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Sudden cardiac arrest in sports
-need for uniform registration
A Position Paper from the Sport Cardiology Section of the European Association
For Cardiovascular Prevention and Rehabilitation
Solberg EE 1 /Borjesson M 2, Sharma S 3, Papadakis M 3, Wilhelm M4, Drezner JA5, Harmon KG5,
Alonso JM 6, Heidbuchel H 7, Dugmore D 8, Panhuyzen-Goedkoop NM 9, Mellwig K- P 10, Carre F
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, Rasmusen H 12, Niebauer J 13, Behr ER 3, Thiene G 14, Sheppard MN 3, Basso C 14, Corrado D14 on
behalf of the Sport Cardiology Section of the EACPR of the ESC
Diakonhjemmet Hospital, Dept. of Medicine, Oslo, Norway 1, Swedish School of Sport and Health
Sciences and Karolinska University Hospital, Stockholm, Sweden 2, St George's University of
London, London, UK 3, University Clinic for Cardiology, Cardiovascular Prevention, Rehabilitation
& Sports Medicine, Inselspital, Bern, CH 4, Department of Family Medicine, University of
Washington, Seattle, US 5, Aspetar, Qatar Orthopedics and Sports Medicine Hospital, Sports
Medicine Department, Doha, Qatar 6 , Cardiology – Arrhythmology, University Hospital Leuven,
Leuven, Belgium 7, St. Georges Park International Sport Medicine Centre, Staffordshire , UK 8,
Radboud University Nijmegen MC and Sports Medical Centre Papendal Arnhem, the Netherlands 9,
Department of Cardiology, Heart and Diabetes Center NRW, Ruhr University of Bochum, Bad
Oeynhausen, Germany10, Pontchaillou Hospital, Rennes France and INSERM U1099, Rennes,
France 11, Dept. Of Cardiology, Bispebjerg University Hospital, Copenhagen, Denmark 12,Institute of
Sports Medicine, Prevention and Rehabilitation, Paracelsus Medical University, Salzburg, Austria 13,
Department of Cardiac, Thoracic and Vascular Sciences, University of Padua, Padua, Italy 14
Corresponding author:
Erik Ekker Solberg, MD, PhD, FESC
Diakonhjemmet Hospital, Dept. of Medicine, Oslo, Norway
E-mail: [email protected], Tel: +47 22451500, Fax: +47 22451776
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Abstract
There are large variations in the incidence, registration methods and reported causes of sudden
cardiac arrest/sudden cardiac death (SCA/SCD) in competitive and recreational athletes. A crucial
question is to which degree these variations are genuine or partly due to methodological
incongruities. This paper discusses the uncertainties about available data and provides
comprehensive suggestions for standard definitions and a guide for uniform registration parameters
of SCA/SCD. The parameters include a definition of what constitutes an ”athlete”, incidence
calculations, enrolment of cases, the importance of gender, ethnicity and age of the athlete, as well as
the type and level of sporting activity. A precise instruction for autopsy practice in case of a SCD of
athletes is given, including the role of molecular samples and evaluation of possible doping. Rational
decisions about cardiac preparticipation screening and cardiac safety at sport facilities requires
increased data quality concerning incidence, aetiology and management of SCA/SCD in sports.
Uniform standard registration of SCA/SCD in athletes and leisure sportsmen would be a first step
towards this goal.
Key words: sudden cardiac death, sudden cardiac arrest, sports, exercise, registry, athletes
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Abbreviations
DNA Deoxyribonucleic acid
ECG electrocardiogram
RNA Ribonucleic acid
SADS sudden arrhythmic death syndrome
SCA sudden cardiac arrest
SCD sudden cardiac death
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Introduction
In recent times, sudden cardiac arrest/sudden cardiac death (SCA/SCD), particularly among high
profile athletes, has gained huge attention. Such catastrophes have generated considerable scientific
interest and triggered debates relating to controversial issues such as the magnitude and the actual
causes of such events. At present, however, despite the impressive number of reports of SCA/SCD in
athletes, our understanding of the precise incidence, demographics, causes and circumstances
surrounding the issue remains limited. This is due to methodological inadequacies of the
observational reports, which include different inclusion criteria, diverse definitions and
characterization of the athletic population and non-uniform methodology in autopsy studies of
competitive and recreational athletes. So far, most of the discrepancies regarding the athlete’s
SCA/SCD are related to data collection which is derived from either prospective (1) or retrospective
registries (2-4), voluntary reporting (5) or from media reports (6). The absence of a uniform
registration method means that it is impossible to compare different data sets; therefore, high quality
meta-analyses are largely unachievable at the present time. Most of the reliable information relating
to the incidence and causes of SCD in young athletes is derived from the Veneto region of Italy,
which maintains a prospective pathology registry on SCD. However, it is difficult to extrapolate
these results to all countries, which vary with respect to the ethnicity of sports participants, the nature
of sporting disciplines practiced, the emergency response plans in the athletic fields and the methods
for performing autopsies.
Aim of paper
The aim of this paper is to provide a template for a uniform registration and autopsy procedure of
SCA/SCD in competitive and recreational athletes which could be applied internationally and is
based on standard definitions. The intention is to improve our understanding of SCA in athletes by
supporting the implementation of a uniform method of registration of SCA/SCDs, of the autopsy
procedures, of the emergency response interventions as well as outcomes (7, 8), which could aid
persons, institutions, organizations, countries or larger regions in developing strategies for
preventing such tragedies.
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Definitions
SCA in sport
In the present manuscript, we focus on SCA/SCD occurring during sport or in close conjunction with
sporting activity. For scientific purposes, it would be useful to clearly define the term ‘sudden’, since
this will influence the incidence rate and have an impact on the epidemiological data. For example,
the proportion of all deaths defined as SCD is 13% when a definition of one hour from onset of
symptoms is used (9), whereas the proportion of SCD rises to 19% when a 24-h time-frame is used
(10). The issue is even more complicated, however, since there are reports of malaise or SCA during
sports, with death occurring several days afterwards (4).
Suggestion: For the purpose of the present paper, we rely on the definition of SCA/SCD occurring
during or within a short period in relation to participation in sport. We suggest to include in the
registry detailed information relating to the time interval in hours between eventual symptoms and
SCA/SCD and the sporting activity and SCA/SCD; categorizing the event as occurring during or
within 1-24 hours post-exercise.
Competitive and recreational athletes
For the purpose of this document, “competitive athletes” are defined as individuals who are
engaged in exercise training on a regular basis and participate in official sports competition. Usually,
they exercise >10hrs per week. A subgroup is the “elite athletes”. The target of the competitive
athlete is to continuously improve their performance and thereby achieve the best possible results in
competitions. Official sports competitions (local, regional, national or international) are defined as
organized team or individual sports events that place a high premium on athletic excellence and
achievement and are organized by a recognized athletic association.
In contrast, “recreational athletes” are defined as individuals engaged in recreational or leisure-time
sports’ activities, on either a regular basis or intermittently. Usually, they exercise <10hrs per week.
Recreational sports do not necessarily require systematic training or the pursuit of excellence, nor do
they convey the same pressure to prevail against others.
Suggestion: “Athletes” should be defined according to the type, frequency, duration and intensity of
sport participation and categorized into “competitive” or ”recreational”.
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Incidence of SCA/SCD in sport
Methodical differences in characterizing the sporting population are likely to contribute to the large
variations in the reported incidence rate of SCA/SCD in sport in the literature, although a generally
accepted value is 1-3:100 000 (11-13). In selected populations, such as military recruits (14) and in
subpopulations of elite athletes (i.e. African-American professional athletes), the incidence of SCA/SCD
has been reported to be substantially higher. The methodological limitations and inadequacies of current
studies are highlighted by two investigations examining the same population of Minnesota high school
athletes, but yielding widely different estimate (15, 16).
Additionally, the large variability of the prevalence of SCA/SCD may in part reflect the role of several
factors that influence SCA/SCD such as the type and level of sports activity, the personal characteristics
of the athlete including the age, gender and ethnicity), climate, as well as behavioral issues (including
drug abuse), regardless of the existence of an underlying pathologic condition.
Suggestion: To include in the registration form factors that may predispose for SCA/SCD, such as
the type and level of sports, age, gender, ethnicity, climate and athlete’s specific behavior, which
may improve our understanding of the event.
Proposed elements of the registry
Comprehensive enrolment of cases
The registry must have a system in place for collecting all cases at regional and national level. Often
the real number of deaths (the numerator) is not consecutively and systematically reported (5).
Harmon et al. and Holst et al. showed that a larger part of the SCA in sports is not captured by media
and, therefore, would not have been identified in a media-based registry (17, 18). Steinvil et al. (6)
reported an overall very low prevalence of SDs in Israeli athletes based on media reports from two
newspapers, raising the suspicion that many cases were missed (19). Another source of error is that
many cases cannot be classified accurately due to missing records, lack of autopsy or non-specific
descriptions of pathology reports. In one retrospective registry-based study, Solberg et al. were
unable to classify 17 % of potential cases (4).
The strategy to ensure comprehensive case enrolment is likely to vary between different countries.
One proposal would be to establish a mandatory emergency ambulance registry which is able to
capture most cases of SCA/SCD (20). Another source of data would be the reporting of all SCD
cases in sports by pathology centers, which may compensate for cases where an ambulance service
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was not involved. To complete case enrolment, researchers should also search other relevant national
sources like e.g. death registries, when available. However, the quality of the data in death registries
ultimately relies on the standard of pathology and/or clinical assessment by the doctor providing the
final diagnosis.
Suggestion: To capture all consecutive cases of SCA/SCDs in the registration form by specifying the
source of this information (ambulance, autopsy, or other source). It is of great relevance not to miss
the survivors (successfully resuscitated SCA).
Demographics
The athlete’s age, gender, ethnicity, sporting discipline and intensity of exercise may influence the
incidence of SCA/SCD during sports.
Age
The incidence rate of SCD in sports is 4-5 times higher in older age groups (>35 years, e.g. master
athletes) compared to athletes of a younger age (≤35 years) (12, 21, 22). These differences reflect a
higher burden of underlying cardiovascular diseases (mostly, ischemic heart disease) consistent with
increasing age. Incidence numbers in the older athletes range from 1:1500-1:50000 (20, 23-25). The
French study on sports-related SCD in the general population shows a clear preponderance of older
athletes (26).
Gender
There has traditionally been a very strong male predisposition to SCA/SCD with ratios of 10:1
amongst competitive athletes (5, 26) and up to 20:1 in the general exercising population (12, 26),
which cannot be explained uniquely by differences in gender participation rates. One large study of
US collegiate athletes showed a lower male/female ratio in cases of SCD (2,3:1) (17).
Ethnicity
Athletes of black ethnicity appear to have a higher incidence of SCA/SCD compared with Caucasian
athletes (27). Black U.S. college athletes had a considerably (about 3-5 times) higher risk of SCD,
compared to white athletes (17, 27). The term “black ethnicity” is ambiguous and comprises
different populations such as Afro-American, Afro-Caribbean, Eastern-Africans and WesternAfricans. Nuances within the term “black ethnicity” as well as those denoting the term “white
(Caucasian) ethnicity” may have an important bearing on the incidence and cause of SCD. The issue
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of race is increasingly complicated as there are a growing number of individuals worldwide who are
of mixed ethnicity (e.g. one parent white, one parent black).
Suggestion: The demographic characteristics of an athlete should be documented. The issue of
ethnicity is complex. In this regard the athletes should be categorized as Caucasian, or Black
(African-American, Afro-Caribbean, Eastern-African, Western-African), or South American, or
Asian (with specific information). In cases of mixed ethnicity data should include elaborate details of
the origins of both parents.
Type of sport
Different sporting disciplines vary with respect to the magnitude of demand applied on the
cardiovascular system, as illustrated in the frequently used Mitchell’s classification of sports (28).
However, this classification does not completely define type of sports according to cardiac load,
relative intensity of exertion, duration and hemodynamic and neuro-adrenergic load, factors that may
be important for triggering SCA. In Bille’s review of SCD in young athletes, the number of cases
was highest in soccer, basketball and running (29). Harmon et al. found the highest incidence in US
collegiate basketball players (i.e.,1:11 000 per year) (17). A probable explanation of these
differences is that various sporting disciplines have a dissimilar participation rate in different
countries. Another point to be considered is the time spent in sport.
Suggestion: To include data on the type and characteristics of sport when the SCA occurred,
whether SCA occurred during training or competition, as well as (estimated) number of years
practicing the sport. At present we recommend the use of the Mitchell’s classification of sports (28).
Level of sport
The risk of SCA/SCD in competitive athletes seems increased compared to leisure sportsmen and
non-athletes (26). The incidence was 2.8 times higher in younger Italian competitive athletes
compared to non-athletes (30). In a US college athletes material, the incidence of SCD was related to
the increased level of competition; in division I 1:29 000, compared to division II (1:42 000) and
division III (1:95 000 (17). Similarly, van Camp found a twofold increase on sudden death in college
athletes compared to high school athletes (31). Toresdahl et al. found a 3.6 times relative risk of
SCA in high school student athletes compared to student non-athletes (32). The relationships,
however, between the level of sports and the risk of SCD are probably multi-factorial and complex
and require further study.
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The risk of a particular sport activity is also dependent on the type of athlete population engaged in
that sport. For instance, marathon and cross-country competitions are mainly composed of amateur
non-elite master athletes, and the incidence of SCD has been described to be 1-2/100 000 (2). Sahlén
et al. showed that certain participants in these races carry severe underlying cardiovascular disease
(33). The higher incidence figures reported in non-elite events, such as marathon, half marathons and
recreational sports (26) may be the expression of higher-risk population engaged in these sporting
disciplines and not the type or level of sport activity per se.
Suggestion: In the SCA/SCD victim, define the precise level of the athletic activity, suggested as:
elite level (professional and semi-professional)/competitive level (including usually more than 10
hours exercise/week)/ recreational and leisure-time athletic activity and including the number of
exercise hours/week.
Clinical information
A detailed personal and family history and knowledge of the precise circumstances of death are
crucial items of information. Specifically, a known cardiac disease and the presence of antecedent
symptoms (pre/syncope, chest pain, abnormal dyspnea during activity), prior cardiac history, family
history of premature (< 50 years old) cardiac disease (coronary artery disease (CAD),
cardiomyopathy, ablations or pacemaker implants and diabetes mellitus) are important elements for
registration. In addition, availability of ECG recordings performed during life should be traced.
Suggestion: Clinical data and all medical records prior to the event, including any available ECG,
as well as other available diagnostic testing (echocardiography, cardiac magnetic resonance
imaging (CMR), blood testing), should be registered. In addition, reports about the deceased athlete
provided by relatives should be traced.
Aetiology of SCA/SCD in athletes
In young athletes, a wide spectrum of underlying inherited, congenital and acquired cardiovascular
abnormalities are reported as a cause of SCD (5, 23, 31, 34). The leading causes include diseases of
the myocardium; cardiomyopathy (either hypertrophic cardiomyopathy (HCM)) or arrhythmogenic
right ventricular cardiomyopathy, ARVC), coronary artery anomaly (CAA), premature coronary
artery disease, cardiac ion-channelopathies (long & short QT-syndrome, Brugada syndrome,
catecholaminergic polymorphic ventricular tachycardia), complications related to Marfan’s
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syndrome, and acquired disorders; commotio cordis (CC) and acute myocarditis (35-37). In master
athletes, the primary cause of SCD is CAD (2, 23, 38, 39).
Regarding non-fatal SCA in athletes, there are no comprehensive data available. The knowledge of
non-fatal causes of SCA relies on clinical evaluation of single cases and the extrapolation of the
findings from cases of SCD.
Preparticipation evaluation affects the aetiology
Preparticipation evaluation of athletes may identify individuals harboring diseases that may convey a
greater risk of SCA in association to sports. According to the current recommendations (40), affected
athletes may be disqualified from competition or advised to restrict their athletic activity. Thus, the
preparticipation evaluation procedure itself may affect the aetiology and incidence figures of SCD in
a particular geographic region.
Pathology vs. normal heart
The distinction between pathologic and normal variants is another challenge in the context of SCD in
athletes (41). Post-mortem diagnoses of HCM and ARVC are sometimes based on the presence of
isolated, even mild, left ventricular hypertrophy (LVH), or fatty detection on the right ventricular
wall, respectively, in the absence of the pathognomonic histological changes (42). Isolated LVH,
however, is a well-recognized feature of physiological cardiac adaptation to exercise (43). Isolated
fatty infiltration of the right ventricle may be present also in the normal heart (44, 45). Moreover,
uncertainty may exist as to the causal relationship between pathological findings and the SCD event.
For instance, the significance of myxoid degeneration of the prolapsed mitral valve, stable
atherosclerotic coronary plaque with limited (<50%) luminal stenosis, myocardial bridging, and focal
myocarditis, may be overestimated and attributed as the cause of death. Such findings however are
also relatively prevalent in the general population (42).
Therefore, caution should be used in interpreting the borderline pathologic findings, as suggested by
the guidelines for autopsy investigation of SCD developed by the Association for European
Cardiovascular Pathology (41). Here the authors highlight the concepts of “different degrees of
certainty in defining the cause–effect relationship between the cardiovascular substrate and the
sudden death event” and the existence of “grey zones” particularly in the setting of myocardial
diseases (41). In these particular instances, screening of relatives may add information that clarifies
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the cause of death. Papadakis et al. demonstrated that familial evaluation of first-degree relatives of
victims of SCD with post-mortem findings of uncertain causal effect could identify a primary
arrhythmogenic syndrome in 46% of cases, a proportion similar to a contemporary series with
normal post-mortem examinations (sudden arrhythmic death syndrome, SADS) (42).
Post-mortem recommendations
The cause of SCD during sport should be established by autopsy, ideally by a cardiac pathologist,
including histological evaluation of the ventricular myocardium, coronary arteries and specialized
conduction tissue, or by additional genetic or toxicological tests. Identification of the cause of the
SCD may be difficult in individual cases, due to the varied degree of morphologic expression of the
arrhythmogenic cardiomyopathies, as well as the lack of structural abnormalities in purely electric
syndromes. Difficulties in establishing the underlying cause greatly affects the precision of data of
SCA/SCD in sports. In addition, many countries are not obliged to conduct autopsies. Therefore, the
number of autopsies will be low, which will affect the precision and the understanding of the causes
of SCD.
The results of the autopsy may trigger new specific screening efforts aimed at identifying potentially
inherited cardiac pathology of first-degree relatives (41). For example, the identification, or the
absence, of any identifiable cardiac pathology at post-mortem, directs the familial evaluation to a
probable diagnosis of structural disorders or primary arrhythmic syndromes, respectively. Erroneous
autopsy diagnoses may misguide familial evaluation or conversely, offer false reassurance for
surviving relatives and dissuade physicians from initiating familial screening altogether, with
potentially devastating consequences for future generations. Thus, accurate interpretation of the
autopsy findings by the pathologist is pivotal (43, 44).
According to the Association for European Cardiovascular Pathology Guidelines for autopsy
investigation of SCD, full autopsy with sequential approach should always be performed to exclude
extra-cardiac causes of sudden death, mostly cerebral or respiratory (41). After exclusion of noncardiac causes, any natural sudden death can be considered cardiac in origin. A detailed protocol of
examination of the heart should be then applied to each case.
Suggestion: Pathologists evaluating an athlete’s heart should adhere to the guideline document
produced by the Association for European Cardiovascular Pathology. The guidelines provide a
detailed account on how to perform the post-mortem evaluation, interpret the results and assign the
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death to specific findings. Cases of SCD in sports in young individuals where diagnostic uncertainty
persists (e.g. in all cases where the cause of death cannot be ascertained with certainty) should be
referred for further evaluation to an expert cardiac pathologist. The examining pathologist should
make a transverse apical section of the heart and take a small sample of myocardium, before fixing
the full heart in formalin 10%. If the heart cannot be retained, it is essential that extensive
photographic documentation is made and multiple samples of the myocardium are taken from a
representative transverse slice of the ventricles to include the free wall of the left ventricle (anterior,
lateral and posterior), the ventricular septum (anterior and posterior), and the free wall of the right
ventricle (anterior, lateral and posterior), as well as right ventricular outflow tract and one block
from each atria. Furthermore, any segment of the myocardium, coronary arteries, valves and great
vessels with significant macroscopic abnormalities should be sampled for histology and stained with
Hematoxylin and Trichrome. Additional stains are performed as indicated. For molecular and
toxicological studies, appropriate storage of autopsy tissues and fluids is essential. If no on-site
facilities are available, the stored material should be sent to the nearest specialized laboratory.
The autopsy report should include a detailed description relating to the histopathological evidence
that support the final diagnosis and the degree of certainty of a cause-effect relationship between the
identified substrate and the SCD (i.e. certain, highly probable or uncertain cause of SCD) (41, 42). It
is recommended that EDTA blood (10 ml) is frozen at -20° and heart and spleen tissues (5 g) are
either frozen and stored at -80°, or stored in RNA later at 4° for up to two weeks before extraction
(41). Samples can be utilized to look for viral DNA-RNA genomes by PCR and reverse transcription
polymerase chain reaction (RT-PCR), as well as genetic screening by DNA direct sequencing in
suspected genetically determined heart diseases (molecular autopsy).
Evaluation of relatives
Evaluation of first degree relatives with ECG or an exercise stress test may provide answers to the
cause of death in autopsy-negative cases. In such instances, molecular testing of an arrhythmia
syndrome related gene panel can be useful for making a diagnosis and if targeted to genes relevant
to the findings in a family may support the underlying diagnosis (46).
Molecular autopsy
When performing an autopsy of a SCD case, in which the heart is morphologically “normal” and no
other aetiology, on toxicology or otherwise, can be identified, the death is labeled as SADS (47, 48).
Molecular autopsy and familial studies in victims of SADS indicate that a considerable proportion of
deaths may be attributed to primary arrhythmogenic cardiac disease. Therefore, we believe it to be
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appropriate that all cases of SD in athletes that remain unexplained despite autopsy by an
experienced pathologist should undergo genetic analysis for the most common arrhythmogenic
syndromes. This may provide a diagnostic result in an additional 20-30% of cases, and may be
applied for cascade genetic testing in relatives. If the genetic result is negative, clinical screening
should still be advised for first-degree relatives. In this setting, cardio genetic family screening may
represent a good opportunity to achieve a diagnosis of the “culprit” inherited heart disease and to
identify other relatives at risk (46, 49).
Virtual autopsy
Virtual autopsy through comprehensive postmortem imaging is evolving and has been proposed as
an alternative to traditional autopsy, particularly in the forensic setting (50, 51). Taking into account
the most common causes and mechanism of SCD in athletes, however, it could assist in the few
mechanical SCDs (i.e. pulmonary embolism, hemopericardium), but would fail detect the majority of
SCDs due to electrical abnormalities. However, virtual autopsy may prove invaluable in excluding
extra-cardiac causes of death in athletes when autopsy is denied by relatives either due to personal or
cultural reasons (52).Thus, modern imaging techniques provide an opportunity for post-mortem
diagnostics to complement, but not replace, traditional autopsy, when looking for the wide spectrum
of causes of SCD in competitive athletes.
Toxicology
Despite the large number of circumstantial reports, there is no clear scientific and unequivocal
evidence supporting or invalidating the wide perception of the influence of doping on SCA/SCD in
sports. Only registration over time, of toxicological agents would help to clarify the actual role of
doping in SCA/SCD. Indirect evidence, however, links the abuse of illicit drugs to SCA in sports.
Such drugs may trigger a wide range of exercise-related cardiac arrhythmias that can be lethal (52).
Abuse of performance-enhancing substances is associated with LVH and repolarisation changes
(53). A body of information exists on cardiovascular side effects of anabolic steroids (AAS),
including lipoprotein profile abnormalities, thrombotic diathesis, coronary vasoconstriction, cardiac
arrhythmias and increase of blood pressure (54, 55). Case studies point to AAS abuse being linked to
acute myocardial infarction and fatal ventricular arrhythmias (56). Other substances have also been
associated with sudden death in sport such as stimulants (amphetamines, cocaine, ephedrine
alkaloids) and erytropoietin (EPO) (52, 56-58). Since there is a large inter-individual variability in
responses to a drug, the adverse effects depend on the type, amount and duration of intake of the
consumed drug as well as the individual susceptibility (55). Scientific reports describing the
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cardiovascular deleterious effects of drug abuse are scarce. Therefore, even when the heart is found
to be abnormal during macroscopic and microscopic examination, toxicology screen for illicit
substances should always be performed prior to attributing the findings to a primary
cardiomyopathy.
Suggestion: When investigating SCA/SCD in sports, we recommend full screening of toxic and
possible doping substances and referral of urine and blood samples to the closest qualified
laboratory. In case of doping substances, follow the legal procedures to allow the testing to be
performed. A proper selection, collection and submission of specimens for toxicological analyses are
mandatory for accurate and scientifically valid results. Urine and blood are the only matrixes
accepted to detect prohibited doping substances and methods (59). The target, and the challenge, is
to obtain accurate and sensitive assessment of used substances in urine or blood in due time after
their intake (55). Toxicological analyses should be quantitative and the following amounts are
usually required: heart blood 25 ml, peripheral blood from femoral veins 10ml, urine 30-50 ml, and
bile 20-30 ml (when urine is not available). All samples are stored at 4°C. A lock of hair (100-200
mg) for possible chronic drug abuse testing should be cut from the back head or from the pubic hair.
Limitations of autopsy
A common perception is that autopsy presents the definitive causal answer to the death. Whilst it
may provide the most definitive answer in several cases, it is imperfect. The reproducibility of
autopsy diagnoses is scarcely studied. Therefore, we reasonably assume that variance in the autopsy
reports describing aetiology of SCD in sports may also be related to the variability of the procedures
in post-mortem assessments. Additionally, diagnosis may be difficult in case of borderline
pathologic features, such as mild LVH or ventricular dilation, or when the significance of the
pathologic report is controversial, such as in case of isolated myocardial bridging, mild right
ventricular fatty infiltration, scattered inflammatory cells or isolated spots of fibrosis.
Other potential limitations of the autopsy are related to the quality of assessment by the forensic
pathologist who performs the initial examination in most cases of SD. This is underscored by the fact
that SCD in athletes are caused by a spectrum of different conditions whose prevalence in the
general population is low. Consequently, the performing forensic pathologist may have limited
experience with the diagnoses of conditions predisposing to SCD in athletes. It has been shown that a
large disparity exists as to the potential cause of death when comparing specialized cardiac
pathologist vs. general pathologist reports (60). General pathologists are more likely to attribute
death to structural causes rather than designate the heart as normal, by attributing, for instance,
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isolated fatty infiltration of the right ventricle to ARVC and LVH, in the absence of myocyte
disarray, to HCM.
Diagnoses based on circumstantial evidence
Some diagnoses are based on circumstantial evidence particularly when the autopsy fails to identify
an underlying cardiac abnormality. Commotio cordis (CC) is the result of a malignant ventricular
arrhythmia caused by a sudden, blunt trauma to the chest (61). Commotio cordis was the cause of
SCD in 20% of cases reported by Maron et al. (62), but is probably underreported in Europe (63).
Baseball is the leading cause in the US, but CC has also been reported in soccer, ice-hockey and
karate (61). The diagnosis of CC is dependent on a thorough description of the circumstances related
to the event preceding collapse of the athlete.
Suggestion: Describe precisely the circumstances (including any collision between the victim and
another person or an object like a ball) related to the SCA/SCD in sport.
Management of SCA
Infrastructure on the sport site
Sport can be practiced in various locations, at sports fields, but also in cities or in isolated and remote
areas. Information concerning the infrastructure at a specific site where SCA/SCD has occurred
should be recorded. This may include the management of the SCA, the skills available to deal with
SCA (Cardiopulmonary resuscitation (CPR)), the availability of cardiac defibrillation equipment and
the speed at which the appropriate interventions were delivered. Teams, clubs, schools, and other
establishments organizing sports are in a unique position to monitor their athletes for cases of
SCA/SCD, and subsequently to report incidents through a uniform registration protocol. As
emergency procedures in sporting venues greatly impact outcomes from SCA, every organization
should have in place an acute cardiovascular emergency procedure to respond to a collapsed athlete
(64). A comprehensive emergency response plan for SCA including rapid public access to an
automated external defibrillator (AED), increases the likelihood of bystander CPR, reduces the time
to defibrillation, and improves survival from SCA in the athletic setting (65, 66). Successful
emergency response plan programs require an organized and practiced response, an established
communication method to activate the local emergency medical services system, and rescuers trained
and equipped to provide CPR and defibrillation.
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Borjesson et al. surveyed the emergency cardiovascular care at major sporting arenas in Europe
questioning the emergency planning, availability of AEDs, emergency personnel, and distance to the
nearest hospital. Only 64% of major football arenas had a written medical action plan for SCA, and
72% had on-site AEDs. In addition, approximately 25% of the arenas situated longer than 10 minutes
from the nearest hospital did not have an on-site AED (67). These findings led to the development of
European consensus recommendations on cardiovascular safety at sports arenas (68).
Suggestion: Include data both of the site of the SCA and of the cardiovascular preparedness
(medical action plan, presence of AED, and training of rescuers) of the sporting site in the registry.
Resuscitation
The success of out-of-hospital resuscitation depends on early recognition of the situation, willingness
and knowledge on how to perform CPR, or how to apply an AED. Data indicates that increased
public awareness of SCA/SCD in sports may have improved survival rate after SCA (7, 8). Delayed
recognition of SCA by first responders, can lead to delays or even failure to activate the emergency
response system, initiate CPR, and provide early defibrillation. Resuscitation may be delayed for
several reasons; people are reluctant to resuscitate, or SCA is mistaken for a seizure or other cause of
collapse (65). Another challenge in recognizing SCA in athletes includes inaccurate rescuerassessment of pulse or respiration (69). Unfortunately, bystander CPR is initiated in less than one
third of cases of witnessed SCA in the general population (69), and, if initiated, more than 40% of
chest compressions are of insufficient quality (70). Consensus guidelines and several public access
defibrillation studies uniformly support access to early defibrillation, targeting a time interval of less
than 3 to 5 minutes from collapse to first shock (64, 71). Reports from schools with an on-site AED
program sustain an improved survival rate for young athletes with SCA if early defibrillation is
achieved (65, 66). Rapid defibrillation has led to increase in survival rates if bystander CPR is
provided and defibrillation occurs rapidly (2, 72), although the underlying disease also is an
important factor (12). There is a great variation in the use of bystander CPR (73), also within the
same country (74, 75). It is prudent to get detailed and uniform information about resuscitation
procedures in cases of SCA, to improve the management of these events.
Suggestion: Use the form in this paper, adapted from the Utstein criteria (76, 77), to obtain uniform
data on clinical management of SCA/SCD in athletes. Data on delay of action, CPR, defibrillation
time and history as well as advanced life support should be included.
Framework for a registry
17
An accurate registry of SCA/SCD is dependent on an organizational frame collecting systematic
information from various collaborative sources including emergency services, witnesses, hospitals,
pathologists and toxicologists. Collaboration among the different actors in the scenario of a SD in
sports is illustrated by experience derived from the registry from the Veneto region of Italy (1) and
from registries in Switzerland and the Netherlands (78, 79).
Suggestions:
Scientific and sporting organizations should promote a national registry which national public
health authorities should undertake and maintain the responsibility of. Mandating the reporting
system may be an obstacle. To integrate sports-related SCA/SCD in existing death certificate system
or other registration system might be a future aim.
As a start, we suggest that at the very least SCA/SCD among competitive athletes in organized sports
should be included. Individual countries may choose to also include recreational athletes based on
feasibility of their infrastructure. The inclusion of all individuals suffering a SCA/SCD during
exercise, though, is desirable to provide a comprehensive understanding of the issue.
The creation of a national body responsible for the collection of the data on SCA would be ideal.
Similarly, it would be prudent to establish a working group on SCD including genetic counselling of
first degree relatives. In the instances where an athlete is considered to have died from a potentially
inherited condition, it would be prudent to approach first degree relatives and discuss inherited
disease and prompt referral to a cardiac expert in the field. A good network and co-operation with
relevant national institutes of forensic medicine is essential for the functioning of the registries.
A quality-tested website should be established. To complement this, an integrated professional- and
an observer access for relatives, coaches and journalists to report cases can be set up.
In cases of SCA, the need for professional help for the bereaved must be acknowledged.
If health personnel are time constrained due to extraordinary circumstances when completing the
registration form, as a minimum, the identity of the victim and date of the event must be filled in, thus
completing the lower quality of data necessary.
To uphold the necessary motivation of the people to submit all cases continuously is a challenge and
should be encouraged repeatedly. This necessitates continued education and information to the
18
relevant health care providers. Research from the registries will aid in continuous education and in
spreading the information.
Concluding remarks
There is a pressing need for uniform registration of sport-related SCA/SCD in order to improve our
understanding of these tragedies. The aim of this document is to provide a comprehensive outline for
such a registry that would be applicable in different countries despite potential practical, ethical and
medico-legal challenges. It is our aspiration that national organizations and public health authorities
may look favorably upon these recommendations as they are or refine them in the future, as a model
on how to construct national registries on SCA/SCD in sports and to design future epidemiological
studies.
19
Acknowledgements
We acknowledge all the Science Committee members of the EACPR, Massimo F. Piepoli
(chairman), Francesco Cosentino, Dirk De Bacquer, Esteban Garcia Porrero, Pedro Marques-Vidal
and Josef Niebauer as reviewers of the paper. Thanks to members of the nucleus, section for sports
cardiology, EACPR, 2012-2014, for helpful discussions. This work was partly supported by The
Lærdal Foundation for Acute medicine. Conflict of Interest: none declared.
20
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