Athlete’s Heart: A Multimodal Approach – From Physiological to Pathological Cardiac Adaptations 0323952216, 9780323952217

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ATHLETE’S HEART

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ATHLETE’S HEART A Multimodal Approach From Physiological to Pathological Cardiac Adaptations Edited by

ANTONELLO D’ANDREA Unit of Cardiology and Intensive Coronary Care, “Umberto I” Hospital, Nocera Inferiore, Italy Division of Cardiology, Department of Translational Medical Sciences, University of Campania “Luigi Vanvitelli”, Monaldi Hospital, Naples, Italy

EDUARDO BOSSONE Public Health Department, University of Naples “Federico II”, Naples, Italy

Academic Press is an imprint of Elsevier 125 London Wall, London EC2Y 5AS, United Kingdom 525 B Street, Suite 1650, San Diego, CA 92101, United States 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, United Kingdom Copyright © 2023 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. ISBN 978-0-323-95221-7 For information on all Academic Press publications visit our website at https://www.elsevier.com/books-and-journals

Publisher: Stacy Masucci Acquisitions Editor: Tracey Lange Editorial Project Manager: Matthew Mapes Production Project Manager: Omer Mukthar Moosa Cover Designer: Miles Hitchen Typeset by STRAIVE, India

Dedication In memory of my father LUIGI, who ignited in me the flame of passion for cardiovascular adaptations to physical exercise Antonello D’Andrea

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Contents Contributors xi

1. What is athlete’s heart?

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Antonello D’Andrea, Andreina Carbone, and Eduardo Bossone

1 Introduction 1 2 Athlete’s heart: Should we need a more specific definition? 1 3 SCD in athletes: The entity of the problem 2 4 Preparticipation cardiovascular screening in athletes 3 5 The role of electrocardiography in the preparticipation 5 6 Indications for further cardiovascular tests 7 7 Cardiovascular screening in older athletes 10 8 Conclusions 11 References 11

2. Physiological and pathological cardiac adaptations to physical exercise

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Antonello D’Andrea, Francesco Gambardella, and Eugenio Picano

1 Introduction 15 2 Physiological modification of the heart with physical exercise 15 3 Physiological modifications in different sports 20 4 Special environment 31 5 Doping and cardiovascular effects 38 6 Conclusions 44 References 45

3. Electrocardiogram in athletes

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Berardo Sarubbi, Giovanni Papaccioli, Giovanni Domenico Ciriello, Vincenzo Russo, Anna Correra, and Aaron Baggish

1 Introduction 51 2 Common and training-related ECG changes in athletes 52 3 Normal ECG changes related to demographics: Age, sex, and ethnicity 56 4 Uncommon and training-unrelated ECG changes in athletes 57 5 Nonspecific ECG findings in athletes 68 6 Supraventricular or ventricular arrhythmias on ambulatory rhythm monitoring 69

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7 Overlap ECG pattern between athlete’s heart and pathologies 71 8 Conclusions 71 References 72

4. Echocardiogram in athlete’s heart

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Antonello D’Andrea, Stefano Palermi, Marc Dweck, Andre La Gerche, and Matteo Cameli

1 Introduction 77 2 Left heart 81 3 Right heart 84 4 Vessels 86 5 New echocardiographic techniques 88 6 Conclusion 93 References 94

5. Multimodality imaging in athlete’s heart

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Antonello D’Andrea, Simona Sperlongano, and Flavio D’Ascenzi

1 Introduction 103 2 Exercise stress testing 103 3 Exercise stress echocardiography 106 4 Cardiac magnetic resonance 108 5 Coronary computed tomography 112 6 Cardiac nuclear imaging 114 7 Conclusion 115 References 115

6. Gray zones in athlete’s heart

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Antonello D’Andrea, Eduardo Bossone, Alessandro Serio, and Gianluca Pontone

1 Introduction 121 2 Left ventricular hypertrophy or hypertrophic cardiomyopathy? 122 3 Athlete’s heart or dilated cardiomyopathy? 129 4 Left ventricular noncompaction cardiomyopathy or adaptive hypertrabeculation? 131 5 Right ventricular physiological dilation or arrhythmogenic right ventricular cardiomyopathy? 134 6 Conclusions 137 References 140



Contents

7. Genetic testing in athletes

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Emanuele Monda, Michael Papadakis, Silvia Castelletti, and Giuseppe Limongelli

1 Introduction 147 2 Genetic testing in athletes 148 3 Inherited cardiac disorders in athletes 149 4 Conclusion 165 References 165 Index175

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Contributors Aaron Baggish Division of Cardiology, Massachusetts General Hospital, Boston, MA, United States Eduardo Bossone Public Health Department, University of Naples “Federico II”, Naples, Italy Matteo Cameli Department of Medical Biotechnologies, Division of Cardiology, University of Siena, Siena, Italy Andreina Carbone Division of Cardiology, Department of Translational Medical Sciences, University of Campania “Luigi Vanvitelli”, Monaldi Hospital, Naples, Italy Silvia Castelletti Sports Cardiology Unit, Cardiology Department, Istituto Auxologico Italiano IRCCS, Milan, Italy Giovanni Domenico Ciriello Adult Congenital Heart Disease Unit, Monaldi Hospital, Naples, Italy Anna Correra Adult Congenital Heart Disease Unit, Monaldi Hospital, Naples, Italy Antonello D’Andrea Unit of Cardiology and Intensive Coronary Care, “Umberto I” Hospital, Nocera Inferiore; Division of Cardiology, Department of Translational Medical Sciences, University of Campania “Luigi Vanvitelli”, Monaldi Hospital, Naples, Italy Flavio D’Ascenzi Department of Medical Biotechnologies, Division of Cardiology, University of Siena, Siena, Italy Marc Dweck British Heart Foundation Centre for Cardiovascular Science, University of Edinburgh, Edinburgh, United Kingdom Francesco Gambardella Public Health Deparment, University of Naples Federico II, Naples, Italy Andre La Gerche Cardiology Department, St Vincent's Hospital Melbourne, Fitzroy,Victoria, Australia Giuseppe Limongelli Inherited and Rare Cardiovascular Disease Unit, Department of Translational Medical Sciences, University of Campania “Luigi Vanvitelli”, Naples, Italy Emanuele Monda Inherited and Rare Cardiovascular Disease Unit, Department of Translational Medical Sciences, University of Campania “Luigi Vanvitelli”, Naples, Italy xi

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Stefano Palermi Public Health Department, University of Naples “Federico II”, Naples, Italy Giovanni Papaccioli Adult Congenital Heart Disease Unit, Monaldi Hospital, Naples, Italy Michael Papadakis Cardiology Clinical and Academic Group, St George’s, University of London, and St George’s University Hospitals NHS Foundation Trust, London, United Kingdom Eugenio Picano Institute of Clinical Physiology, Italian National Research Council, Pisa, Italy Gianluca Pontone Cardiovascular Imaging Department, Centro Cardiologico Monzino IRCCS, Milan, Italy Vincenzo Russo Department of Translational Medical Sciences, University of Campania “Luigi Vanvitelli”, Naples, Italy Berardo Sarubbi Adult Congenital Heart Disease Unit, Monaldi Hospital, Naples, Italy Alessandro Serio Public Health Department, University of Naples “Federico II”, Naples, Italy Simona Sperlongano Division of Cardiology, Department of Translational Medical Sciences, University of Campania “Luigi Vanvitelli”, Monaldi Hospital, Naples, Italy

CHAPTER 1

What is athlete’s heart? Antonello D’Andreaa,b, Andreina Carboneb, and Eduardo Bossonec a Unit of Cardiology and Intensive Coronary Care, “Umberto I” Hospital, Nocera Inferiore, Italy Division of Cardiology, Department of Translational Medical Sciences, University of Campania “Luigi Vanvitelli”, Monaldi Hospital, Naples, Italy c Public Health Department, University of Naples “Federico II”, Naples, Italy b

1 Introduction Vigorous exercise training determines profound effects on cardiac structure and function, often referred to as the athlete’s heart, characterized by increased left ventricular mass (LVM), cavity dimensions, and wall thickness with normal systolic and diastolic function [1].The actual evidence suggests that there may be some overlap between physiological and pathological conditions, some of which are related to sudden cardiac death (SCD). During dynamic exercise, the rise in pressure and volume determines an increase in the wall stress of both ventricles and in the atria [2–4]. Furthermore, ventricular afterload increases with exercise intensity in a near-linear manner, increasing progressively with exercise load [3–5].The duration of physical efforts represents the second major determinant of the entity of cardiac remodeling [4]. For this reason, endurance athletes have greater cardiac remodeling than athletes from team or sprint sports [4,6]. The differences in cardiac remodeling may be attributed to both hemodynamic conditions created from a variety of static and dynamic exercise components and the time of exposure to exercise load [4]. A diagnostic gray zone between physiological remodeling and cardiac alterations exists at the extremes of athletic cardiac remodeling, and questions arise as to whether the observed increase in cardiac dimensions is proportional to the amount of exercise conditioning [1]. The differentiation between physiological and pathological changes in athletes is mandatory because an incorrect diagnosis has important consequences, such as exclusion from competitive sports, false reassurance, and missed opportunities for effective therapeutic intervention.

2  Athlete’s heart: Should we need a more specific definition? Athlete’s heart is defined as a benign increase in cardiac mass, with specific circulatory and cardiac morphological alterations, that represents a physiological adaptation to systematic training [7]. A more consistent definition of Athlete’s Heart https://doi.org/10.1016/B978-0-323-95221-7.00007-0

Copyright © 2023 Elsevier Inc. All rights reserved.

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athlete is essential for understanding the heterogeneity regarding the degree of cardiac changes as a result of exercise training and to better differentiate physiological and pathological remodeling [4]. If the cardiac remodeling is consistent with the level of training, further examinations may not be required. However, it can be extremely difficult to estimate the degree of expected remodeling given the broad ranges published in the literature [4]. The Michell criteria have been used to explain cardiac remodeling in athletes categorizing sports according to the relative amount of static and dynamic exercise [4,6]. Beaudry et al. proposed a simple model of the athlete’s heart, defined by two variables of exercise intensity and duration [4]. Briefly, the entity of myocardial adaptation is proportional to the hemodynamic stress (amount of intensity) and the time in which this stress is applied (duration and frequency of training). However, this is a simplified model of a more complex system in which also genetic factors and environmental issues play an important role. For example, cardiac remodeling is probably less marked in women than in men [8], and electrical and structural adaptations appear to be more evident in black compared with white athletes [9–11]. Furthermore, other genetic features, such as the age and cumulative years of exercise exposure, may have a role in the entity of cardiac remodeling [4].

3  SCD in athletes: The entity of the problem SCD associated with sports is a rare but catastrophic event. Strenuous exercise training may be a trigger of ventricular tachyarrhythmias, usually ventricular fibrillation (VF) or ventricular tachycardia degenerating in VF, in predisposed individuals [12]. SCD associated with sport is defined as sudden and unexpected death occurring during, or shortly after exercise training in an apparently healthy individual [13].The real incidence of SCD in athletes is uncertain [13]. As a general estimate, 1 to 2 of 100,000 athletes between the age of 12 and 35 years experienced SCD each year [12,14–17]. The most reliable data are those resulting from Italian studies [12,18,19], retrospective US cohort studies [17], a prospective observational study in high school [20], and studies in active US military recruits [21]. Italian data show a three times higher incidence of SCDs in athletes than in nonathletes [12]. However, in a Danish study, the incidence of SCD is similar in competitive and recreational sports [22]. The incidence is 2–25 times higher in men than in females and increases with age, being 5–10 times higher in athletes over 35 years old [12,14,16,17,20,23]. Sport-related SCD is more frequent in black athletes (5.5/100,000) and male basketball players (10/100,000)



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Table 1  Causes of SCD in athletes. Structurally heart anomalies

Structurally normal heart

HCM ARVC Coronary artery anomalies LFVN

Long QT syndrome Short QT syndrome Brugada Catecholaminergic polymorphic ventricular tachycardia Other channelopathies WPW syndrome Commotio cordis

DCM Myocarditis Marfan syndrome (aortic rupture) Valvular heart disease Coronary artery disease (>35 years old)

HCM, hypertrophic cardiomyopathy; DCM, dilated cardiomyopathy; LVNC, left ventricle noncompaction; ARVC, arrhythmogenic right ventricle cardiomyopathy; WPW, Wolff-Parkinson-White.

[14,23]. There is a great interest in the early identification of at-risk athletes to minimize the risk of SCD, and the preparticipation evaluation (PPE) is a reasonable strategy to identify subjects at risk, although debated and controversial.

3.1  Cardiac conditions associated with SCD SCD in young athletes is usually caused by genetic or congenital structural cardiac disorders [12,22,24–27]. In young athletes (35 years of age, more than 80% of all SCD is due to atherosclerotic coronary artery disease, and vigorous physical activity is associated with an increased risk of the acute coronary syndrome and SCD [24]. The most common causes of SCD are summarized in Table 1. These conditions are variable depending on the age and geographical factors of the studied population [13].

4  Preparticipation cardiovascular screening in athletes Preparticipation cardiovascular screening aimed at the identification of anomalies associated with SCD and is supported by major international medical societies [13,24,29–31]. However, the best strategies remain controversial. The inclusion of the 12‑lead ECG in the initial screening is a

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source of debate. In particular, the American Heart Association (AHA) recommends taking accurate medical and familial history and physical examination, whereas the European Society of Cardiology (ESC) recommends routine execution of a 12‑lead ECG [7]. Further evaluations (exercise ECG, cardiovascular imaging tests, etc.) are recommended in symptomatic and/or high cardiovascular risk patients [24]. In Italy since 1982, athletes had to undergo a clinical evaluation to obtain eligibility for competitive sports. The recommendations of “Comitato Organizzativo Cardiologico per l’Idoneità allo Sport” (COCIS) organization represent the pillar of the screening program in Italian athletes [32].

4.1  Clinical and familial history A comprehensive clinical history is critical to identify athletes with underlying medical conditions that may interfere with participation in sports. Particular attention should be given to the personal and family cardiac histories [7,13]. Ideally, a parent should be present at the preparticipation clinical evaluation to provide historical details for athletes younger than 18 years [7]. The first element to be taken into consideration is the entity of the sport (type of sport, intensity, duration of training, and competitions), to correlate it with subsequent clinical, electrocardiographic, and echocardiographic findings [32]. The family history should be evaluated, in particular the presence of heart disease in the first-degree relatives, including sudden unexplained deaths or sudden deaths before age 50 related to heart problems, heart disease in childhood, drowning/predrowning or accidents unexplained, which may indicate the presence of genetic cardiovascular disorders [32]. In the personal medical history, in addition to any previous pathological conditions, the evaluation of the presence of risk factors for coronary artery disease (especially in master athletes who are at higher risk of atherosclerotic coronary heart disease) and the use of cardiotoxic substances such as alcohol and drugs (especially cocaine) are recommended [32]. Warning signs and symptoms (chest pain from exertion, syncope or presyncope, palpitations, excessive dyspnea or fatigue disproportionate to the level of exercise, unexplained seizures) reported by the athlete should lead to further diagnostic investigations [7,32]. The AHA proposed a 14-points screening questionnaire as part of a comprehensive history-taking and physical examination to detect or raise suspicion of genetic/congenital cardiovascular abnormalities [7] (Table 2). Furthermore, the Italian COCIS 2017 proposed a structured checklist for anamnesis [32].



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4.2  Cardiovascular physical examination The cardiovascular evaluation should be performed in a quiet room to facilitate auscultation. A brief visual inspection of the precordium to evaluate for asymmetry and abnormal impulses is recommended. Precordial palpation can detect thrills, abnormal apical impulse location, and parasternal heave.The physician then should carefully auscultate to identify the first and second heart sounds, extra heart sounds, and murmurs. A “fixed split” of a second heart sound can be a sign of an atrial septal defect, and a “paradoxical split” (i.e., narrowing on inspiration) can be a sign of severe aortic stenosis, hypertrophic cardiomyopathy, or left bundle branch block [33]. Murmurs should be characterized based on timing, location, character, and intensity. Dynamic auscultation (e.g., squat-to-stand and Valsalva maneuvres) can further clarify the murmur type. Squatting increases venous return to the heart, thereby increasing left ventricular blood volume, chamber size, and stroke volume [32]. In contrast, standing and the Valsalva maneuvre decrease venous return, thereby decreasing left ventricular size and stroke volume. Increased stroke volume causes murmurs to become louder with squatting and quieter with standing or the Valsalva maneuvre. However, if a murmur is softer when the patient squats or is louder or longer when he or she returns to a standing position or during the Valsalva maneuvre, hypertrophic cardiomyopathy or mitral valve prolapse should be suspected [33]. Also, physical examination should focus on [32,33]: • Femoral and radial pulses: a discrepancy between radial (normal) pulses and femoral (reduced) suggests aortic coarctation, especially if an intrascapular murmur is associated; • Any physical signs of Marfan syndrome such as pectus excavatum or carinatum, thoracolumbar scoliosis, disproportionately long arms, legs and fingers, an abnormal extension of the thumb, tall and slender build, a high, arched palate and crowded teeth, heart murmurs, extreme nearsightedness, an abnormally curved spine, flat feet. • Blood pressure of the brachial artery preferably in both limbs.

5  The role of electrocardiography in the preparticipation The ECG evaluation in addition to a standard cardiac history and physical examination has sparked debates on the most appropriate sports eligibility protocol. The medical history (personal and familial) and the cardiac examination have limited accuracy to identify cardiac silent conditions

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Table 2  Fourteen-points questionnaire for preparticipation cardiovascular screening of competitive athletes, according to American Heart Association. Medical history

Personal historya 1. Chest pain/discomfort/tightness/pressure related to exertion 2. Unexplained syncope/near-syncopeb 3. Excessive and unexplained dyspnea/fatigue or palpitations, associated with exercise 4. Prior recognition of a heart murmur 5. Elevated systemic blood pressure 6. Prior restriction from participation in sports 7. Prior testing for the heart, ordered by a physician Family history 8. Premature death (sudden and unexpected, or otherwise) before 50 years of age attributable to heart disease in ≥1 relative 9. Disability from heart disease in close relative