Sudden cardiac death (SCD) in children and young athletes is a devastating event, with compelling reasons to implement preventive strategies. Sudden cardiac arrest (SCA) from occult cardiovascular disease is the leading cause of death in athletes during sports participation (30,32). Although the precise frequency of SCD remains disputed, the tragic death of a young athlete predictably generates intense public scrutiny regarding preathletic screening procedures.
Cardiovascular screening for athletes is routinely practiced and supported by most major sporting and medical associations, including the American Heart Association, European Society of Cardiology, and the International Olympic Committee (13,26,27,37). However, universal endorsement of a single screening strategy to identify athletes at risk for SCD remains elusive and a topic of tremendous debate within the international sports medicine and cardiology communities.
The screening controversy is principally centered upon the inclusion (or not) of a resting 12-lead electrocardiogram (ECG) in addition to a history and physical examination during the preathletic evaluation (6,17,18,39). Important data exist from the Italian screening program that a protocol using ECG reduces the incidence of SCD in athletes (8). However, application of this program in other countries with different or more heterogeneous populations has raised concerns regarding false positive results, cost-effectiveness, physician infrastructure, and health care resources (47).
This article frames the current challenges and controversies surrounding the preparticipation physical evaluation (PPE) and ECG screening in young athletes. Our goal is to address key questions that primary care and sports clinicians have in determining the most appropriate protocol for cardiovascular screening in athletes and to identify those areas requiring further study.
WHAT ARE WE SCREENING FOR?
Etiology of SCD in Athletes
The differential diagnosis for causes of pediatric and young adult SCA is detailed in Table 1. SCA is caused by a heterogeneous group of cardiac diseases that generally can be separated into structural cardiovascular abnormalities (e.g., cardiomyopathies) and primary cardiac electrical diseases (e.g., ion channel disorders). Hypertrophic cardiomyopathy (HCM) is the most common structural and functional disease associated with pediatric and young adult SCA (28,30,32). Several studies have suggested that HCM is the leading cause of SCD in young athletes in the United States, accounting for approximately one third of cases (30,32). While some patients with HCM may present with symptoms (e.g., chest pain, syncope, or exertional lightheadedness) (1), studies suggest that 80% of athletes who die from HCM have no warning symptoms before their death (36). The majority (75%) of patients with HCM also do not have detectable murmurs on cardiac auscultation (29). Thus, detection of patients with HCM by history and physical alone is difficult. Congenital coronary artery anomalies are another common etiology of SCD in young competitive athletes, representing 17% of cases (32). Arrhythmogenic right ventricular cardiomyopathy (ARVC) represents 4% of SCD in the United States, (32) but has been reported as the leading cause of SCD (22%) in the Veneto region of northeastern Italy (11). Marfan syndrome is an inherited connective tissue disorder that causes a progressive dilatation and weakness (cystic medial necrosis) of the proximal aorta that can lead to rupture and sudden death. Aortic rupture accounts for approximately 3% of SCD cases in young athletes in the United States (32).
Primary cardiac electrical diseases, or ion channel disorders, are increasingly recognized as a significant cause of pediatric and young adult SCA (44,45). In some cases, postmortem examination fails to identify a structural cardiac cause of death. These deaths, known as autopsy-negative sudden unexplained death (SUD), may be due to inherited arrhythmia syndromes and ion channel disorders such as long QT syndrome (LQTS), short QT syndrome, Brugada syndrome, or familial catecholaminergic polymorphic ventricular tachycardia (CPVT) (30). The prevalence of ion channel disorders as a cause of SCD in U.S. athletes may be underestimated, as autopsy-negative SUD represents a substantially larger proportion of SCD in the young in other study populations, and the accurate diagnosis of ion channelopathies postmortem is still limited. In Australia, autopsy-negative SUD represents approximately 30% of SCD in individuals younger than 35 yr (15,43), and in U.S. military recruits, autopsy-negative SUD accounts for 35% of nontraumatic exercise-related SCD (19,20). These findings stand in contrast to the reported 3% of autopsy-negative SUD in U.S. athletes (32).
Patients with ion channel disorders may present with syncope or unexplained seizure activity. Syncope is caused by short, self-terminating, ventricular tachyarrhythmias, such as torsades de pointes (LQTS) and ventricular tachycardia (CPVT), but sustained arrhythmias and SCA also may be the first manifestation of disease (25). Other causes of SCD include the use of illicit drugs and stimulants, as well as commotio cordis due to a blunt, traumatic blow over the left precordium, which induces ventricular fibrillation (34).
Importantly, roughly half of the disorders causing pediatric and young adult SCA are known to be familial or genetic (Table 1). Therefore, the identification of even a presymptomatic proband is critical, as diagnosis of a child or adult family member may impact subsequent detection of the same disease within multiple family members (10). Thus, the role of genetic evaluation after disease identification as a result of screening is becoming increasingly important, and for most diseases, is commercially available.
WHAT IS THE SCOPE OF THE PROBLEM?
Incidence of SCD
SCD is the leading cause of death in young athletes on the playing field (32). However, the exact incidence of SCD is disputed, and it is difficult to compare incidence studies with profoundly different methodologies and from widely different geographic locations. Estimates from the United States range from 1:160,000 to 1:300,000 competitive athlete deaths per year due to cardiovascular diseases (32,33,48). These studies, while rigorous in effort, rely primarily on searches of public media reports and other electronic databases and are at risk of underestimating the incidence of SCD because of the lack of a mandatory reporting system. With no reliable reporting system and no universal definition of "athlete," accurate reflection of the numerator (number of cases per year) and the denominator (number of athlete participants per year) makes calculating the incidence of SCD in athletes challenging.
In contrast, the Veneto region of Italy uses a regional registry for juvenile sudden death and reported a SCD incidence of 1:28,000 for young competitive athletes (aged 12-35 yr) prior to implementing a national screening program (8). Similarly, a recent prospective population-based study conducted at 11 U.S. and Canadian cities found an incidence of SCA from cardiovascular disease of 1:27,000 in children and young adults (aged 14-24 yr) (3). In U.S. military recruits (aged 18-35 yr), the incidence of nontraumatic, exercise-related SCA was calculated at 1:9000 (19). Thus initial reports in U.S. athletes may have vastly underestimated the magnitude of SCD.
WHAT IS THE PURPOSE OF SCREENING?
Incidence Versus Prevalence
It is critical to clarify the purpose of cardiovascular screening in athletes in order to develop an appropriate screening program. Is the goal of screening simply to prevent SCD, or is the goal of screening to identify children with cardiovascular conditions at risk for SCD? The American College of Cardiology contends that the "ultimate objective of preparticipation screening of athletes is the detection of silent cardiovascular abnormalities that can lead to SCD" (38). The Preparticipation Physical Evaluation Monograph, written and endorsed by six national medical societies, states that its primary objective is to detect, through screening, potentially life-threatening or disabling conditions before undergoing specific athletic participation (2).
Thus perhaps it is the prevalence of cardiovascular conditions with the potential for sudden death, rather than the incidence of SCD itself, that should influence the rigor of our screening procedures. The goal of screening is to detect occult cardiovascular disorders, as many of these conditions can be effectively managed through activity modification and medical intervention (pharmacotherapy, radiofrequency ablation, implantable cardioverter defibrillator, or even surgery) to reduce the risk of sudden death. The American Heart Association estimates the combined disease prevalence of all cardiovascular disorders that potentially predispose young athletes to SCD is 0.3% (37). In contrast to the wide range of estimates for SCD incidence, the prevalence of potentially lethal cardiovascular diseases in athletes has consistently ranged between 0.2% and 0.4% in studies using ECG screening (8,21,49). In other words, approximately 1 in 300 to 500 athletes harbor an occult cardiovascular condition that could place them at risk for SCD. No study using history and physical alone as the screening protocol has demonstrated any significant detection of underlying cardiovascular disease in athletes.
WHO SHOULD BE SCREENED?
All Children or Only Competitive Athletes
The PPE is used in a variety of settings, from youth sports to high school, college, and professional levels, to promote the safety and health of athletes participating in sport. However, there are broader public health issues entrenched within the topic of preathletic screening. If specific screening tests or procedures are valuable for the minority of children and young adults who participate in organized sports, should these tests be available for all children, given the emphasis of exercise as a pathway to long-term health?
On the one hand, it generally is accepted that exercise and intense physical exertion through athletic participation increase the likelihood of sudden death for many disorders predisposing to SCA. Corrado et al. identified a 2.5 times relative risk factor for SCD due to sports activity in athletes versus an age-matched nonathletic population (9).
On the other hand, although not all children are considered competitive athletes, all children are active and athletic in some way. Activities other than organized club, high school, collegiate, and professional sports can increase the risk of SCA, and certainly multiple cases of pediatric SCA have been documented during school physical education classes and other recreational sporting activities. This raises the concern as to whether a greater focus on cardiovascular screening should be reserved only for competitive athletes or better incorporated into routine well-child care (5).
Disorders such as LQTS and CPVT typically present at a younger age, often younger than 10 yr of age. Postponing preparticipation evaluation until high school or college, therefore, may underdetect these patients and families at risk. An alternative or complementary cardiovascular risk assessment process included throughout the well-child continuum has been proposed (5). This assessment can be initiated for any patient of any age by any care provider at any time. The form incorporates similar questions as the American Heart Association preparticipation guidelines and the PPE Monograph (2,37), as well as family history questions about specific genetic disorders known to predispose to SCA, accidental deaths, near drowning, congenital deafness, and unexplained seizure activity (5,37).
Patients and family members must assume responsibility for providing accurate and detailed family and patient history information. Care providers should be guided by a standardized history questionnaire and be aware of the disorders that predispose a patient to pediatric and young adult SCA and the possible presenting symptoms, including potential symptoms or misdirects that commonly are attributed to organ systems other than the heart, such as unexplained seizure activity or respiratory symptoms. Recommended personal and family history questions are listed in Table 2.
HOW SHOULD WE SCREEN?
History and Physical With or Without ECG
A substantial challenge to screening is that most apparently healthy athletes with unsuspected cardiovascular disease are asymptomatic. Sudden death is the first clinical manifestation of cardiac disease in up to 60%-80% of athletes with SCD (4,36,46). While there is general agreement that conducting a comprehensive personal and family history and physical examination is important during screening, the sensitivity of a history and physical examination alone is limited. No study to date monitoring SCD has shown that a preparticipation evaluation based on history and physical examination can detect athletes at risk and prevent sudden death.
The value of adding noninvasive cardiovascular tests such as ECG to the screening process in athletes is widely debated (6,39). In 2007, the American Heart Association reaffirmed its recommendations against universal ECG screening in athletes, citing a low prevalence of disease, poor sensitivity, high false positive rate, poor cost-effectiveness, and a lack of clinicians to interpret the results (37). In contrast, the European Society of Cardiology (13), International Olympic Committee (26,27), and the governing associations of several U.S. and international professional sports leagues endorse the use of ECG in the preparticipation screening of athletes. These recommendations are supported by studies showing that ECG is more sensitive than history and physical examination alone in identifying athletes with underlying cardiovascular disease. One study found that electrocardiography had a 77% greater power than history and physical examination to detect HCM (11). It is well established that 95% of individuals with HCM and 80% of individuals with ARVC exhibit electrocardiographic abnormalities (7,28,35).
In 2006, Corrado et al. reported data from a national preparticipation screening program in Italy in 42,386 athletes over 25 yr of age (8). It found that disqualification on the basis of a standardized history, physical examination, and ECG produced a 10-fold reduction in the incidence of SCD in young, competitive athletes and an 89% reduction of SCD as a result of cardiomyopathy (8). Although only 0.2% of athletes were disqualified for potentially lethal cardiovascular conditions, the study reported a 7% false positive rate and a 2% overall disqualification rate (8). This raised concerns that adopting such a program would lead to an unacceptable number of disqualifications in athletes with a low risk of SCD (47).
Challenges and Considerations
When evaluating the potential value or limitation of including ECG in a screening protocol, it is critical to recognize that the total-positive and false positive rates for any ECG screening study or practice are immensely affected by the criteria chosen to define "abnormal." There is an urgent need for uniform terminology when describing ECG findings in athletes (16). Many ECG changes once referred to as abnormal are now recognized as physiologic and part of benign cardiac adaptation in athletes (so-called "athlete's heart"). Physicians interpreting ECGs in athletes should be familiar with common training-related ECG alterations that are normal variants. In contrast, training-unrelated ECG changes suggest the possibility of underlying pathology, require further diagnostic workup, and should be considered abnormal. Recently, Corrado et al. eloquently summarized the current understanding of ECG interpretation in athletes and provided modern recommendations to distinguish pathologic ECG abnormalities from physiologic ECG alterations in athletes (12,14). A summary of these recommendations is provided in Tables 3 and 4.
An initial screening study performed in the United States more than two decades ago reported a false positive rate of 15% (31). However, more recent studies applying modern, strict ECG criteria to screen athletes have resulted in substantially lower false positive rates. Pelliccia et al. reported on 32,652 ECGs in young amateur athletes (median age 17 yr, range 8-78 yr), and distinct ECG abnormalities suggesting cardiac disease were found in only 4.8% of athletes (42). In a study of 2720 competitive athletes and physically active school children in the United Kingdom, Wilson et al. reported a false positive rate of 3.7% using history, physical examination, and ECG, with only 1.9% of false positives determined by ECG alone (49). In this study, nine athletes (0.3% of those screened) were found to have a cardiovascular condition known to cause SCD in the young, and all of these athletes were detected by ECG and not by history or physical examination (49). Nora et al. reported preliminary findings of ECG screening in 9125 young adults (aged 14-18 yr) from the Midwest region of the United States (40). This is the largest study to date of ECG screening in a U.S. population and found only 2% of ECGs to be abnormal using modern ECG criteria (40). The authors concluded that ECG screening of high school students resulted in an acceptable proportion of abnormal findings, and the types of abnormalities detected often were of clinical significance. A recent review by Papadakis and Sharma proposes that appropriate adjustment of the recommended European Society of Cardiology 12-lead ECG criteria published in 2005 would reduce the false positive rate to as low as 2% when screening competitive athletes (41). These studies using modern ECG criteria were performed by physicians with extensive experience in ECG interpretation, and it remains uncertain whether the results can be extrapolated to a general population of health care providers with less experience in ECG interpretation.
For those considering or conducting ECG screening, the timing and frequency of ECG screening in athletes needs to be determined, especially when considering the cost implications of mass screening. With no U.S. recommendations to guide the frequency of ECG screening, one potential approach would be to perform an ECG upon entry to high school athletics (age 14 yr) and again upon entry to college or elite athletics as a supplement to the existing guidelines for a PPE based on history and physical examination (17).
WHERE DO WE GO FROM HERE?
Future Considerations and Remaining Questions
Many challenges remain regarding SCD prevention that must be addressed through further research and education. Unfortunately, even past screening recommendations that are universally endorsed, such as the use of a comprehensive personal and family questionnaire to guide the preparticipation evaluation, have not been widely adopted, and recommended screening protocols are often incompletely or inadequately implemented (22-24). Improved education of primary care and sports physicians conducting these evaluations regarding the warning symptoms and family history that may indicate the presence of a lethal cardiovascular abnormality is needed. Research to determine the sensitivity and specificity of screening personal and family history questions also is needed and may shape future recommendations. It also would be valuable to better define the true incidence of SCA/SCD in young athletes through improved methodology and reporting systems; however, a national mandate to develop a registry for causes of juvenile sudden death has not occurred, and the resources are hard to define.
Inclusion of ECG in the screening protocol will improve detection of those at risk with potentially serious cardiovascular disorders. However, feasibility and practical concerns still exist regarding large-scale implementation of ECG screening in the United States. Who will pay for and interpret the ECGs? What is the long-term result of disqualifying athletes with cardiovascular disease at an increased but unquantifiable risk for SCD? Clearly, large-scale, outcome-based and health-economic research is needed in larger populations of athletes to better define the true prevalence of disease, the cost of the screening process, the cost of investigating false positives and true positives through subsequent testing, and the potential reduction of SCD through withdrawal from athletic participation and other management interventions. The cost-effectiveness of any screening protocol (i.e., history, physical examination, and/or ECG) will be influenced by both physician competency and response to abnormal or borderline findings. Education of primary care providers, sports medicine physicians, and cardiologists in accurate ECG interpretation in athletes using modern ECG guidelines is essential before widespread implementation of ECG screening can occur with an appropriate accuracy and acceptable false positive rate. However, to confront these challenges we must move beyond a debate grounded in incidence estimates and false positive rates that derive from studies with vastly different methodologies and terminologies, and move to a discussion of physician education and practical challenges and improvements to our current health system infrastructure. Until then, the debate on ECG screening and discordance between recommendations from U.S. and European authorities likely will continue.
Studies demonstrating the effectiveness of cardiovascular screening using only history and physical examination are lacking. However, warning signs and symptoms may be present in children or families affected by cardiovascular diseases that predispose to SCA, and thus a cardiovascular risk assessment process that includes a structured and comprehensive history should be incorporated into any preparticipation evaluation, as well as the continuum of well-child care. Addition of a resting 12-lead ECG to the screening process for young athletes will increase detection of those with occult cardiovascular disorders at risk for sudden death and more effectively fulfill the primary objective of preparticipation cardiovascular screening. However, ECG interpretations using modern criteria to distinguish abnormal findings from physiologic alterations in athletes must be used to ensure acceptable accuracy, and athletes with abnormal findings should be referred for appropriate diagnostic testing and cardiology consultation. With no national guidelines and continued debate regarding the utility of ECG screening, implementation of ECG screening remains at the discretion of the physician and likely influenced by individual physician confidence and available resources. Complex issues regarding infrastructure, cost-effectiveness, and physician education remain that must be addressed through further research if widespread ECG screening is to be pursued in the United States.
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