INTRODUCTION
Sudden cardiac death (SCD) in a competitive athlete is a tragic event that can have dramatic reactions in the community. Recommendations from expert panels have proposed a preparticipation examination (PPE), which aims to prevent these sudden deaths in young athletes. Establishing screening PPE guidelines is especially difficult given the extremely low incidence of cardiac events, roughly 1 in 200 000 athlete years.1 Screening guidelines that are too broad and inclusive result in a delay in participation and unnecessary cost.
For these reasons, expert panels have different recommendations for what composes the PPE, specifically regarding the use of the screening electrocardiogram (ECG). European guidelines recommend use of the screening ECG based on studies in Italy that suggested a reduction in cardiac deaths.2,3 However, this potential reduction in cardiac deaths is offset by the extremely high number of athletes excluded from participation, amounting to roughly 680 for every life saved.4 For these reasons, American guidelines do not recommend use of the screening ECG because of its potential to increase the number of healthy athletes who screen positive.5
Although controversy remains regarding the screening ECG, all experts agree that the preparticipation screening should include a cardiovascular-oriented history and physical examination. The most current American Heart Association (AHA) guidelines from 2007 recommend performing the cardiovascular-oriented history and physical examination using 12 elements, which consist of 8 questions pertaining to the personal and family history and 4 findings from the physical examination (Table 1 ).5 A positive response to any of the 12 elements, at the discretion of the examiner, can trigger a referral for further cardiovascular evaluation.
TABLE 1: The 12-Element AHA Recommendations for Preparticipation Cardiovascular Screening of Competitive Athletes
Few studies have addressed the rate of positive responses to the AHA 12-elements along with the screening ECG. In this article, we examine the rate of abnormalities obtained for the 8 personal and family history elements along with 3 different screening ECG criteria. We then propose a new set of screening guidelines that aim to reduce the number of healthy athletes who screen positive and potentially lessen the number of athletes who suffer cardiac events.
METHODS
Study Population
The study population consisted of 297 athletes from several high schools, 1016 athletes from a single college, and 283 athletes from 2 professional sport teams, all in the San Francisco Bay Area. Consent was obtained from each participant through a consent form approved by the Stanford Investigational Review Board. All athletes completed a questionnaire that included the 8 personal and family history items from the AHA 12-elements. The questionnaire was administered by either Stanford Sports Medicine staff or medical volunteers who were familiarized with the AHA personal and family history questions. Responses to each of the 8 personal and family history elements were recorded along with their age, gender, race, and sport. Athletes with a positive response to one of the 8 personal and family questions were interviewed by an experienced sports medicine physician to determine clinical significance. Nine athletes were referred to a specialist for further evaluation based on their clinical history.
Statistical Analysis
All data were stored and analyzed using NCSS 9 software (NCSS, LLC, Kaysville, Utah). All categorical values were statistically analyzed using the χ2 test. A P value of <0.05 was used to determine statistical significance.
ECG Analysis
Electrocardiograms were obtained for all participants using CardeaScreen, a handheld ECG device designed for use in young athletes (Cardea Associates Inc, Seattle, Washington). CardeaScreen's user interface includes the opportunity for athletes to complete the AHA personal and family history questionnaire. CardeaScreen has been validated through comparison to 2 other commercial ECG devices and has been approved by the FDA. Electrocardiograms were interpreted using the Seattle criteria, Stanford criteria, and ESC recommendations, which aim to distinguish pathological disease from normal physiologic adaptation in an athlete's heart.6,7 Athletes with an abnormal ECG by either Stanford or Seattle criteria underwent evaluation with an echocardiogram. All ECGs were reviewed for accuracy by an expert in sports cardiology.
RESULTS
Study Population
A total of 1596 athletes across 21 sports participated in this study. Sports varied in cardiovascular demand and therefore risk of SCD, from low risk sports like golf and fencing to high-risk sports, such as basketball and football. The majority of high school and college athletes participated in football, basketball, or crew/rowing. All of the professional athletes were male football and basketball players, whereas the percentages of male high school and college athletes were 56% and 53%, respectively (Table 2 ). The average age for each class was 16.2 for high school, 18.8 for college, and 26.3 for professional athletes. Most of the athletes enrolled were white (64.5%), whereas other races included African American (19.3%), Asian (9.8%), Hispanic (4.1%), Pacific Islander (1%), Native American (0.4%), and other (1.0%).
TABLE 2: Baseline Characteristics of Study Population
Responses to AHA Personal and Family History Elements
The total number of positive responses by class can be found in Table 3 . Of 1596 athletes who completed the AHA personal and family history questionnaire, 380 (23.8%) had at least 1 positive response and 109 (6.8%) had at least 2 positive responses (Table 4 ).
TABLE 3: Total Number of Positive Responses by Class
TABLE 4: Aggregate Sum of Positive Responses by Class
The personal and family history elements that had the most positive responses included unexplained syncope or near syncope (8.0%), excessive exertional dyspnea associated with exercise (7.1%), and exertional chest pain/discomfort (5.1%). The other 5 personal and family history elements had a positive rate between 1.6% and 3.3% (Table 5 ).
TABLE 5: Number and Percentage of Positive Responses by Class
High school and college athletes had similar rates of having at least 1 positive response (25.9% vs 27.4%), whereas professional athletes had a significantly lower rate of having at least 1 positive response (8.8%, P < 0.05). Compared with high school males, professional athletes had fewer positive responses to exertional chest pain (0.4% vs 6.6%, P < 0.05), excessive exertional dyspnea with exercise (1.1% vs 7.2%, P < 0.05), disability from heart disease in a close relative (0.7% vs 7.8%, P < 0.05), and specific knowledge of certain cardiac conditions in family members (1.8% vs 9.6%, P < 0.05). Compared with college males, professional athletes had fewer positive responses to exertional chest pain (0.4% vs 4.6%, P < 0.05), unexplained syncope or near syncope (2.1% vs 8.5%, P < 0.05), excessive exertional dyspnea with exercise (1.1% vs 5.7%, P < 0.05), and prior recognition of heart murmur (0.7% vs 4.3%, P < 0.05) (Table 6 ).
TABLE 6: Number and Percentage of Positive Responses in Males by Class
High school and college males had similar rates of positive responses to each of the personal history elements (Table 7 ). However, high school males, when compared with college males, had more positive responses to each of the family history elements, which included premature cardiac death in a young relative (6.6% vs 2.4%, P < 0.05), cardiac disability in a young relative (7.8% vs 0.7%, P < 0.05), and family history of certain cardiac conditions (9.6% vs 3.0%, P < 0.05). The responses to the family history elements continue to remain statistically significant when the comparison of high school and college athletes includes both males and females.
TABLE 7: Number and Percentage of Positive Responses in High School and College Athletes by Sex
When excluding the professional athletes, comparison of males with females shows that overall there was no difference in the number of athletes who had 1 or more positive responses (25.4% vs 28.9%, P = 0.17). However, female athletes had more positive responses to unexplained syncope or near syncope (11.4% vs 7.5%, P = 0.017) and excessive exertional dyspnea associated with exercise (11.1% vs 6.1%, P = 0.001) when compared with male athletes.
Screening ECG
Of 1596 athletes who received a screening ECG, 95 (6.0%) were judged to have an abnormal ECG based on Seattle criteria, 78 (8.8%) based on Stanford criteria, and 428 (26.8%) based on European Society of Cardiology criteria.8
Only 22 athletes (1.4%) had both an abnormal ECG based on Seattle criteria and had at least 1 positive response to the AHA personal and family history elements. Similarly, only 38 athletes (2.4%) had both an abnormal ECG based on Stanford criteria and at least 1 positive response. This is in contrast to the 98 athletes (6.1%) that had both an abnormal ECG based on ESC criteria and had at least 1 positive response.
Several athletes in this study population were judged to have an abnormal ECG and did undergo further diagnostic workup, including consultation with a sports cardiologist, exercise stress test, echocardiography, and/or cardiac magnetic resonance imaging (MRI). However, no athlete was found to have a clinical condition precluding participation, and to date, no athlete within this cohort has experienced an adverse cardiac event.
DISCUSSION
Based on these results, there are a number of concerns with the AHA 12-elements that warrant the development of a new set of screening guidelines. For 1, the AHA personal and family history elements, even when not including the 4 physical examination elements, yield a very high rate of positive responses. According to our results, approximately 25% of all athletes screened using AHA personal and family history elements would be referred for cardiovascular evaluation according to the current guidelines. Of the 10 million athletes eligible for screening in the United States each year, approximately 2.5 million athletes would be referred for further cardiovascular evaluation if they were screened using the AHA 12-elements alone.5 This is in contrast to the extremely low incidence of SCD in athletes, which is roughly 300 people per year.4
Similarly, the screening ECG when interpreted using the European Society of Cardiology recommendations also yields a high rate of athletes who screen positive. Just over 25% of athletes screened in this study were flagged as abnormal based on ESC recommendations. Interpretation of the screening ECG using the Seattle criteria and Stanford criteria lowered the number of ECGs flagged as abnormal to 6% and 8.8%, respectively. For this reason, we believe that the Seattle criteria and the Stanford criteria are preferred over ESC recommendations for ECG interpretation.
Another concern regarding the AHA 12-elements is the amount of variability in the responses obtained from different groups of athletes. Most striking is the significantly lower percentage of professional athletes who had any positive responses to the AHA personal and family history elements. Several hypotheses could potentially explain this finding. To start, professional athletes have a financial incentive to ensure that they participate in athletic competition. Professional athletes may fear that having a positive response to one of the AHA 12-elements could potentially limit their athletic participation and consequently lead to negative financial consequences. In addition, athletes with cardiac conditions that could lead to the symptoms described in the AHA personal history elements may have been selected out of the population before they reached the professional level.
The responses to the AHA personal and family history elements also varied based on gender. Specifically, females reported increased episodes of syncope/near syncope and excessive dyspnea with exercise, both of which are consistent with findings from previous studies.9,10 Syncope in adolescents and young adults has been shown to peak at 15 years of age and is about twice as common in females than males.9 Most syncopal events in the young adult population are benign and simply require reassurance. However, syncope that occurs during or after exertion in an otherwise healthy athlete is thought to be more likely caused by an organic etiology, such as hypertrophic cardiomyopathy (HCM) or arrhythmogenic right ventricular cardiomyopathy (ARVC).11 Therefore, the context of the syncopal event is vital to capture the at-risk population.
When compared with college athletes, high school athletes had similar rates of positive responses to the personal history elements but had more positive responses to the family history elements. This could be because high school athletes are more likely to be accompanied by their parents or other relatives who have more knowledge of the athlete's family history. In addition, high school athletes may have less medical literacy and may misinterpret the medical terminology associated with the screening PPE.
Overall, the AHA 12-elements have excessive positive responses, roughly 25% of athletes screened, which make it an inappropriate screening test. For this reason, the history and physical examination components that compose the PPE need to be revised to be more specific with a much lower rate of false positives. We therefore propose a new set of questions that should not only be more specific but also include several updates based on recent findings (Table 8 ).
TABLE 8: The Stanford 12-Elements for Preparticipation Cardiovascular Screening of Competitive Athletes
The Stanford 12-elements start by asking the participant if they have ever been diagnosed with any cardiac condition that could increase their risk of SCD. The full list of these cardiac conditions can be found in Table 8 . Although this question may seem obvious, many athletes undergo their PPE at mass screening events, often with the help the volunteers. Given this, 1 question should be dedicated to asking the athlete if they have any life-threatening condition so that they may be taken out of the general screening process.
Participants are then screened for any subjective symptoms that could represent precursors to SCD. These symptoms include chest pain, syncope, seizure, dyspnea, and palpitations. These symptoms should be included in the PPE as several studies have shown them to precede episodes of sudden death.12 Importantly, these symptoms must occur either during or after exercise. Adding this qualifier should limit the number of athletes who screen positive without decreasing the sensitivity.
The next several elements ask about prior clinical investigations. Prior restriction from participation for a medical problem not related to the musculoskeletal system raises a red flag and requires further evaluation. Prior recognition of a murmur, high blood pressure, arrhythmia, or any other heart problem in a competitive athlete is unusual and could suggest an underlying and potentially life-threatening cardiac disease. In addition, prior cardiac diagnostic testing including an ECG or imaging with ECHO/CT/MRI suggests workup of a prior abnormality requiring comprehensive review before return to athletic participation.
Screening for family history is extremely important as many conditions that lead to SCD are inherited. The athlete's relative must be aged 40 years or younger at the time of an event to qualify. This improves specificity since most sudden deaths over age 40 are due to coronary artery disease, a rare cause of death in young athletes.13
The first family history question asks the athlete if they have any relative with a known heart problem including an arrhythmia or inherited cardiac condition. The second family history question asks the athlete if they have any relative who died suddenly, including unusual circumstances, such as driving, drowning, or sudden infant death syndrome, received CPR or had a cardiac arrest, or had a history of seizures. The third family history question asks the athlete if they have any relative who had a defibrillator or pacemaker placement. The second and third family history questions indirectly search for an SCD event as many times the diagnosis of an underlying cardiac condition cannot be found or may not be known to the athlete.
The only physical examination finding included in the Stanford 12-elements is the presence of a pathological murmur. We agree with prior recommendations that any diastolic murmur or a systolic murmur louder than soft should be worked up further with echocardiography and/or referral.14 Given that HCM can cause SCD in athletes, any systolic murmur consistent with HCM, such as increases with Valsalva, should be considered abnormal and that athlete should undergo cardiology referral. In addition, any murmur consistent with mitral regurgitation or mitral valve prolapse should be considered pathologic.
Notably, the Stanford 12-elements do not include blood pressure measurement as it is routinely performed during the examination. Also, the Stanford 12-elements do not include assessment of Marfan syndrome stigmata or femoral pulses looking for coarctation of the aorta.
Overall, the Stanford 12-elements proposed in this article are a blend of the AHA 12-elements and fourth PPE CV questions but in general are more specific and include updates based on the recent literature. We plan to implement the Stanford 12-elements in our PPE along with the screening ECG. Future studies are needed to determine whether the Stanford 12-elements acceptably reduce the number of healthy athletes who screen positive without decreasing the sensitivity of the screening PPE.
Limitations
This is an observational study that was limited to athletes participating around the area of San Francisco, CA. Results of this study may not be generalizable to other regions.
CONCLUSIONS
The current AHA screening recommendations lead to an excessive number of athletes who screen positive, and results of screening ECGs vary broadly by interpretation criteria. Because the reaction to a positive response is not standardized, this may lead to variation in practice, along with unnecessary cost and delay. Newer screening guidelines are needed, with fewer false positives and evidence-based updates. The Stanford 12-elements will hopefully achieve this, and if validated, should be considered for wider application.
REFERENCES
1. Maron BJ, Gohman TE, Aeppli D. Prevalence of sudden cardiac death during competitive sports activities in Minnesota high school athletes. J Am Coll Cardiol. 1998;32:1881–1884.
2. Corrado D, Pelliccia A, Bjornstad H, et al.. Study group of sport cardiology of the working group of cardiac rehabilitation and exercise physiology and the working group of myocardial and pericardial diseases of the European Society of Cardiology. Cardiovascular pre-participation screening of young competitive athletes for prevention of sudden death: proposal for a common European protocol. Eur Heart J. 2005;26:516–524.
3. Corrado D, Basso C, Pavei A, et al.. Trends in sudden cardiovascular death in young competitive athletes after implementation of a preparticipation screening program. JAMA. 2006;296:1593–1601.
4. Halkin A, Steinvil A, Rosso R, et al.. Preventing sudden death of athletes with electrocardiographic screening. J Am Coll Cardiol. 2012;60:2271–2276.
5. Maron B, Thompson P, Ackerman M, et al.. Recommendations and considerations related to preparticipation screening for cardiovascular abnormalities in competitive athletes: 2007 update: a scientific statement from the American Heart Association council on nutrition, physical activity, and metabolism: endorsed by the American College of Cardiology Foundation. Circulation. 2007;115:1643–1655.
6. Drezner J, Ackerman M, Anderson J, et al.. Electrocardiographic interpretation in athletes: the “Seattle criteria”. Br J Sports Med. 2013;47:122–124.
7. Corrado D, Pelliccia A, Heidbuchel H, et al.. Recommendations for interpretation of 12-lead electrocardiogram in the athlete. Eur Heart J. 2010;31:243–259.
8. Pickham D, Zarafshar S, Sani D. Comparison of three ECG criteria for athlete pre-participation screening. J Electrocardiol. 2014;47:769–774.
9. Kenny R, Bhangu J, King-Kallimanis B. Epidemiology of syncope/collapse in younger and older western patient populations. Prog Cardiovasc Dis. 2013;55:357–363.
10. Ofir D, Laveneziana P, Webb K, et al.. Sex differences in the perceived intensity of breathlessness during exercise with advancing age. J Appl Physiol (1985). 2008;104:1583–1593.
11. O'Connor F, Oriscello R, Levine B. Exercise-related syncope in the young athlete: reassurance, restriction or referral? Am Fam Physician. 1999;60:2001–2008.
12. Corrado D, Basso C, Thiene G. Sudden cardiac death in young people with apparently normal heart. Cardiovasc Res. 2001;50:399–408.
13. Eckart R, Shry E, Burk A, et al.. Sudden death in young athletes: an autopsy-based series of a population undergoing active surveillance. J Am Coll Cardiol. 2011;58:1254–1261.
14. McConnell M, Adkins S, Hannon D. Heart murmurs in pediatric patients: when do you refer? Am Fam Physician. 1999;60:558–564.