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The adolescent athlete's heart; A miniature adult or grown‐up child?

Abstract The systematic development of early age talent in sports academies has led to the professionalization of pediatric sport and the sports physician need to be aware of pediatric cardiological problems. Research into the medical cardiac care and assessment of the pediatric athlete are accumulating, but specific pediatric international guidelines are not available yet and reference data for ECG and echocardiography are incomplete, in particular for the age group <12 years of age. This article is an introduction to the physiological and diagnostics specifics of the pediatric athlete. The focus lies in the differences in presentation and diagnosis between pediatric and adult athletes for the most common pathologies. Reference data for electrical and structural adaptations to intensive exercise are sparse particularly in athletes aged below 12 years old. Training related changes include decrease of resting heart rate, increase of cardiac output, ventricular cavity size, and wall thickness. Cardiac hypertrophy is less pronounced in pediatric athletes, as HR mediated cardiac output increase to endurance exercise is the dominant mechanism in peripubertal children. As in adults, the most pronounced cardiovascular adaptations appear in classical endurance sports like rowing, triathlon, and swimming, but the specifics of pediatric ECG and echocardiographic changes need to be considered.

Although overall cardiorespiratory fitness has been falling in teenagers for many years, this decline has stabilized since 2000 with the greatest improvement in countries with the least income inequality. 1,2 The importance of integration of sports and exercise into the daily lives of children is reflected in the international activity recommendations for children and adolescents, modified from References 3, 4.
At least 60 minutes of moderate to vigorous physical activity daily, >60 minutes provide additional health benefits. Most physical activity should be aerobic.
• Vigorous-intensity activities at least 3 days a week • Activities that strengthen muscle and bone These recommendations reflect the overwhelming evidence of health benefits from regular physical exercise and are intended to counteract the alarming sedentary lifestyle in children worldwide.
Data from the United Kingdom, suggests, that only 14% of 13 to 15 year old boys and 9% of girls achieve physical activity targets-a figure which has fallen from 28% in boys and 14% in girls in 2008. 5 In contrast to the sedentary majority, there is an emerging subpopulation of children and adolescents that train to a very high level. Moreover, there is robust evidence to suggest that in children and adolescents, higher amounts of physical activity are associated with multiple health benefits including cardiorespiratory and muscular fitness, bone health, and weight status or adiposity. 6 Although the term "pediatric athlete" is usually defined as 12 to 16 years old, 7 regular training can begin from the age of 6 years onward for some sports disciplines (eg, gymnastics). Specific strategies for athlete development from a young age may include "professional" level training intensity and volumes. 8 However, in addition to some positive adaptive responses, intensive training can have a detrimental effect on the developing musculoskeletal system leading to overuse injuries, overtraining syndrome and burnout. 9,10 Hence, training the elite pediatric athlete will need to be accompanied by evidenced based medical care for the pediatric athlete.

| Epidemiology of disease and sudden cardiac death
The etiology of sudden cardiac death (SCD) in pediatric athletes is comparable to those in young adult athletes. Available data show for example that 2000 children die each year from SCD in the US, the incidence ranging from 0.6-8/100000. 11,12 A recent study of 11 168 adolescent footballers, who were undergoing cardiac screening, identified disorders associated with SCD in 0.38% and an incidence of SCD in 6.8 per 100 000 athletes during follow up. 13 While available data supports the concept that cardiac screening can pick up cardiac disease in pediatric and adolescent athletes, [14][15][16] the optimal screening strategy is still debated. 17,18 Additionally its efficacy in preventing SCD in this population is still a matter of debate. The causes of SCD in the pediatric athlete population 19,20 include 44% structural heart disease such as congenital cardiac anomalies or cardiomyopathies, nonstructural heart disease, primarily channelopathies, accounting for the remaining 56%. The variable etiology, incidence and age of presentation of common causes of SCD such as cardiomyopathies and inherited arrhythmia disorders needs to be taken into account when assessing the true incidence and etiology of SCD in childhood. 21,22 Alarmingly, sudden cardiac arrest is the first presenting symptom in approximately 50% of cases, providing a strong argument for early detection of disease by preparticipation screening. 23,24 1.3 | Maturation, growth, and adaption of the cardiovascular system in childhood Knowledge of the physiological changes in the pediatric athlete caused by growth, maturation, and training are incomplete but have been increasingly investigated over the last decade. This has informed training and talent development 8 However, it is still difficult to predict adult athletic performance before puberty. 25 Many of the most talented young athletes are simply those with those most advanced pubertal development. Trainability and training effects have been investigated in pediatric athletes, 26 but physiological gender related maturation and development particular during puberty with growth, hormone dependent bone and muscle mass maturation, changes in endurance, speed, strength, balance, age and weight related heart rate, blood pressure and cardiac output, respiratory capacity and peak oxygen uptake need to be taken into account when differentiating training progress from growth and maturation or indeed pathology.
Although some sports specialization is important to develop elite-level skills, it is recommended that intense training in a single sport should be delayed until late adolescence to minimize injury, psychological stress, and burnout. 27 Exercise training effects in childhood include improvements in bone strength, kinetic skills, biological maturity, lung and endocrine function, academic performance and mental health. 28 The complex interaction between growth, training, gender and maturity is also true and must be taken into account when assessing the cardiovascular system of pediatric athletes. During puberty, significant changes occur which affect both cardiac size and function and are reflected in screening tests such as echocardiography and the ECG. Importantly, this is also the time where inherited arrhythmia disorders or cardiomyopathies can present for the first time as growth and hormonal changes unmask genetic cardiac disease. This is seen in electrical diseases such as channelopathies and in structural diseases such as the cardiomyopathies. Thus, 23% of children with a family history of Brugada syndrome and a negative ajmaline challenge in early childhood will have a positive (diagnostic) ajmaline challenge if repeated after puberty. 29 Similarly, in a large multicenter review of young people with catecholaminergic polymorphic ventricular tachycardia (CPVT), the average onset of symptoms was 10.8 years with diagnosis delayed for up to 2.5 years. 30 This is also relevant for cardiomyopathies (eg, hypertrophic cardiomyopathy [HCM]), where a clear prepubertal phenotype is more difficult to recognize than in adult life. 31 For children with a family history of HCM, 1 to 2 yearly screening is recommended from aged 10 years 32 as presentation can occur in childhood. 33 These factors make the assessment of normality of cardiac size and function challenging, and during childhood, cardiac chamber sizes should be referenced to somatic size using z scores or relating cardiac dimensions to height or body surface area. Pubertal stage should also be taken into account, although this is rarely formalized due to the impracticality of assessing pubertal stage in teenagers which requires either an assessment of secondary sexual characteristics or x-ray imaging such as bone age. Size/gender specific pediatric centiles for both echocardiographic measurements and cardiac MRI in the nonathletic pediatric population are available. [34][35][36] Prior and La Gerche defined athlete's heart as "the complex of structural and functional electrical remodeling that accompanies athletic training". 37 Knowledge and data on physiological changes to athletic training in childhood are well documented in adults but less is known in children and in particular the developing pediatric  Table 1. Adaptation in cardiac chamber size and myocardial mass have been described, 41 but are less pronounced in pediatric athletes, which may reflect the different effect of exercise on the immature heart but it may also be due to the reduced intensity and volume of exercise training participated in by younger children. Interestingly, overtraining can occur in pediatric athletes, for example described by elevation in microvolt T wave alternans as a specific sign of overtraining in elite child athletes. 42 When cardiac adaptations to training occur in the pediatric athlete, the phenotype is different to adults, 43 These are summarized in Table 2 and include a more pronounced chamber dilatation and less ventricular hypertrophy than in adults. 44

| 12-lead ECG
The 12-lead ECG is the primary cardiac screening tool in athletes. 49 Moreover, even in the USA where the ECG is less commonly used as an athletic screening tool, many pediatricians will use the ECG selectively for assessment rather than relying on clinical examination and preparticipation questionnaire alone, 54

| Echocardiography
Echocardiography is the first line diagnostic imaging tool also for the pediatric athlete. Pediatric echocardiographic examinations should include a morphological assessment 64 and include a coronary artery assessment. 65 Normative reference values exist for cardiac morphology 66

| Cross sectional imaging
Cross sectional imaging to investigate pediatric athletes for a cardiac pathology should follow adult recommendations, 77 but protocols (higher incidence of undiagnosed congenital heart disease in children) and the relevance of specific diagnostic parameters (different diagnostic criteria for cardiomyopathies) differ. Size and gender specific pediatric centiles are available for cardiac magnetic resonance imaging (CMR) parameters. [34][35][36] CMR has recently been used as a primary screening tool for cardiac anomalies, in particular coronary artery anomalies. 78 Cardiac CT is the imaging modality of choice in the delineation of small anatomical structures such as coronary arteries and collateral arteries and for imaging parenchymal lung pathology.

| Exercise assessment
Exercise testing, in particular cardio-pulmonary exercise testing (CPET) is also a core diagnostic tool in children to investigate metabolic, respiratory, or cardiac pathology 79,80 as it can investigate pulmonary vascular disease, dysfunction of the autonomic nervous system, peripheral defects in oxygen transport, oxygen utilization at the working muscle and indirectly cardiac function. It can be safely performed in children above the age of 8 years. 81 CPET should always be combined with exercise 12-lead ECG testing to allow assessment of underlying exercise-related arrhythmias. It is paramount that supervising personnel should be trained and familiar with the pediatric population to encourage maximal effort and deliver reliable test results. 82,83 Exercise metabolism in pediatric athletes differs from adults in that children do not always attain a true VO 2 max, 84 and submaximal measures such as ventilatory anaerobic threshold 85 or oxygen uptake efficiency slope 86 can be equally good markers for endurance performance. CPET is also -used to indirectly investigate stroke volume response in pediatric patients with ventricular dysfunction, cardiomyopathies or congenital heart disease and is a core part in assessing sports participation eligibility also in the pediatric athlete. Exercise stress echocardiography can aid in detecting early systolic and diastolic dysfunction, assess valve function, myocardial exercise reserve, subtle wall motion abnormalities or dyssynchrony.
Myocardial exercise reserve to investigate borderline or low cardiac function at rest, often seen in athletes can be determined by relatively load independent parameters such myocardial deformation (strain) and Tissue Doppler where, contrary to the adult population, normative reference data exist. 69,70 No studies exist to date using exercise stress CMR to assess cardiac volumes, function and wall motion abnormalities during exercise in athletes as is now performed in adult athletes. 87 Cableless mobile and app based devices to monitor heart rate and rhythm during exercise have been piloted in children and are a credible alternative to laboratory testing. 88

| SPECIFIC DIAGNOSTIC CONSIDERATIONS IN THE PEDIATRIC ATHLETE
The spectrum of hereditary and acquired arrhythmia disorders and cardiomyopathies as a cause of SCD is very similar to that seen in adult athletes, and thus, adult competitive sports participation guidelines should be adhered to in the diagnosis and management of arrhythmias 89 and cardiomyopathies. 90

| Arrhythmogenic ventricular cardiomyopathy
Disease is often concealed in childhood and mimics changes seen in the healthy young athletic population. 94 Diagnostic criteria are less sensitive and specific in pediatric ARVC 95,96 as they are based on data from affected adults 97 Echocardiographic revised task force criteria in particular rarely trigger suspicion in children and adolescents as they rely on adult RV diameters and are less sensitive and specific in pediatric ARVC 98 and enlarged RV diameters in pediatric athletes can mimic cardiomyopathic changes. 73 Recent data suggest that additional modalities such as 2-D strain are more sensitive in assessing adolescents with ARVC. 96 CMR is the diagnostic imaging modality of choice also in children, but CMR findings in adult arrhythmogenic ventricular cardiomyopathy (AVC) such as fatty infiltration and fibrosis are of limited value in children and focus lies on ventricular function, regional wall motion abnormalities, and z-scores of RV and LV dimensions. 95 Arrhythmic activity is highly variable in adolescent patients with AVC, 99  although it used to be thought that intermittent pre-excitation was a good prognostic finding, it is now clear that intermittent preexcitation does not imply a low risk pathway in children. 105 Consequently, most pediatric electrophysiologists would now carry out an invasive electrophysiology study to establish risk and the presence of pre-excitation on the ECG of a child athlete should lead to a referral to a pediatric electrophysiologist for further risk stratification. 106

| Congenital heart disease
Congenital heart disease (CHD) is the most common birth defect with a good survival rate and there are now many more adults than children with congenital heart disease-approximately 1 in 150 young adults have some form of CHD. 107 Recently, exercise advise in children and adolescents has shifted away from a more restrictive approach. It is now recommended that exercise advice and prescription should be an integral component of every patient encounter. 108 The assessment and follow up of the pediatric athlete should be in the hands of experienced congenital cardiologists, the -recommendations on individual exercise and eligibility assessments in -patients with CHD help risk stratify individuals in terms of type, intensity and level of exercise 109 but these relate to athletes over the age of 16 years of age.

| Care of the pediatric athlete in the future
The rapid development and professionalization of youth sports academies demands increased diligence to safeguard the development of the pediatric athlete. The significant progress achieved in adult sports cardiology can guide assessment of the pediatric athlete, but adult F I G U R E 1 Bar chart shows the percentage of false-positive ECG findings according to the 3 ECG interpretation criteria by chronological age. *P < .05, significantly reduced prevalence to ESC 2010 recommendations. #P < .05, significantly reduced prevalence to Seattle Criteria, reproduced with permission from Reference 61 cardiac preparticipation screening and management recommendations cannot be unequivocally applied to the pediatric heart. Somatic growth, psycho-cognitive maturation with particular communicational and also ethical and legal considerations require an interdisciplinary approach involving pediatricians, pediatric cardiologists and sports medicine professionals as well as coaching staff with the young athlete in the center.
Future research should focus on the development of gender, growth, and age specific normative assessment criteria for ECG and echocardiogram to increase diagnostic accuracy. Most importantly, development of training pathways and a stronger engagement of pediatric and sports governing bodies is required, as too few pediatricians and pediatric cardiologists are sufficiently trained to provide expert opinion on the pediatric athlete. 110 Consequently, an approach requiring synergy between pediatric and sports cardiologists, exercise physiologists, policy makers, and sports organizations is required to develop pediatric cardiac monitoring tools and protocols, eventually working towards a child athlete centered specialty (pediatric sports cardiology) that matches the sports professionalism of the current and future pediatric athlete.

CONFLICT OF INTEREST
Dr. Guido E. Pieles is director of the sports cardiology consulting company "Cardiac Health and Performance Ltd", Prof. A Graham Stuart is Medical Director of "Sports Cardiology UK"-a company which specializes in the assessment and management of athletes with cardiovascular problems.

ETHICS STATEMENT
This article does not contain any studies with human participants or animals performed by any of the authors.