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Authors

G. Mascia1, 4, L. Di Biase2, 5, 7, 8, G. Galanti3, A. Natale2, 6, 7, 9, 10, 11, L. Padeletti1, 4

Affiliations

Affiliation addresses are listed at the end of the article

Key words ▶ athletes ● ▶ arrhythmias ● ▶ sudden cardiac death ● ▶ defibrillators ●

Abstract

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Although athletic participation lowers cardiovascular risk and improves quality of life, it may represent a hazard in high-risk group athletes such as those with cardiac abnormalities receiving an implantable cardioverter defibrillator (ICD). ICD sports participants are exposed to the potential risk of inappropriate shocks due to sinus tachycardia and other supraventricular arrhythmias during exertion as well as device

Introduction

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accepted after revision October 24, 2013 Bibliography DOI http://dx.doi.org/ 10.1055/s-0033-1361185 Published online: April 15, 2014 Int J Sports Med 2014; 35: 800–806 © Georg Thieme Verlag KG Stuttgart · New York ISSN 0172-4622 Correspondence Dr. Giuseppe Mascia Department of Medical and Surgical Critical Care University of Florence Viale Morgagni 85 50134 Florence Italy Tel.: + 39/333/7513 936 Fax: + 39/055/4378 638 [email protected]

Since ICD was first used in humans [55] major developments have been observed and, according to several multicentre trials, indications for ICD implantation in secondary or primary prevention of sudden cardiac death (SCD) now range from ischemic heart failure to various types of cardiomyopathies and cardiac ion channelopathies [10, 12, 16, 17, 21, 38, 57, 59, 73]. Secondary prevention of SCD refers to ICD implantation in patients who have survived a sustained ventricular tachycardia (VT) or a prior cardiac arrest [21]. In this patient population, robust data from trials demonstrate that ICD is associated with clinically and statistically significant reduction in sudden death and total mortality compared to antiarrhythmic drug therapy [12, 13, 22, 38, 73]. On the other hand primary prevention of SCD refers to use of ICD in patients who are at risk for but have not yet had an episode of sustained VT or prior cardiac arrest [21]. Clinical trials demonstrate improved survival in some subsets of patient with coronary artery disease [4, 10, 57, 59, 60] or idiopathic dilated cardiomyopathy [4, 8, 20, 32, 84]. In patients with hypertrophic cardiomyopathy, arrhythmogenic right ventricular dysplasia (ARVD) and long-QT syndrome (LQTS), registry data are less robust but still useful for risk stratification and recommen-

Mascia G et al. Implantable Cardioverter Defibrillator in … Int J Sports Med 2014; 35: 800–806

injury. The safety of athletic participation of ICD-patients is not completely defined and ICD efficacy in interrupting malignant arrhythmias during intense exercise is partly unknown. This explains difficulties in current recommendations made by physicians, given the associated potentially ischemic, autonomic and metabolic conditions. The scope of this review is to underline specific considerations including potential risks and recommendations for athletic participation in this patient-group.

dations for ICD implantation [17, 31, 49, 51, 56, 83]. In conditions such as catecholaminergic polymorphic VT, Brugada syndrome and noncompaction of the left ventricle, registry data provide less rigorous evidence in support of recommendations, while ICD implantation constitutes the best available evidence for these conditions [11, 64, 84]. In most athletes treated with an ICD, an underlying structural cardiovascular disease or a channelopathy is present [29].

Sustained Exertion and Risk of Sudden Cardiac Death

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Although regular physical activity has been demonstrated to improve quality of life [27] and to lower cardiovascular risk [7, 35], exertion places a strain on the heart and in the presence of cardiovascular abnormalities athletic activity could be a trigger for ventricular arrhythmias [14]. Adrenaline surge could be an important factor in arrhythmia generation, although other factors may decrease the arrhythmia threshold including electrolyte imbalance and dehydration [44]. In young athletes, cardiomyopathies have been considered as very important causes of sportsrelated cardiac arrest with ARVD accounting for approximately one fourth of fatal cases in Italy [15, 18] and hypertrophic cardiomyopathy for

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Implantable Cardioverter Defibrillator in Sport Participation

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Table 1 Potential risks of athletic activity with the presence of ICD. Potential risks of sport participation

Hypothesized responsible factors

in ICD-patients Sympathetically driven heart rates, potentially triggered by emotion or stress of sports, could exceed the ventricular tachycardia detection rate determining inappropriate shock. Rates into the ventricular tachycardia detection zone due to episodes of atrial fibrillation or supraventricular arrhythmias during athletic activity could trigger inappropriate shocks. Aggressive contact sport either directly because of trauma or indirectly because of the stretching of leads could cause ICD damage, thereby delivering inappropriate shocks through electromechanical noise. During athletic activity, a physiologic release of catecholamines during exertion could create an arrhythmogenic state more susceptible to development of arrhythmias and less favorable for defibrillation. At time of ICD shock occurring during athletic activity every athlete has an increased risk for body injury.

more than one third of deaths in U.S. [46, 47]. Different genetic substrates may likely explain the difference of incidence in the 2 countries. Specifically, Corrado et al. assessed the risk of sudden death and the underlying pathologic substrates in athletic and non-athletic young populations, and found that the estimated relative risk of total sudden death among athletes compared to non-athletes was 2.5 [14]. This higher risk in the athletic population was strongly related to underlying cardiovascular diseases such as ARVD, congenital coronary artery anomaly and premature coronary artery disease [14]. Investigating sudden deaths occurring in trained U.S. athletes, Maron et al. demonstrated 15 % non-cardiovascular causes at autopsy and found hypertrophic cardiomyopathy and malformations involving anomalous coronary artery origin as the most common structural cardiac diseases identified as the primary cause of death [50]. However, this study was biased by attributing the cause of death by standard autopsy study, and because causes which are not structural as channelopathies were generally not diagnosed [50]. Exertion is also considered an important trigger for events in patients with LQT-1 and catecholaminergic polymorphic VT [45, 63]. In patients with Brugada syndrome where malignant arrhythmias are vagally dependent typically occurring at rest or during sleep, an increased vagal rebound after exertion could indicate a higher risk of those arrhythmias immediately after sport practice [54]. However, despite causes of SCD in athletes ranging from ischemic and non-ischemic cardiomyopathies to channelopathies there is still confusion surrounding the aetiology of SCD in some athletic populations, such as endurance athletes. In this population, cases may also result from a new understanding that sustained exertion could cause a distinct form of cardiomyopathy [76]. Trivax et al. proposed that in marathon runners focal patchy areas of fibrosis, seen on late gadolinium enhancement using cardiac magnetic resonance imaging and at autopsy, could be the substrate for re-entrant ventricular malignant tachycardia increasing risk of SCD [75]. In endurance athletes, the heart undergoes increased pressure and volume overload, and responds through ventricular hypertrophy, cardiac chamber dilatation and an increase in substrate for both atrial and ventricular arrhythmias [30, 33, 75]. Thus in predisposed athletes sustained elevations of cardiac output may determine recurrent dilation of cardiac chambers [37], stimulating resident fibroblasts and macrophages and resulting in deposition of collagen with patchy areas of fibrosis that could become the substrate for re-entrant malignant arrhythmias [75]. In a cohort of highly trained athletes, La Gerche et al. suggested that myocardial dysfunction following intense athletic activity may predominantly affect the right ventricle increasing with race duration and correlating with increases in biomarkers of cardiac

injury [40]. Moreover in athletes with a longer history of endurance sports involvement, increased right ventricular remodelling and focal gadolinium enhancement were more prevalent, leading to extensive right ventricular changes and myocardial fibrosis [40]. In animal model, Benito et al. also documented cardiac fibrosis following long-term strenuous exercise, demonstrating an increased expression of transforming growth factor-β1 that stimulates collagen-producing fibroblasts, thereby increasing the risk of malignant arrhythmias [5].

Safety of Sports Participation in ICD-athletes

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Sports participation in athletes with ICD implantation may have profound implications [23, 53], and postulated risks are ▶ Table 1. Regarding, Lampert et al. surveyed 614 described in ● physician members of the Heart Rhythm Society concerning the safety of sport participation in ICD-athletes [42]. Results were truly surprising with only 10 % respondents recommending avoidance of sports more vigorous than bowling or golf, but most (76 %) recommending avoidance of contact sports, considering these to be high-risk activities. Despite the fact that shocks were common and cited by 40 % of physicians, adverse events were rare ( < 1 % of physicians reported failure of shocks to convert life-threatening arrhythmias, 1 % reported known injury to patient). In this survey running, skiing and basketball were the most common sports associated with shock-therapy. The authors, however, did not assess whether reported shocks were inappropriate [42]. In fact, sinus tachycardia during exertion or supraventricular tachycardia (SVT) that could be present during athletic participation may hinder an appropriate differentiation from malignant arrhythmias, increasing the risk of inappropriate therapies [2]. One of the most frequent risks to athletes is also damage to ICD system during participation in contact sports, making it no surprise that most physicians usually recommend against these sports (basketball, football, rugby, soccer, hockey and wrestling are those most commonly cited) [42]. Moreover, not only contact sport participation but also repetitive arm motion during athletic involvement could cause damage to the ICD system. In the survey by Lampert et al. some cases attributed to golf, weight-lifting or other repetitive motion activities were reported [42]. Damage to the subcutaneously implanted device or its connection with the lead-system either directly due to abrupt trauma or indirectly as result of leads stretching could cause oversensing to non-physiological potentials, resulting in inappropriate detection of ventricular arrhythmias and shocks. Such damage could also result in a failure to deliver enough energy to terminate a malignant arrhythmia

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Inappropriate shocks during sinus tachycardia Inappropriate shocks during supraventricular arrhythmias Inappropriate shocks due to ICD damage Potential failure of a shock to convert a malignant arrhythmia Loss of body control during shock therapy

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Table 2 Strategies for reducing inappropriate or unnecessary ICD-shocks. Parameter

Use

Reducing inappropriate or unnecessary shocks

Detection rate interval Duration criterion Sudden onset Stability criterion Morphology discrimination

Programming rate interval for VT discrimination Differentiates non-sustained from sustained VT Differentiates sinus tachycardia from VT Differentiates atrial fibrillation from VT Compares EGM-morphology in sinus rhythm to EGMmorphology during tachycardia Differentiates lead noise from VT Reduces inappropriate detections of VT/VF in spontaneous T-wave oversensing episodes Refers to the use of pacing stimulation techniques for termination of tachyarrhythmias

Both inappropriate and unnecessary shocks Both inappropriate and unnecessary shocks Inappropriate shocks Inappropriate shocks Inappropriate shocks

Anti-tachycardia pacing

[28]. Moreover, physiological changes associated with physical activity as increase of catecholamines, electrolyte imbalances, tissue acidosis or volume depletion may also contribute to potential failure of a shock to convert a malignant arrhythmia [44, 67, 77]. Finally, loss of bodily control at time of ICD-therapy may increase the risk for bodily injury and poses a potential added level of risk to athletes with ICD implantation [52, 61].

Preventing inappropriate and unnecessary shocks and ICD-programming in athletes The active lifestyle of ICD-athletes and postulated risks during sport participation such as inappropriate shocks during sinus tachycardia and SVT or due to ICD-damage delivering inappropriate shocks through electromechanical noise may require particular attention in device programming. In recent years, several ▶ Table 2) have been proposed for methods and algorithms (● achieving a better discrimination and avoiding inappropriate or unnecessary therapies [36, 78]. Historically, a strong argument for implantation of a dual-chamber ICD (DDD-ICD) and against implantation of single-chamber ICD (VVI-ICD) has been that additional atrial lead could add more valuable information for discrimination. However, multiple studies have not conclusively demonstrated the superiority of DDD over VVI-ICD [1, 3, 19, 24, 39, 74], and to date we do not have any recommendation as to which device would be best suited in athletes. The following programming strategies for reducing inappropriate ICD-shocks are currently being considered: 1) detection rate interval, and 2) duration criterion representing the number of intervals needed to satisfy the rate criterion. ICD uses both rate and duration as 2 basic characteristics of arrhythmia to trigger device therapy [36]. Normally the longer a malignant arrhythmia lasts, the more likely a patient may have symptoms including dizziness or syncope prior to ICD therapy. Moreover, when higher rates are used to trigger ICD therapies, a VT below the detection rate may lead to symptoms and hemodynamic compromise, possibly rendering ICD-therapy ineffective. 3 trials thoroughly examined these issues [25, 58, 82]. The PREPARE study in ICD-primary prevention patients, which programmed a detection time about twice as long as the default-programming and a relatively higher detection rate, demonstrated fewer shocks and did not report an increase in the incidence of death or syncope [82]. In the MADIT-RIT trial prolonging the detection rate of arrhythmia, or setting a high cut-off rate resulted in significant lowering of ICD inappropriate therapies [58]. Both strategies were associated with an insignificantly increased risk of syncope, and in a secondary analysis with a statistically significant reduction in overall mortality [58]. In the ADVANCE III

Inappropriate shocks Inappropriate shocks Unnecessary shocks

study, increasing the number of detection intervals using 30 of 40 intervals to detect ventricular arrhythmias vs. standard detection with 18 of 24 intervals reduced rates of antitachycardia pacing (ATP), shocks and inappropriate shocks in patients undergoing first ICD-implantation [25]. However, in this trial, the follow-up was too short to assess whether longer detection intervals and subsequently lower rates of ventricular therapies delivered and inappropriate shocks translated to a mortality benefit [25]. Algorithms in reducing inappropriate shocks are also considered: 3) discrimination algorithms such as sudden onset that distinguishes sinus tachycardia from VT, stability criterion that distinguishes atrial fibrillation from VT, or morphology discrimination comparing EGM-morphology in sinus rhythm to EGM-morphology during tachycardia [36]. However, neither assumption in something actually infallible nor the performance of both sudden onset or stability criterion could be limited to rates < 180–190 beats/min in single-chamber devices [9], while morphology discrimination could fail to recognize fast-SVTs due to frequency-related conduction abnormalities [34]. 4) lead noise algorithms, including alerts based on both high lead impedance and oversensing [71]. A different algorithm differentiates lead noise from VT analyzing the far-field electrogram signal in an amplitude measurement window centered around events on near-field electrogram. Oversensing due to connection or lead problem could be identified when the peak to peak amplitudes on the far-field electrogram show great disparity [26, 36, 78]. 5) T-wave oversensing algorithms, programming decay in sensitivity after a sensed QRS [68]. The latest generation of T-wave oversensing algorithm differentiates R waves from T waves by analyzing the sensing electrogram with differences in amplitude, frequency content and pattern to distinguish R and T waves from VT [78]. In sports practice it could be important to reduce not only inappropriate but also unnecessary shocks including those delivered for ventricular arrhythmias that would have spontaneously finished, or would have terminated with ATP [36]. Tachycardia detection rate cutoffs and longer detection time could be both important strategies for reducing unnecessary therapies [78]. Many trials also exhibited benefits using ATP and reported an important reduction in delivered shocks [79– 82]. However, delivering ATP after a short duration of VT could overestimate its efficacy because some short episodes may also terminate spontaneously [72, 80]. On the other hand, ATP therapy may entail the potential risk of VT acceleration [66]. Despite ATP reducing unnecessary shocks it could accordingly be very difficult to assess the real efficacy of this painless therapy particularly in active patients involved in sports.

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Lead noise algorithms T-wave oversensing algorithms

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ICD efficacy during exercise is not fully known. It has been shown that arrhythmias could be harder to terminate during high catecholamine states, and some authors have studied the effect of sympathetic activation on the efficacy of ICD in converting ventricular arrhythmias [67, 77]. In ICD-patients undergoing device testing before and after infusion of epinephrine, Sousa et al. demonstrated that rise in plasma catecholamine concentration could increase the number and magnitude of shocks needed to terminate ventricular arrhythmias [67]. Moreover, given that both epinephrine and norepinephrine plasma levels peak during the morning hours [69], Venditti et al. suggested a circadian variation in required defibrillation energy, demonstrating a peak in the measured defibrillation threshold and a decreased first shock efficacy in the morning [77]. However, although in theory these studies may suggest, among the athletic population, a potential risk of shock failure to convert a malignant arrhythmia due to catecholamines that could create an arrhythmogenic state, which is more susceptible to development of arrhythmias and less favorable to defibrillation [67, 77], there are still conflicting findings [70], and in practice it remains unknown whether there is potential diminishing success. Moreover, other physiological changes associated with physical activity such as electrolyte imbalances, tissue acidosis or volume depletion may all be possible factors that contribute to a decreased success [44].

Recent Data from the “ICD-sport Registry”

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In view of the information presented above, further data are needed to better define the safety of sports for patients with ICD. For this reason a prospective ICD-sport registry has been developed [43]. The goal of this registry was to follow athletes prospectively to quantify risks of sport practice. This registry enrolled patients from 10 to 60 years old participating in organized sports (n = 328) involving regular practice and scheduled competition in sports with both dynamic and static components greater than those classified traditionally as IA (golf, billiards or bowling), or patients participating in high-risk sports (n = 44), which are defined as those in which a loss of control may result in injury. LQTS, hypertrophic cardiomyopathy and ARVD were the most common diagnoses [43]. Results showed no occurrence of the primary endpoints, which are defined as adverse events occurring within 2 h following athletic activity such as arrhythmic death or externally resuscitated arrhythmia caused by shock failure, injury due to arrhythmic symptoms and/or shock [43]. Overall 13 % of study population received at least one appropriate shock, and 11 % at least one inappropriate. There was no difference between the portion of athletes receiving an ICD shock during practice/competition (10 % of study population) and those during other physical activity (8 %), while 6 % experienced shocks at rest. Moreover, the proportion of athletes receiving appropriate shocks during practice/competition or any other physical activity (8 %) was greater than during rest (3 %) [43]. However, although more appropriate and inappropriate shock therapies occurred during exertion with no difference between practice/competition and usual physical activities, overall rates of patients receiving ICD-shocks among the athletic population are almost similar to rates reported for less active pediatric patients or adults, representing typical ICD-patients [6, 65]. Moreover, the ICD-sport registry does not document a higher

incidence of shocks in endurance sports [43], despite the fact that in this patient population the development of "Phidippides cardiomyopathy" could be hypothesized as the ideal substrate for re-entrant ventricular malignant tachycardia increasing the risk of SCD in this population. Furthermore this registry enrolled many athletes participating in moderate contact sports, but few in aggressive contact sports, and it is possible that incidence of ICD-system damage or injury may be higher in these sports. Freedom from lead malfunction at 5 years from ICD implantation was 97 % and at 10 years, it was 90 % [43]. Actually, these recent data do not support competitive sports restriction for all athletes with ICDs, and despite the occurrence of appropriate and inappropriate shocks, many of these athletes may engage in vigorous activities and competitive athletic activity without injury or potential shock failure to terminate arrhythmias.

Recommendations Regarding Athletic Involvement

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As the ICD patient population continues to expand, physicians are increasingly being asked for recommendations regarding what sport activities are allowed in these patients. They have to weigh the potential risk in athletic participation for ICD patients against the demonstrated adverse effect of physical inactivity [23]. This conflict is resolved if the patient has left ventricular dysfunction or exercise-induced malignant arrhythmias, but is more difficult in ICD-patients with normal left ventricular function [41]. While the issue has generated controversy, both the 36th Bethesda Conference [52] and the European Society of Cardiology (ESC) [29, 61] are in agreement on this point, despite the pronounced legal, social and cultural differences between the U.S. and Europe [62]. According to the Bethesda Conference, there is little room for medical discretion: ICD presence both for secondary or primary prevention should disqualify athletes from competitive sports, including those that involve bodily trauma (except “class IA” low-intensity activities) [52]. In Europe, ICD patients with no structural cardiac disease and preserved left ventricular function may be allowed to participate only low-static and low-dynamic sports except for those involving the risk of bodily collision [29, 61]. In summary, both U.S. and European documents state that ICD-patients can safely participate in activities such as golf, cricket, riflery, billiards and bowling, which are considered to be low-intensity sports. However, controversies regarding recommendations exist. In Europe, for example, a sports medicine specialist assumes the authority to apply disqualification [62]. In the U.S., on the other hand, disqualification of athletes with cardiac abnormalities from competitive sport practice can be recommended by the managing physician, although ultimately high-school or college officials are responsible for a decision, since no state or federal law governs medical clearance for high-school/college athletics [62]. The case of Nicholas Knapp, a basketball player at Northwestern University with hypertrophic cardiomyopathy and a secondary prevention ICD, is definitely a legal precedent for U.S. [48]. According to university’s team physicians, Knapp’s sport participation posed an unacceptable risk of SCD, while the athlete asserted that he should be permitted to assume risks associated with playing basketball, including risk of SCD. However, in this case an appellate court affirmed the right of the Northwestern University to exclude the athlete from sports participation based on the medical disability, given that college sports programs do not constitute matters of civil liberties [48].

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Potential shock-failure in ICD-athletes during physiologic sympathetic activation

Conclusions

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Despite recent encouraging data from the ICD sport registry, recommendations regarding athletic activity in ICD patients are still prudent for restricting participation in competitive sports, except those with low cardiovascular demand and no risk of collision. How best to evaluate an athlete’s individual risk before a potential ICD-implantation and optimum programming of ICD post-implantation are both important avenues for future research. Moreover, in recent years diffusion of home monitoring systems increasing frequency of ICD interrogation may aid in early detection of changes in lead performance. However, data on the risks or benefits of ICD in physically active patients are lacking, and in the future further data are definitely necessary to better define with acceptable risk the levels of sports participation for ICD-patients.

Acknowledgements

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Giuseppe Mascia MD, Giorgio Galanti MD: no conflicts of interest. Luigi Di Biase MD has received consultant fees or speaker honoraria from Biosense Webster, Hansen Medical, St Jude Medical and Biotronik. Andrea Natale MD has received consultant fees or speaker honoraria from Biosense Webster, Boston Scientific, Medtronic, Biotronik and Janssen. Luigi Padeletti MD is a consultant for Boston Scientific, Medtronic, St. Jude Medical, Sorin Biomedica. Affiliations 1 Department of Medical and Surgical Critical Care, University of Florence, Florence, Italy 2 St. David’s Medical Center, Texas Cardiac Arrhythmia Institute, Austin, United States 3 Sports Medicine Department, University of Florence, Florence, Italy 4 Cliniche Gavazzeni, Bergamo, Italy 5 Albert Einstein College of Medicine, Montefiore Hospital, Bronx, NY, United States 6 Division of Cardiology, Stanford University, Palo Alto, California, United States 7 Department of Biomedical Engineering, University of Texas, Austin, Texas, USA 8 Department of Cardiology, University of Foggia, Foggia, Italy 9 California Pacific Medical Center, San Francisco, California, USA 10 Heart and Vascular Center, Case Western Reserve University, Cleveland, Ohio, USA 11 Interventional Electrophysiology, Scripps Clinic, La Jolla, California, USA

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Notice: This article was changed according to the erratum on July 9th 2014. The HTML-Version contains an error in Affiliations. The 4th author A. Natale’s affiliation is St. David’s Medical Center, Texas Cardiac Arrhythmia Institute, Austin, United States not Sports Medicine Department, University of Florence, Florence, Italy.

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