjustified exclusion from competition. 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^.^ Consequently, it appears that a complete and careful personal and family history and physical examination designed to identify (or raise suspicion of) 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. It is recommended that both a history and a physical cardiovascular examination be performed before the initial engagement in organized high school (grades 9 through 12) and collegiate sports and subsequently repeated every 2 years. In intervening years, an interim history should be obtained. For young competitive athletes, this recommendation is consistent with procedures that are customary for most high school and college athletes in the United States. Official recommendations or requirements by athletic governing bodies regarding the nature and scope of preparticipation medical
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evaluations of athletes are not standardized among the states, and they necessarily cannot be viewed as medically sufficient in many instances. Therefore, because of this heterogeneity in the design and content of preparticipation examinations, it is also recommended that a systematic national standard for preparticipation medical evaluations be developed. Adherence to uniformly applicable guidelines would have a substantial impact on the health of student athletes, in a costeffective manner, by enhancing the safety of their athletic activities. For older athletes (>35 years of age), despite the limitations of the history and physical examination in detecting coronary artery disease, a personal history of coronary risk factors or familial occurrence of premature ischemic heart disease may be useful for identification of that disease in a screening setting and therefore should be performed before initiating competitive exercise. In addition, it is prudent to perform medically supervised exercise stress testing selectively in men over age 40 (women over age 50) who wish to engage in habitual physical training and competitive sports should the examining physician suspect occult coronary artery disease on the basis of risk factors, either 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. The present guidelines should not promulgate a false sense of security on the part of medical practitioners or the general public. The standard history and physical examination intrinsically lacks the power to identify reliably many potentially lethal cardiovascular abnormalities. It is, therefore, an unrealistic expectation that large-scale standard athletic screening examinations can exclude most important cardiac lesions. Methodology
Preparticipation sports examinations are presently performed by a variety of individuals, including paid or volunteer physicians or nonphysician health care workers with variable training and experience. Examiners may be associated with, or administratively independent of, the concerned institution, school, or team.
Consequently, athletic screening should be performed by an appropriately trained health care worker with the requisite training, medical skills, and background to perform reliably a detailed cardiovascular history and physical examination and to recognize heart disease. Although 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 health care workers (including chiropractors) are permitted to perform preparticipation screening, it is necessary to establish a formal certification process to demonstrate expertise in performing cardiovascular examinations. Specifically, athletic screening evaluations should comprise a complete medical history and physical examination, including brachial artery blood pressure measurement. This examination should be conducted in a physical environment conducive to optimal cardiac auscultation, whether performed individually in a private office or in a station-format 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 from the athlete: (1) prior occurrence of exertional chest pain or discomfort or syncope (or nearsyncope) as well as excessive, unexpected, and unexplained shortness of breath or fatigue associated with exercise; (2) past recognition of a heart murmur or increased systemic blood pressure; and (3) family history of premature death (sudden or otherwise) or morbidity from cardiovascular disease in close relative(s) younger than age 50 or specific knowledge of the occurrence of certain conditions in family members (e.g., hypertrophic cardiomyopathy, dilated cardiomyopathy, long QT syndrome, Marfan's syndrome, or clinically important arrhythmias). These recommendations are offered recognizing that the accuracy of some responses elicited from young athletes may depend on their level of compliance and historical knowledge. Parents should be responsible for completing the history form of high school athletes. The cardiovascular physical examination should emphasize (but not necessarily be lim-
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ited to (1) precordial auscultation in both the supine and the standing positions to identify, in particular, heart murmurs consistent with 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’s 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 specialist for further evaluation and confirmation. Definitively identified cardiovascular abnormalities should be judged with respect to the Bethesda Conference #26 consensus panel guidelines regarding the final determination of eligibility for future athletic c ~ m p e t i t i o n . ~ ~
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