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Centre of Sports Medicine, Division of Physical and Rehabilitation Medicine, Lausanne University Hospital, SwitzerlandCentre for Primary Care and Public Health (Unisanté), University of Lausanne, SwitzerlandSportAdo Centre, Department of Woman-Mother-Child, Lausanne University Hospital, Switzerland
Athletes performing sports on high level are at increased risk for sudden cardiac death. This includes paediatric athletes, even though data on screening strategies in this age group remain scarce. This study aimed to assess electrocardiogram interpretation criteria in paediatric athletes and to evaluate the cost of screening.
Methods
National, multicentre, retrospective, observational study on 891 athletes of paediatric age (<18 years) evaluated by history, physical examination and 12-lead electrocardiogram. The primary outcome measure was abnormal electrocardiogram findings according to the International Recommendations for Electrographic Interpretation in Athletes. The secondary outcome measure was cost of screening.
Results
19 athletes (2.1%) presented abnormal electrocardiogram findings requiring further investigations, mainly abnormal T-wave inversion. These 19 athletes were predominantly males, performing endurance sports with a mean volume of 10 weekly hours for a mean duration of 6 years of training. Further investigations did not identify any relevant pathology. All athletes were cleared for competition with regular follow-up. Total costs of the screening were 108,860 USD (122 USD per athlete).
Conclusions
Our study using the International Recommendations for Electrographic Interpretation in Athletes identified a low count of abnormal findings in paediatric athletes, yet raising substantially the cost of screening. Hence, the utility of electrocardiogram-inclusive screening of paediatric athletes remains to be elucidated by longitudinal data.
Of the 891 paediatric athletes (mean age 14 years), 3.8% had abnormal findings, identified by history, physical examination and 12-lead electrocardiogram (ECG).
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2.1% presented abnormal ECG findings according to the International Recommendations for Electrographic Interpretation in Athletes, resulting in a low rate of subsequent downstream investigations.
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Subsequent assessment failed to identify any pathology questioning the utility of general ECG screening in the paediatric age range.
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The cost of screening was 122 USD per athlete.
1. Introduction
Pre-participation screening for athletes continues to be a matter of debate. Often cited arguments against routine electrocardiogram (ECG) screening include lack of definitive outcome data, imperfect sensitivity and specificity, cost, difficulties with quality control and ethical issues.
Accuracy of the ECG for differential diagnosis between hypertrophic cardiomyopathy and athlete’s heart: comparison between the European Society of Cardiology (2010) and International (2017) criteria.
During childhood and adolescence, the heart is continuously developing. Major steps in cardiovascular growth and development occur during puberty, resulting in slightly less pronounced cardiac adaptations to exercise in pre-pubertal athletes.
It therefore remains to elucidate whether diagnostic ECG criteria targeting adult athletes can be applied to the paediatric population. A meta-analysis demonstrated that paediatric athletes gather more training related and training unrelated ECG changes than non-athletes.
These modifications are mainly influenced by chronological age and ethnicity with more changes in athletes older than 14 years and of Afro-Caribbean ethnicity.
in a paediatric population and to investigate the financial implications of this screening program. We hypothesised that due to the phenotypical emergence of SCD related disease with age, the rate of abnormal electrocardiographic findings in paediatric athletes would be lower compared to adult data with subsequently higher costs per finding.
2. Methods
We enrolled 891 athletes between 2011 and 2017 undergoing single, first-time preparticipation cardiovascular screening from six medical centres in Switzerland: Lausanne, Bern (in collaboration with the Swiss Federal Institute of Sports Magglingen), Geneva, Zurich, Bellinzona and Lugano. Inclusion criteria included age less than 18 years, sport participation at an international, national or regional level, and minimal training frequency of 6 h per week. We excluded individuals with known heart disease. The Swiss Ethics Committee approved the study protocol (Project No 2018-00121). Given the fact that the participants were included retrospectively, the Swiss Ethics Committee declared that no retroactive consent of the single participants was required.
The following parameters were collected: age, sex, ethnicity, weight, height, body mass index (BMI), body fat mass, sport type, training volume in weekly hours, duration in years of training, level of performance, sports category according to the Mitchell criteria,
personal and family medical history, physical examination, resting heart rate and resting blood pressure.
Medical history consisted of screening for cardiovascular symptoms such as chest pain, palpitation, dyspnoea and prior syncope. Family history included structural heart disease, primary arrhythmia and sudden cardiac death (SCD). Physical examination aimed at the detection of Marfanoid features, arterial hypertension, cardiac murmurs, and aortic coarctation. Arterial hypertension was defined as proposed by the American Academy of Pediatrics.
A 12-lead ECG was performed and analysed by the treating sports physician and/or cardiologist. All ECGs were reviewed in each centre by an experienced sports cardiologist. ECG analysis aimed to differentiate normal ECG adaptations from patterns suggestive of disease and was retrospectively analysed according to the International Recommendations for Electrocardiographic Interpretation in Athletes.
Athletes with abnormal medical history, physical examination or ECG findings (two borderline or one abnormal) were subject to further investigations at the discretion of the treating physician, including transthoracic echocardiography, 24 h-Holter monitoring, maximal exercise stress testing, cardiac magnetic resonance imaging (MRI), 24 h blood pressure monitoring or ECG with pharmacological exposure. In cases where criteria for borderline or abnormal ECG findings were equivocal, the ECG was repeated on a different appointment. Further cardiology work-up was only performed if the initial finding could be reproduced. Even though ECG analysis by the time of medical consultation relied on the use of contemporary ECG criteria, retrospective analysis by the International Recommendations for Electrographic Interpretation in Athletes in our study did not show any case of false-positive ECG findings based on less specific prior criteria, requiring unnecessary secondary examinations. In each study centre, the need for follow-up testing was determined by the consulting physicians and was not standardised. Exclusion from sports participation was based on additional examinations and shared decision making involving the treating physician, a cardiologist and/or a paediatric cardiologist.
Costs were calculated in Swiss francs according to the data of Menafoglio
Costs and yield of a 15-month preparticipation cardiovascular examination with ECG in 1070 young athletes in Switzerland: implications for routine ECG screening.
Costs and yield of a 15-month preparticipation cardiovascular examination with ECG in 1070 young athletes in Switzerland: implications for routine ECG screening.
Values are presented as either percentage or median with interquartile range [IQR]. In order to test the influence of quantitative variables on the percentage of ECG abnormalities, we used one-way ANOVA followed by Bonferroni multiple comparison procedure; or Kruskal-Wallis test followed by Dunn's test with Bonferroni procedure, if normality assumptions were not verified. For the influence of qualitative variable, as we expected small numbers of ECG abnormalities in our cohort, we used the Fisher's exact test for 2 × 2 tables and the Pearson χ2 test otherwise. Values of p < 0.05 were considered statistically significant. All statistical analysis was performed using NCSS (Number Cruncher Statistical System. 2013: Atlanta).
3. Results
We included 891 athletes with a mean age of 14.8 ± 1.6 (SD) years (range 8 to 17). Approximately two-thirds of the cohort were males (580; 65%) and nearly all were of Caucasian ethnicity (864; 97%). The 45 different sports represented all nine categories of the Mitchell classification.
High-dynamic moderate-static class sports (IIC) (366; 41%), and high-dynamic low-static class sports (IC) (194; 22%) accounted for the majority of athletes. Football was the most common single sport represented (158; 18%). The athletes performed on international (22%), national (34%) and regional (44%) level of competition. Training time was 10.8 ± 5.3 (SD) h per week and training duration was 6.5 ± 2.7 (SD) years.
History revealed cardiac symptoms in 15 athletes (1.7%) as follows at rest and/or with exertion: chest pain (n = 7), palpitation (n = 3), prior syncope (n = 3) and dyspnoea (n = 2). Family history of first-degree relatives was positive in 15 athletes (1.7%), thereof premature cardiac death (n = 1), dilated cardiomyopathy (n = 1) and Brugada syndrome (n = 1). Physical examination detected abnormalities suggestive of underlying cardiovascular disease in 19 athletes (2.1%) with the following findings: cardiac murmur (n = 10), arterial hypertension (n = 8), and irregular cardiac rhythm (n = 1). One athlete had abnormal history and physical examination. Three athletes had abnormal history and family history. Four athletes had abnormal family history and physical examination. Overall, there were 36 athletes identified without ECG.
Of the 891 athletes, 672 (75.4%) demonstrated normal findings on standard 12-lead ECG according to the International Recommendations for Electrographic Interpretation in Athletes, thereof 12.8% a juvenile pattern, i.e., T-wave inversion in leads V1–V3 under the age of 16 years. Thirty-eight (4.3%) fulfilled borderline criteria. Only two (0.2%) of them had two borderline criteria requiring further investigations. 17 (2.1%) athletes presented at least one abnormal finding as detailed below. Of the 36 athletes with abnormal history and physical examination, three had one borderline finding and two had an abnormal ECG finding. 21 of the 36 athletes with abnormal history and physical examination were not further investigated, since the abnormal findings were not suggesting severe disease. Overall, 34 (3.8%) athletes were deemed to require post-screening investigation after integration of data from medical history, physical examination, and 12-lead ECG.
The 2 athletes with two borderline findings presented both right axis deviation and complete right bundle branch block (RBBB). Of the 17 athletes with abnormal findings, 8 (47%) had isolated T wave inversion while only 1 had two abnormal criteria: T wave inversion and ST segment depression. The remaining abnormal findings were distributed as follows: premature ventricular contractions (n = 5; 29%), pathologic Q waves (n = 3; 18%) and prolonged QT interval (n = 1; 6%) (Table 2).
Table 2Detailed cohort characteristics of athletes with abnormal ECG findings.
Recommendations for participation in competitive sports of athletes with arterial hypertension: a position statement from the sports cardiology section of the European Association of Preventive Cardiology (EAPC).
All but one of the athletes with abnormal findings on ECG (two borderline or one abnormal) were of Caucasian ethnicity. Thirteen of the 19 athletes with abnormal ECG were males (68%) resulting in a similar male–female ratio compared to the whole cohort (65% male). The concerned athletes performed in 12 different types of sports. The predominant type of sport was football with 37% and thus twice more represented than in the whole cohort (18%).
When comparing athletes without ECG findings, training-related ECG, one borderline finding and abnormal ECG (including individuals with 2 borderline findings), the only differences were found for training volume and heart rate of athletes without ECG findings compared to training-related ECG (Table 3). When separating by age, we used a cut-off of 15 years to determine post-pubertal athletes, since Tanner stages were not available retrospectively. Athletes older than 15 years presented greater training volume (10.9 ± 5.3 vs 10.5 ± 5.4, p < 0.05) and duration of training (7.1 ± 2.7 vs 5.6 ± 2.5, p < 0.05).
Table 3Demographic, anthropometric, sport-related and clinical data of athletes classified by ECG findings according to the International Recommendations for Electrographic Interpretation in Athletes.
Among the athletes with abnormal personal or family history and/or physical examination but with normal ECG, further examinations were performed in 15 athletes including transthoracic echocardiography (n = 7), exercise testing (n = 6), 24 h blood pressure monitoring (n = 2), ECG with ajmaline challenge (n = 1), and 24 h-Holter monitoring (n = 1). No pathology was detected in any of these 15 athletes and all were cleared for sports participation.
The 19 athletes with abnormal ECG findings underwent transthoracic echocardiography (n = 12), 24 h-Holter (n = 7), exercise testing (n = 7) and cardiac MRI (n = 3). Athlete 8 (Table 2) with pathologic T wave inversion was found to have medio-mural apical fibrosis of the left ventricle on MRI which was considered an unspecific finding but could be suggestive of former myocarditis in an atypical localisation. Athlete 3 with pathologic T wave inversion had a mild posterior leaflet mitral prolapse with minimal insufficiency. Among the remaining 6 athletes with pathologic T wave inversion, including the one with additional ST segment depression, no diagnosis was established after comprehensive testing. Among the 5 athletes with premature ventricular contractions, no underlying cardiovascular disease was found. The remaining findings such as pathologic Q waves (n = 3), prolonged QT interval (n = 1), and two borderline ECG criteria (n = 2) could not be reproduced on follow-up ECG and long QT syndrome was ruled out. Consequently, no athletes in our cohort were excluded from competitive sport participation.
Follow-up data for athletes with abnormal history, physical examination and/or ECG were available for 24/34 (71%) of affected individuals with a mean duration of 3.8 years. Athlete 6 has been followed until now and recently had a wall thickness of maximally 14 mm. He was allowed to continue his sport with annual follow-up. Athlete 15 has been investigated for four years due to ventricular extrasystoles and a positive family history (premature SCD of his father). A recent electrophysiological study was performed because of palpitations and wide complex tachycardia on implantable cardiac monitor. It showed atrioventricular nodal re-entrant tachycardia with aberrant conduction enabling him to continue sport.
Costs for basic screening of the 891 athletes amounted to 96,416 USD (108 USD per athlete): history-taking 31,232 USD, clinical examination 39,907 USD, and 12-lead ECG 25,276 USD. Further examinations because of ECG findings increased the costs to 105,180 USD (118 USD per athlete). Further examinations because of abnormal history and physical examination amounted to 4157 USD (115 USD per athlete) (Fig. 1). Thus, the total costs of the program were 109,025 USD (122 USD per athlete). Screening confined to history and physical examination would have decreased the costs to 75,297 USD (85 USD per athlete) for basic screening excluding 12-lead ECG and further investigations.
Fig. 1Abnormal findings identified by history, physical examination and/or 12-lead ECG with cost calculation.
The cost of post-screening investigations for the 19 athletes with ECG included: transthoracic echocardiography = 3942 USD, exercise testing = 1156 USD, 24 h-Holter monitoring = 1439 USD, and cardiac MRI = 2227 USD. This represented 10 USD per athlete or 461 USD per athlete with abnormal ECG. Since there were no diagnoses associated with sudden cardiac death (SCD), costs per finding could not be calculated.
4. Discussion
This study was designed to determine the diagnostic yield and financial implications of ECG-inclusive screening among paediatric competitive Swiss athletes. Key findings can be summarised as follows: First, the rate of abnormal ECG findings based upon the International Recommendations for Electrographic Interpretation in Athletes requiring further investigations was low amounting to 2.1%. Second, none of the further evaluated athletes were diagnosed with an SCD related pathology. Thus, all athletes were cleared for competition. Third, ECG inclusion raised the costs per athlete by more than 30% compared to a screening program based on history and physical examination.
The guidelines of the Swiss Society of Sports Medicine for athletes screening were published first in 1998 and reinforced in 2010.
Task Force “Prevention of Sudden Death in Elite Sport” SGSM/SSMS 2010; the sudden cardiac death of a young athlete: recommendations for a sensible and effective preventive exam.
Schweizerische Zeitschrift für “Sportmedizin und Sporttraumatologie”.2011; 2: 108-109
They target athletes above 14 years and suggest preparticipation screening every 1–2 years including ECG, based on the fact that ECG was shown to detect conditions accounting for SCD in athletes in approximately two thirds of all cases.
History and physical examination remain the cornerstones of athlete screening. Nevertheless, at least 60% of conditions predisposing to SCD in young athletes are detected on ECG.
Pre-participation cardiovascular evaluation for athletic participants to prevent sudden death: position paper from the EHRA and the EACPR, branches of the ESC. Endorsed by APHRS, HRS, and SOLAECE.
The effectiveness of screening history, physical exam, and ECG to detect potentially lethal cardiac disorders in athletes: a systematic review/meta-analysis.
The recently published Canadian statement is an intermediary approach that argues against routine ECG and suggests a tiered approach in evaluating athletes.
Consequently, costs are reduced at the price of a higher rate of missed SCD related diseases.
If ECG screening is still a matter of debate in the adult population, there is no established strategy for children yet. With only 2.1% of abnormal ECG in our cohort we can conclude that the false positive rate is low and similar to older athletes.
In addition, the fact that non-invasive additional investigations allowed to clear all athletes is encouraging. Data from other studies on paediatric athletes confirm the trend of a low rate of abnormal findings in athletes under 18 years: Calo demonstrated in Italian male paediatric football players 2.9% of abnormal ECG.
This suggests that adult diagnostic criteria can be used in children without an unacceptable amount of false positive results. However, a study on paediatric athletes from the Middle East identified 8.2% of abnormal findings by ECG.
Given the lack of generalised follow-up in our cohort and the absence of universal imaging to exclude or detect occult disease we cannot comment on sensitivity and false negative rate. Nevertheless, the International Recommendations for Electrographic Interpretation in Athletes achieved high accuracy rates in adolescent football players.
Accuracy of the 2017 international recommendations for clinicians who interpret adolescent athletes’ ECGs: a cohort study of 11 168 British white and black soccer players.
None of the 891 athletes screened had a diagnosis associated with SCD. It therefore raises the question whether ECG screening is efficient in the paediatric population. The heart continues to develop during growth and ECG reflects dynamic changes during this period. Structural heart diseases are conditions that develop with age. Hypertrophic cardiomyopathy (HCM) and arrhythmogenic right ventricular cardiomyopathy (ARVC) are the most frequent SCD related structural diseases.
The genetic predisposition to develop these conditions is present at birth, but the morphological and electrical manifestation are often absent in children and young adults. This may require regular ECG in the screening strategy of this population. The best example for the emergence of cardiomyopathies with age is shown by athlete number 6 from Table 2. Based on his initially abnormal ECG, it took nine years of yearly follow-up to identify a left ventricular wall thickness (14 mm) which raised the suspicion of HCM, yet not confirmed. Of note, serial screening proved to increase the diagnostic yield of SCD related conditions by factor three compared to single screening.
It is worth to mention that the incidence of inherited heart disease varies between different countries. In the Italian study that had presented a decline of 89% in SCD after implementation of a mandatory ECG-inclusive screening for athletes, ARVC was the predominantly diagnosed condition.
Populations of other countries, like the US, seem to bare another genetic profile with HCM being the most common identified cause for SCD in the young athlete.
These geographical differences need to be taken into account before implementing a general screening program in a paediatric population. It is not appropriate to screen children for a condition that does not manifest before adulthood. However, in recent series of SCD, the origin remained predominantly undetermined with a structurally normal heart at autopsy.
All of the athletes were screened first by history and physical examination. Interestingly, between the 36 athletes with abnormal history and physical examination and the 19 athletes with abnormal ECG, there were only two overlapping. One may argue that limiting ECG screening to athletes with positive history and physical examination might have reduced our rate of false-positive findings, thus reducing cost. However, the sensitivity of clinical parameters alone to detect sinister conditions is insufficient.
Performance of the American Heart Association (AHA) 14-point evaluation versus electrocardiography for the cardiovascular screening of high school athletes: a prospective study.
Therefore, early identification of underlying (cardiac) disease also allows guiding young individuals towards their future career.
As stated in the above-mentioned study by Malhotra on adolescent football players in the UK, the rate of SCD related disorders on one-time screening was very low.
Comparable to our study, for 2% of abnormal findings on initial screening, no diagnosis could be established. However, long-term follow-up (mean 10.6 years) demonstrated several missed fatalities, resulting in an SCD-rate in screened athletes of 6.8/100,000 athletes. We therefore believe that follow-up is of paramount importance in screening athletes in the paediatric age range, notably in post-pubertal individuals.
In this controversial debate on ECG inclusion, cost is often cited as an additional concern: according to reports from the US, nationwide inclusion of ECG would increase the costs to several billions of dollars.
Assessment of the 12-lead ECG as a screening test for detection of cardiovascular disease in healthy general populations of young people (12–25 years of age): a scientific statement from the American Heart Association and the American College of Cardiology.
However, these calculations do not consider the increased sensitivity and specificity of the most recent International Recommendations for Electrographic Interpretation in Athletes.
A study from the UK demonstrated a 27% cost reduction by the International Recommendations for Electrographic Interpretation in Athletes compared to the 2010 ESC criteria.
In 42% of abnormal history and physical examination in our cohort, further investigations other than ECG were performed. This contrasted to 63% in the group of abnormal ECGs who had at least one further investigation. Even though ECG increases the absolute cost of screening, it proved to be more cost-effective than history and physical examination only.
Comparison of cardiovascular screening in college athletes by history and physical examination with and without an electrocardiogram: efficacy and cost.
Another important factor to be considered is the timing of secondary investigations, keeping athletes away from training and thus potentially interfering with their sports career. In this ongoing debate, it should be emphasised that screening young athletes, in addition to risk stratification, offers a unique opportunity to address the specific issues of athletes' health like injury prevention, overtraining, doping and to assess potential problems of the adolescent population like eating disorders or fatigue.
In this study, we respond to the urgent demand for more data on ECG screening in young athletes.
However, we admit several limitations. Firstly, only athletes who were part of an organised screening program were included. This may cause a selection bias. Secondly, nearly all athletes included were Caucasians. Thus, the often-addressed ethnical impact on electrocardiographic findings could not be evaluated.
Thirdly, due to the retrospective, multicentre nature of the study, we did not use standardised medical history, physical examination or ECG protocols and moreover referral and choice of further investigations were based on local attitude. Fourthly, although this is one of the biggest studies in elite paediatric athletes, still the number is small when considering the prevalence of SCD related conditions in young individuals, reported as 1 in 300.
Finally, we were unable to obtain follow-up data in a significant proportion of athletes referred for further evaluation, raising the possibility that we may have missed some diagnoses.
In conclusion, the low rate of abnormal ECG findings suggests that adult criteria can be used in paediatric athletes. The lack of correlation with the presence of relevant disease in a broad paediatric population and the absence of diagnosis of SCD related conditions on single screening underline the need for regular follow-up. With further investigations taken into account, adding ECG to history and physical examination increased the cost of screening from 85 to 122 USD. Our data may be helpful in the development of cardiac screening programs in paediatric athletes. Future policy makers should carefully assess the diagnostic yield and costs of individual screening modalities and adopt the most cost-efficient strategy. Prospective follow-up data are needed to elucidate long-term evolution of these athletes starting their sports career in early life.
Funding information
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Declaration of interest statement
The authors have no interest to declare.
Confirmation of ethical compliance
The authors followed the WMA Declaration of Helsinki – Ethical Principles For Medical Research Involving Human Subjects.
The Swiss Ethics Committee approved the study protocol (Project No 2018-00121).
Acknowledgement
No financial assistance.
References
Lampert R.
ECG screening in athletes: differing views from two sides of the Atlantic.
Accuracy of the ECG for differential diagnosis between hypertrophic cardiomyopathy and athlete’s heart: comparison between the European Society of Cardiology (2010) and International (2017) criteria.
Costs and yield of a 15-month preparticipation cardiovascular examination with ECG in 1070 young athletes in Switzerland: implications for routine ECG screening.
Task Force “Prevention of Sudden Death in Elite Sport” SGSM/SSMS 2010; the sudden cardiac death of a young athlete: recommendations for a sensible and effective preventive exam.
Schweizerische Zeitschrift für “Sportmedizin und Sporttraumatologie”.2011; 2: 108-109
Pre-participation cardiovascular evaluation for athletic participants to prevent sudden death: position paper from the EHRA and the EACPR, branches of the ESC. Endorsed by APHRS, HRS, and SOLAECE.
The effectiveness of screening history, physical exam, and ECG to detect potentially lethal cardiac disorders in athletes: a systematic review/meta-analysis.
Accuracy of the 2017 international recommendations for clinicians who interpret adolescent athletes’ ECGs: a cohort study of 11 168 British white and black soccer players.
Performance of the American Heart Association (AHA) 14-point evaluation versus electrocardiography for the cardiovascular screening of high school athletes: a prospective study.
Assessment of the 12-lead ECG as a screening test for detection of cardiovascular disease in healthy general populations of young people (12–25 years of age): a scientific statement from the American Heart Association and the American College of Cardiology.
Comparison of cardiovascular screening in college athletes by history and physical examination with and without an electrocardiogram: efficacy and cost.
Recommendations for participation in competitive sports of athletes with arterial hypertension: a position statement from the sports cardiology section of the European Association of Preventive Cardiology (EAPC).
Statistically significant (p < 0.05) between subgroups.
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