The growing field of sports cardiology is focused on the cardiovascular health and safety of the athlete. Of central importance to this discipline is the prevention of sudden cardiac death (SCD), which is the leading cause of mortality in athletes during exercise. Organizations, such as the American Heart Association (AHA), recommend a history and physical-based cardiovascular evaluation prior to competitive athletics. However, this strategy has proven limited in its ability to identify cardiovascular disorders that predispose athletes to sudden cardiac arrest (SCA). Moreover, it may provide false reassurance to young athletes, parents, and team officials who believe that the evaluation has actively excluded the presence of potentially lethal cardiac disorders.
Recently, there has been considerable research demonstrating that an electrocardiogram (ECG) provides additional value compared with the history and physical examination alone. In fact, modern athlete-specific ECG interpretation criteria have reduced false-positive rates to <3% in some studies while maintaining the sensitivity. In contrast, the false-positive response rates produced by screening cardiac questionnaires are as high as 35% to 68% (11,21,47,52). This article provides an overview of the evidence to support the addition of ECG to current cardiovascular screening in athletes and offers a contemporary approach to the primary prevention of SCD in sports.
Is There a Need for Cardiovascular Screening in Young Athletes?
The tragic death of a seemingly healthy young athlete during a sport event generates considerable attention and publicity, often raising questions about the value and rigor of screening programs. While exercise is associated with significant health benefits, an exercise paradox exists such that vigorous athletic activity can transiently increase the risk of SCD nearly five-fold in those with underlying cardiovascular disorders compared with sedentary individuals (3,7,31). An important ethical question in the consideration of cardiovascular screening in young athletes is whether athletes are at increased risk of SCD compared with nonathletes. In a 2-year prospective study with more than 1.5 million athlete-years and 2.5 million nonathlete years of surveillance for SCA events in U.S. high schools, student athletes were 3.6 times more likely to experience SCA than their nonathlete peers (50).
The AHA, in three separate statements (1996, 2007, and 2014), has endorsed cardiovascular screening in asymptomatic young athletes based on ethical, legal, and medical grounds (34,36,38). As stated in the fourth edition of Preparticipation Physical Evaluation (PPE monograph), the purpose of the PPE is to “identify potentially life-threatening or disabling conditions so they can be treated or risk factors modified” (2). The American College of Cardiology takes this a step further and explicitly states that “the ultimate objective of preparticipation screening is to detect ‘silent’ cardiovascular abnormalities that can lead to sudden cardiac death” (39).
The National Heart, Lung, and Blood Institute has deemed SCD in the young as a significant public health concern (45). As long as cardiovascular screening continues to be recommended by medical and sports governing bodies, it would seem prudent to employ a technique that best achieves the aim of identifying potentially lethal underlying conditions.
SCD: More Frequent than Previously Realized
SCD occurs with a frequency that is nearly five-fold higher than initially reported. The first studies to report the incidence of SCD in young athletes were published in the 1990s. These investigations estimated rates of SCD to be 1/200,000 to 300,000. While these studies brought critical attention to the issue of SCD in athletes, limitations in study design inhibit applicability in the modern era. For example, these original studies relied on media reports or insurance claims for case identification, which are generally not effective in identifying all cases of SCD. In fact, a retrospective study of high profile collegiate athletes found that media reports identified only 56% of cases, which is surprising since the media generally scrutinizes this population heavily (22). These findings are not isolated to the U.S. population. A study from Denmark reported that only 20% of athlete deaths identified through death certificate review also were found by search of media reports (26). Interestingly, the use of media reports for case identification appears to be even more deficient in lower profile athletes. In a recent investigation, media reports captured 87% of SCD cases in National Collegiate Athletic Association (NCAA) Division I athletes, but only 44% in Division III (23). Insurance claims data appear seriously deficient in identifying cases of SCD. For example, insurance claims captured only 11% to 14% of athlete SCD in one U.S. study (22,23). As a result, using either media searches (especially in a preinternet era) or insurance claims data for case identification will underestimate the true incidence of SCD.
An accurate rate of SCD hinges upon a precise numerator (cases identified) and a defined denominator (population). Mandatory reporting systems offer the most reliable information, but few of these types of datasets exist outside of the military. A comprehensive study of military personnel provides an example of an ideal investigation given the defined target population, mandatory reporting of death, and standardized post-mortem protocols. The rate of SCD in this population was 1/25,000 in those <35 years of age from more than 15.2 million person-years of active surveillance during a 10-year span (19).
The U.S. NCAA athlete population (approximately 500,000 athletes per year) is another well-defined group with a narrowly demarcated age range. Precise demographics and participation rates are published each year in the NCAA Sports Sponsorship and Participation Rates Report and the NCAA Student Athlete Ethnicity Report. A recent study examined all-cause mortality in NCAA athletes from 2003 to 2013 with review of autopsy data. A total of 514 student athlete deaths occurred within 4,242,519 athlete-years of participation. The most common medical cause of death was SCD, with a frequency of 1/53,703 athlete-years. Men were at significantly higher risk than women (1/37,790 vs 1/120,481; incidence rate ratio, 3.2, P < 0.00001), and black athletes were at significantly higher risk than white athletes (1/21,491 vs 1/68,027; incidence rate ratio, 3.2; P < 0.00001). The incidence of SCD was highest in Division I male basketball athletes at 1/5,200 athlete-years. Averaged over a 4-year career, these rates translate to a risk of SCD of 1/13,426 per athlete for the entire NCAA, and 1/1,300 for Division I male basketball players. Importantly, these alarmingly high rates have occurred in athletes already screened using at minimum the standard PPE consisting of a medical history and a physical examination (23).
The heterogeneity of case identification and lack of systematic data collection methods have hampered accurate assessment for the rate of SCD in high school athletes. In fact, depending on the study, rates vary from 1/23,000 to 1/917,000. Many of the investigations examine deaths only during school hours, focus only on deaths during school-sponsored activities, include cases of death but not cardiac arrest with survival, or rely solely on media reports or insurance claims for case identification (24). The limitations in study methodology likely result in missed cases of cardiovascular events and an underestimation of the true incidence. Based on studies with stronger methodology, the incidence of SCD in high school athletes is estimated at 1/50,000 to 1/80,000, with male athletes at higher risk (24). Since the athlete healthcare team is responsible for the overall health of the athlete in any setting, incidence calculations should ideally include events that occur at any time both inside and outside of sports, during exercise at any time (not just organized school activities), include SCA as an end point, and include a defined study population.
Screening for SCD: What Are We Looking for?
Hypertrophic cardiomyopathy is reported as the most common autopsy-confirmed etiology of SCD in the United States. Additional data have shown that autopsy-negative sudden unexplained death also represents a major proportion of SCD in athletes. A retrospective study of NCAA athletes over a 10-year period (2003 to 2013) reviewed available autopsy reports using a multidisciplinary panel of cardiologists, sports medicine physicians, and a cardiovascular pathologist (23). While autopsy protocols were not standardized and many of the reports with inadequate detail, the most common finding at death was a structurally normal heart (25%); confirmed hypertrophic cardiomyopathy (HCM) was present in 8% of cases (23). Standardized post-mortem evaluation using advanced techniques, such as genetic testing in autopsy negative cases, is needed to better define the cardiovascular pathology leading to SCD.
ECG increases the sensitivity to identify the most common disorders associated with SCD where early detection is the objective of screening. ECG abnormalities are present in about 90% of patients with HCM (5,44,46). In contrast, a pathological murmur is present in only 25% of cases, and most athletes who die of HCM have no prodromal symptoms (35). ECG also represents the standard for diagnosis of ion channelopathies and ventricular preexcitation. Notably, two important causes of SCD, anomalous coronaries and aortopathies, are not readily detectable by ECG or evaluation by history and physical examination. While ECG improves the detection of at-risk conditions, no screening strategy will provide absolute protection against SCD.
Limitations in Current Screening Paradigm
The current protocol endorsed by the AHA includes a 14-point history and physical examination. This includes seven elements related to personal history, three elements of family history, and four elements for physical examination (37). There are a small percentage of athletes with cardiovascular warning symptoms, such as syncope, unexplained seizure activity, exertional chest pain, or a family history of early (<50 years old) SCD that should not be missed and is readily detected by careful evaluation. However, studies have shown that a history and physical examination has limited effectiveness in detecting underlying cardiac disease. In a study of 115 cases of SCD, only one (0.9%) was correctly identified through a preparticipation history and physical examination (35). A recent meta-analysis demonstrated that the sensitivity of the history (20%) and physical examination (9%) was remarkably low in identifying potentially lethal cardiovascular disorders (25).
The underlying limitation to screening by history and physical examination alone is that the majority of competitive athletes who have pathological cardiac disease are asymptomatic. Reports have shown that 60% to 80% of athletes who experienced SCD did not have warning signs or symptoms and cardiac arrest was the first manifestation of their disease (1,6,10,18,35). Thus, a screening protocol rooted in history and physical examination alone will result in a high number of false negatives and false reassurance to the majority of athletes with potentially lethal cardiovascular disease.
The vague nature and high positive response rate of cardiac history questions also pose a challenge for the evaluating physician. Studies show that 14% to 68% of high school or college athletes report at least one positive symptom or family history response on modern screening questionnaires (16,21,43). Proper evaluation of concerning symptoms or family history is critical, but also with broad clinician variation. Guidance for physicians following a positive response to cardiac history questions is available in the two-part symposium on The Cardiovascular Preparticipation Evaluation (PPE) for the Primary Care and Sports Medicine Physician previously published in Current Sports Medicine Reports (48,49).
Enhanced Disease Detection with an ECG
The most effective strategy for screening for cardiovascular disease in athletes occurs with the use of an ECG. For every reason screening by history and physical examination is promoted, the addition of ECG allows a more effective screen when conducted by experienced clinicians. ECG is nearly five times more sensitive than the current medical history questions, 10 times more sensitive than the physical examination, and has a higher positive likelihood ratio, a lower negative likelihood ratio, and a lower false-positive rate than history and physical examination (25). While the AHA opposed mandatory or nationalized ECG screening programs, the AHA has long supported ECG programs that are locally driven, well-organized, and with sufficient physician interest and resources (32,37). The European Society of Cardiology (ESC), International Olympic Committee, Federation de Internationale de Football Association, IOC, FIFA, and many professional U.S. sporting organizations (National Football League, Major League Baseball, National Basketball Association, Major League Soccer, and National Hockey League) also endorse cardiovascular screening by ECG (8,17,29,37).
Critics of an ECG screening program typically cite concerns about high false-positive rates and poor cost effectiveness. These two items are linked, such that lower false-positive rates ultimately improve cost efficiency. Changes in the ECG of highly trained athletes usually develop as a result of physiological adaptation to regular physical activity (athlete's heart). When traditional ECG interpretation parameters were used to interpret an athlete's ECG, the false-positive rates were reported to be 15% to 40% (33,41). However, much of this research is more than a decade old.
New research has provided an improved understanding of the diseases associated with SCD and how the ECG can be applied for early detection. Contemporary athlete-specific ECG interpretation standards that account for physiological changes associated with exercise have drastically reduced false-positive rates (14). Several recent consensus statements detail the difference between normal physiological changes in response to exercise from findings suggesting cardiac pathology (9,12,51). With the use of these guidelines, false-positive rates for ECG screening in athletes have become lower than the methods to detect other lethal diseases such as breast cancer (40). For example, a comprehensive cardiovascular screening study in high school athletes in which all athletes received a history, physical examination, ECG, and echocardiogram demonstrated that an ECG interpreted with modern standards yielded a false-positive rate of only 2.8% (43). Similarly, Marek et al. (30) performed a large 5-year ECG screening study with over 32,500 adolescent individuals, which demonstrated an abnormal ECG in only 2.5% of subjects. In a study of 790 college athletes, an abnormal ECG was present in only 2.8% of athletes and led to the detection of five potentially lethal cardiac disorders, all of which would have been missed by history and physical examination alone (15).
The three recent athlete-specific ECG interpretation standards include the ESC (2010), Stanford (2011), and Seattle Criteria (2013). Each subsequent revision of ECG standards has improved the specificity (lower false-positive rate) without compromising sensitivity. A study of 1,417 healthy U.S. athletes found that the Seattle Criteria (6%) was associated with the lowest false-positive rates as compared with the Stanford (8%) and ESC (26%) criteria (42). Similarly, an Australian study of 1,078 elite athletes demonstrated a dramatic reduction in false-positive rates (17.3% to 4.5%, P < 0.001) through the use of the Seattle Criteria versus the ESC guidelines (4). Importantly, these criteria demonstrate lower false-positive rates with preserved sensitivity for detecting cardiovascular abnormalities. The improved accuracy found in these types of studies has broad implications for the feasibility of ECG screening programs as lower false-positive rates mean that fewer athletes will be referred for follow-up testing, which will ultimately lead to improved cost effectiveness if accurate ECG interpretation and proper secondary evaluation of ECG abnormalities can be achieved.
Disease Detection Does not Mean Disqualification
Guidelines for the management of athletes with cardiovascular disorders have historically been based on consensus recommendations (39). These guidelines suggest that athletes who are diagnosed with certain genetically inheritable conditions be disqualified from sporting activity or advised to compete in class IA sports only, such as bowling, golf, or billiards (39).
Recent medical advances and research challenge the notion that disease detection equals disqualification. Advancements in medical management have been utilized to reduce the risk for SCD and return athletes to sport. For instance, after noninvasive risk assessment with an exercise stress test for athletes with Wolff-Parkinson-White, catheter ablation can be utilized in high-risk accessory pathways. In a 10-year study of 130 competitive athletes with long QT syndrome, there was a low rate of cardiovascular events (0.003 per athlete year) in those who received the appropriate medical therapy such as beta-blockers or an implantable cardioverter defibrillator (ICD) (27). Similarly, an investigation of 372 athletes participating in organized with an ICD found that at a median of 31 months, there were no reported deaths from ventricular tachyarrhythmias or shock-related injury during athletics (28). These studies highlight the advantages of early detection, active medical management strategies, and mitigation of risk factors in lowering the rate of SCD events (27,28).
More outcomes research is needed to better determine the potential reduction in morbidity and mortality in athletes identified with a serious cardiac disorder. Opponents of ECG screening who cite the need for more outcomes research before ECG screening is accepted are really arguing against cardiovascular screening of any type. For instance, it is inconsistent to support detection of HCM because of a heart murmur, but not support detection of the same disease by ECG, which has significantly better sensitivity. Early detection of disease with risk factor modification and individualized medical management is the primary aim of cardiovascular screening in athletes and better accomplished by screening protocols inclusive of ECG.
The Need for Education
If ECG is included in the cardiovascular screening of young athletes, it must be interpreted by modern athlete-specific standards and with adequate cardiology oversight and resources to conduct appropriate secondary investigations. A major hurdle for broader application of ECG screening includes the lack of a trained physician workforce in sports cardiology. Several studies have demonstrated that education can improve quality of care. Recent studies testing U.S., Australian, and New Zealand physicians affirm that physician education can improve accuracy in ECG interpretation of athletes (13,20). Free in-depth online modules accompany the Seattle Criteria and are a valuable resource for clinicians who choose to do ECG screening or wish to know management strategies after an abnormality is discovered (http://learning.bmj.com/ECGathlete). The lack of a broad physician infrastructure capable of implementing quality ECG programs should not deter recognition that ECG screening better achieves the goals of cardiovascular screening when conducted by experienced clinicians; rather, it should motivate the sports medicine and cardiology communities to reach and establish a new standard for the cardiovascular care of athletes.
The field of sports cardiology has advanced considerably since the development of the original cardiovascular screening questionnaires. For all of the reasons that preparticipation cardiovascular screening was designed — namely, early detection of potentially lethal cardiovascular conditions to reduce the risk of SCD — the ECG can accomplish the same goal with considerably greater effectiveness when interpreted with modern standards and with appropriate cardiology resources. ECG screening should be strongly considered in the highest risk athlete subgroups, where traditional screening by only history and physical examination has been ineffective in identifying at-risk disorders for SCD prevention.
The authors declare no conflict of interest and do not have any financial disclosures.
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