Author + information
- Received January 11, 2014
- Revision received April 13, 2014
- Accepted May 12, 2014
- Published online August 5, 2014.
- Lior Yankelson, MD, PhD∗,
- Ben Sadeh, MD∗,
- Liron Gershovitz, MD∗,
- Julieta Werthein, MD†,
- Karin Heller, MD†,
- Pinchas Halpern, MD†,
- Amir Halkin, MD∗,
- Arnon Adler, MD∗,
- Arie Steinvil, MD∗ and
- Sami Viskin, MD∗∗ ()
- ∗Department of Cardiology, Tel Aviv Sourasky Medical Center and Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel
- †Department of Emergency Medicine, Tel Aviv Sourasky Medical Center and Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel
- ↵∗Reprint requests and correspondence:
Dr. Sami Viskin, Department of Cardiology, Tel Aviv Medical Center, Weizman 6, Tel Aviv 64239, Israel.
Background Two important causes of sudden death during endurance races are arrhythmic death and heat stroke. However, “arrhythmic death” has caught practically all the attention of the medical community whereas the importance of heat stroke is less appreciated.
Objectives The study sought to determine what percentage of life-threatening events during endurance races are due to heat stroke or cardiac causes.
Methods This retrospective study examined all the long distance popular races that took place in Tel Aviv from March 2007 to November 2013. The number of athletes at risk was known. The number of athletes developing serious sport-related events and requiring hospitalization was known. Life-threatening events were those requiring mechanical ventilation and hospitalization in intensive care units.
Results Overall, 137,580 runners participated in long distance races during the study period. There were only 2 serious cardiac events (1 myocardial infarction and 1 hypotensive supraventricular tachyarrhythmia), neither of which were fatal or life threatening. In contrast, there were 21 serious cases of heat stroke, including 2 that were fatal and 12 that were life threatening. One of the heat stroke fatalities presented with cardiac arrest without previous warning.
Conclusions In our cohort of athletes participating in endurance sports, for every serious cardiac adverse event, there were 10 serious events related to heat stroke. One of the heat stroke–related fatalities presented with unheralded cardiac arrest. Our results put in a different perspective the ongoing debate about the role of pre-participation electrocardiographic screening for the prevention of sudden death in athletes.
There is an increasing rise in the number of recreational runners participating in long distance races of 10 km or more, generally referred to as endurance races. For instance, approximately 500,000 runners crossed the finish line of a marathon race in the United States in 2011 alone, representing a 20-fold increase from the 25,000 finishers in 1976 (1). Although regular physical activity is generally considered healthy and is recommended by all major cardiovascular societies (2), long distance running, especially full and half marathon races, involve an increased risk of sudden death (3). Although the absolute risk for the participants is low, ranging from 0.5 to 1.5 cases per 100,000 athletes (3–7), such tragedies are particularly meaningful, because they involve young subjects, perceived to be healthy, dying as a result of participating in a recreational event.
Two important causes of sudden death during endurance races are arrhythmic death and heat stroke. Yet, arrhythmic death has caught the majority of attention from the medical community. For example, a PubMed search (performed in 2013) using the key words [“arrhythmias”] AND [“athletes” OR “sports”] yields >1,500 medical studies; in contrast, there are <260 medical publications on [“heat stroke”] AND [“athletes” OR “sports”].
Exertional heat stroke is defined as a core body temperature of >104°F to 105°F (40.0°C to 40.5°C) associated with multiorgan dysfunction (8). Cerebral dysfunction, a sine qua non of this entity, ranges from disorientation, confusion, loss of balance, irrational behavior, apathy, aggressiveness, and delirium to sudden collapse with loss of consciousness. Importantly, the initial symptoms of heat stroke often go unrecognized, so rapid deterioration culminating in cardiac arrest (9) and ventricular fibrillation (10) may occur. Moreover, in an athlete admitted after sudden collapse, the diagnosis of heat stroke will be missed if—as often happens—the core body temperature is not immediately measured (11). In such cases, a primary cardiac disorder may be suspected when arrhythmias predominate the clinical presentation at the time of collapse.
During a 2011 Tel Aviv endurance race, heat stroke by far outweighed cardiac conditions as the reason for admission of participant athletes to our hospital (a tertiary medical center, serving as the city hospital of Tel Aviv). In light of this, we conducted the present study to define the role of heat stroke and cardiac arrhythmias as the cause of serious sudden adverse event among athletes participating in endurance races.
We performed a retrospective study of all the long distance races that took place in Tel Aviv between March 2007 and November 2012 and prospectively collected data for the 2013 races. The number of athletes participating in each 1 of the races was obtained from the official database of the race organizations. The number of athletes experiencing serious sudden adverse events was determined from the number of race participants requiring emergency medical care and hospitalization as a consequence of medical event occurring during the race.
Since 1997, public races have been conducted in Tel Aviv twice a year. To avoid extreme weather conditions, 1 daytime race (the Tel Aviv Race) is conducted during early spring, whereas the other (the Tel Aviv Night Run) is conducted during the summer but at night. The races offer several options for professional and amateur participants, including 10 km, half marathon (21.1 km), and full marathon (42.2 km) tracks. The 2 races are held within the perimeter of downtown Tel Aviv, and the entire path of the races is within 10 min driving distance from the Tel Aviv Medical Center, the city hospital. Therefore, athletes developing serious medical problems are transferred to our hospital.
In these popular races, participants range from highly trained athletes, mainly racing the marathon, to self-trained amateur athletes, mainly participating in the popular 10 km and 21.1 km races. Participants have to register in advance. The number of runners in each race was obtained from official online records, which track the athletes that cross the finish line (12).
The Israeli sports law states that pre-participation medical approval, including mandatory electrocardiographic (ECG) screening, is required for participants who are organized in teams or associations, but not for subjects attending public sporting events, such as these studied races. To participate in these races, the runners only were required to submit a personal statement confirming a state of “good health.” Nevertheless, to determine the percent of participants undergoing medical and/or ECG screening prior to the races, we performed a prospective evaluation using a questioner that was distributed among participants of the 2013 race (see subsequent sections).
Medical attention at all these races included several levels: 1) the first level involves the national medical emergency service “Magen David Adom” (Israeli equivalent of the Red Cross) with ambulances, mobile intensive care units, and paramedics on motorcycles spread along the course of the race; and 2) a first-line emergency station deployed by the director of our Department of Emergency Medicine (P.H.) and fully trained emergency medicine physicians from our hospital. This first line station is located nearby the finish line that is common to all the races. This station is fully equipped with means of resuscitation, including mechanical respirators. Initial medical attention is provided on the track by either ambulance teams or scooters equipped with basic and advanced life support capability. Following initial contact with an emergency service team, patients are either discharged or transported for further evaluation and treatment. Patients in unstable condition, particularly those requiring resuscitation maneuvers in the last part of the race, nearby the finish line, are transported to the first-line emergency station, where advanced medical care is available. From there, patients are either discharged or further transported to our hospital. Importantly, participating medical professionals are fully aware of the risks of heat stroke and are instructed to actively search for this diagnosis by checking rectal temperature immediately on arrival.
We defined serious sports-related adverse events as any medical problem occurring to an athlete participating in the race that resulted in either death or hospitalization. One assigned investigator evaluated all these cases. A serious adverse event was further defined as life threatening (if cardiopulmonary resuscitation or mechanical ventilation were required and were followed by hospitalization in an intensive care unit) or a fatal event (if it resulted in death). Confidence intervals of the mortality rate were calculated with the Wilson score for binomial parameters (13).
Pre-participation screening survey
To assess the public compliance with Israeli Sports Law, which mandates medical and ECG screening for those participating in organized sports, we prospectively conducted a questioner-based survey on the day of the 2013 Tel Aviv marathon race. Athletes participating in the race were invited to take the survey sometime before crossing the starting line or after crossing the finish line. To encourage honest and full disclosure, we conducted the survey in an anonymous fashion. The questions in the survey were based on the assessment recommended by the American Heart Association (14). In addition, the survey collected information about the percent of race participants who had undergone screening with resting ECG and exercise stress testing. Of note, the exact number and demographic features of the athletes who declined the survey were not recorded, so their comparison to survey participants was not feasible. The Tel Aviv Sourasky Medical Center ethics committee approved this study and voided the need to obtain informed consent from the reported patients.
Race-related morbidity and mortality
Overall, 137,580 runners participated in all Tel Aviv races taking place from March 2007 to November 2013. Serious adverse events (resulting in hospitalization or death) occurred in 23 athletes (Central Illustration). Two athletes died as a result of participation in a race, for a sport-related mortality rate of nearly 1 per 69,000 (95% confidence interval: 0.4 to 5.3 per 100,000). Both fatalities were due to heat stroke.
Incidence of serious events of cardiac origin
There were no fatalities caused by a primary arrhythmia or by cardiac disease. Thus, the 95% confidence interval for the risk of cardiac death in the Tel Aviv races was 0 to 2.2 per 100,000 participants. There were 2 hospitalizations for cardiac events, including a single case of non-fatal myocardial infarction and a single case of supraventricular tachyarrhythmia.
The myocardial infarction occurred in a 38-year-old man participating in the full marathon of 2011. He collapsed on the 20th km mark with chest pain and dyspnea. Myocardial infarction was diagnosed and urgent cardiac catheterization revealed single-vessel coronary disease with a complete occlusion of the right coronary artery. Interestingly, this previously asymptomatic athlete had no known cardiovascular risk factors and had undergone pre-participation screening that included resting ECG and exercise stress tests repeatedly. One such exercise test was performed only 3 weeks prior to the race. The test was available for review: it was a maximal, symptom-limited exercise test and was strictly normal.
The case with supraventricular arrhythmia was a 38-year-old man who nearly fainted while running the 2012 Night Run. Hypotensive atrioventricular nodal reentry tachycardia was documented at the time of symptoms and terminated onsite with adenosine. The patient was hospitalized and eventually underwent radiofrequency ablation therapy.
Incidence of serious events of noncardiac origin
During the same time period, 21 cases of serious exertional heat stroke were identified, including 12 that were life threatening and 2 that were fatal.
The first fatality occurred during the 2011 Tel Aviv race. A 42-year-old man finished the 21.1-km-long half marathon race and collapsed near the finish line. He immediately received basic and advanced life support at the first-line emergency station. His body temperature was documented in the first-line emergency-station as 41°C (105.8°F). Emergency therapy included immediate and thorough cooling and mechanical ventilation. He was hospitalized alive but died of multiorgan failure 48 h later.
The second fatal event occurred during the Tel Aviv marathon of 2013. This race was scheduled for March 15, with races of 10 km, half marathon, and full marathon planned. However, in view of an official weather forecast predicting extremely high temperatures for the day of the race, the following changes were made: 1) the marathon race was cancelled; and 2) the start time for the 10 km and 21.1 km races was advanced to early morning (scheduled to start at 5:45 am instead of 6:30 am). Importantly, the mean daily temperature on the week preceding the race was 17.5°C (63.5°F) and the day before the race, recorded temperatures were 16°C at 5:00 am and 19°C (66.2°F) at 11:00 AM. However, on the actual day of the race, recorded temperatures were significantly higher than during the previous week, with 24°C (75.2°F) recorded at 5:00 am, 27°C (80.6°F) at 08:00 am, and 35°C (95°F) around the time when the last participant finished the race (11:00 am). On the 18 km mark of the half marathon, a 29-year-old highly trained male athlete had an unheralded cardiac arrest. Basic cardiopulmonary resuscitation was started, and paramedics and a doctor from the first-line emergency station continued advance life support. The first documented arrhythmia was asystole. All resuscitation maneuvers failed. The patient’s documented body temperature was >41°C (>105.8°F).
Twelve additional cases of near-fatal heat stroke requiring mechanical ventilation followed by hospitalization in intensive care units were documented over the years (Central Illustration). In the most recent race, the 2013 10 km Tel Aviv Night Run, we identified 1 case of heat stroke presenting with syncope and tonic seizures. This was a 27-year-old male, noncompetitive athlete who runs 10 km 3 times per week. Notably, he had mild diarrhea with low-grade fever on the day before the race. He ran the race faster than usual and did not feel anything wrong until he collapsed abruptly, shortly before the finish line. The rectal temperature recorded immediately in the ambulance was 40°C (104°F). He recuperated quickly in the emergency room and was hospitalized for 2 days.
We identified 42 cases of heat exhaustion requiring hospitalization but not in intensive care units. Of all cases with heat stroke or heat exhaustion, 15 patients had abnormal ECG findings at the time of hospitalization, including early repolarization in 10 patients, ST-segment elevation depression in 3 patients, and T-wave inversion in 2 patients. The overall occurrence of serious sports-related adverse events is presented in the Central Illustration. On average, for every serious cardiac event, there were 10 serious and more than 5 life-threatening/fatal events due to heat stroke.
Compliance with pre-participation guidelines
A total of 513 runners participating in the 2013 race agreed to participate in our survey (Table 1). Their mean age was 35 ± 12 years and 74% of them were men. Of these athletes, 56% ran the 10 km race, and 37% ran the 21.1 km race, (the 42.2 km marathon had been cancelled due to weather conditions). Only 35% and 46% of athletes reported having undergone ECG screening during the previous 1 and 5 years previously, respectively.
Sudden death of athletes is an important topic that has drawn the attention not only of clinicians and epidemiologists, but of the lay press as well. Somewhat surprisingly however, professional and lay publications on sudden athlete deaths occurring during sporting activity have focused primarily on arrhythmic events, whereas the mortality caused by heat stroke has received far less attention. This is evident not only from the number of medical publications on sports-related mortality, with papers related to arrhythmic death outnumbering those on heat stroke by a factor of 5 (see previous text), but also by the emphasis on pre-participation screening of athletes for the prevention of arrhythmic death (15–17). It is within this context that our study is important, showing that life-threatening events during endurance races taking place in warm climates are more likely to be caused by heat stroke than by cardiac arrhythmias.
Interpretation of our main findings
We collected data for 14 endurance races that took place in Tel Aviv during the last 7 years, compiling data on almost 140,000 runners. Our mortality risk estimates are accurate, because the number of athletes experiencing fatal or life-threatening events and the number of athletes participating in the races were known with fair accuracy, rather than estimated. The mortality rate related to endurance race participation observed in the present was 1:69,000, which is within the range reported in others (3,4,18). However, all fatal and life-threatening events in our study were caused by heat stroke rather than by cardiac arrhythmias. Importantly, 1 fatality in a male athlete resulting from cardiac arrest might have been misclassified as a primary rhythm disturbance had the first responders not actively measured his rectal temperature as part of their emergency assessment.
Importance of heat stroke
Several lines of evidence indicate that the hazards of heat stroke during sports are under-appreciated. First, the incidence of exertional heat stroke is as high as 1 to 2 cases per 1,000 participants in races held in hot and humid environments (19,20). Heat stroke also strikes in areas generally considered of mild climate. An example is the Great North Run, the world’s largest half marathon race, held annually in Newcastle, Great Britain. In 2009, 55 of 54,000 participants were diagnosed with exertional heat stroke (21) and in 2005, 4 athletes died with suspected heat stroke as the cause of death (22). Furthermore, in the 2007 Chicago marathon, there were 300 reported cases of heat-related injuries among 35,000 runners, including 1 fatality (23). Second, the risk of heat stroke is not limited to endurance races. According to a Centers for Disease Control and Prevention survey on sport-related injuries among high school athletes (24), heat stroke was a leading cause of death during the time period of 2005 to 2009. In a separate survey by the National Center for Catastrophic Injury Research, heat stroke was an important cause of death among high school and college football players (25), who train and compete wearing heavy protective equipment. Even experienced runners, who have completed several marathons uneventfully, are not immune (26).
Is heat stroke under-reported as cause of sports-related cardiac arrest
The largest series reporting on cardiac arrest during endurance sports is a retrospective analysis of >10 million participants in long distance races taking place in the United States during the last decade (3). In this large series, only 3% of fatal cardiac arrests were due to heat stroke. However, the fact that none of the non-fatal cardiac arrests were ascribed to this entity raises the possibility that heat stroke remained underdiagnosed in this retrospective study (9). The diagnosis of heat stroke depends on accurate measurement of body temperature. However, any temperature measurement other than rectal or by invasive techniques is likely to be spuriously low; this is true for skin, oral, and aural measurements (27). Yet, social-cultural conceptions and logistic issues may prevent the implementation of immediate rectal temperature assessment following collapse in a race, especially in urban areas. Unheralded collapse (9) with documented ventricular fibrillation (10) may be the mode of presentation of heat stroke. In this setting, the correct diagnosis will be missed if, as often happens (11), the rectal temperature is not measured promptly. In the largest analysis of adverse events during long races (3), a considerable percent of cardiac arrest victims had inconclusive diagnoses. Given the frequent failure to measure core body temperature, it is plausible that some of these events were erroneously attributed to cardiac conditions on the basis of incidental pathological findings, whereas heat stroke was the real etiology. For survivors of the event, the ECG abnormalities commonly caused by heat stroke (28) may lead the treating physician away from the correct diagnosis.
Recognizing that heat stroke is likely to be a more common cause of sport-related death than commonly appreciated has important implications. First, there are no clinical studies of potential strategies to prevent heat stroke during endurance sports. Conceptually, a number of interventions could be used to minimize risk. Because the likelihood of heat stroke is enhanced by lack of acclimatization, a period of 10 to 14 days should be allowed for proper adjustment to warm climate (29). Recognizing the key role of acclimatization is important for individual participants living in cooler areas, who should arrive at the location of the race earlier. Event planners also should acknowledge the need for acclimatization. Ironically, the customary practice of scheduling endurance races during the spring, rather than the summer to avoid the hottest weather, may actually increase the risk for heat stroke by reducing the time available for acclimatization. Second, pre-existing fever impairs human ability to dissipate the additional heat stress imposed by exercise. It is thus not surprising that heat stroke survivors often report a recent minor illness (30). Thus, candidates should be warned against participation in endurance sports if they are presently ill or recuperating from a recent febrile illness. Third, experienced runners, as well as onsite witnesses and health care providers, may be totally unaware of a developing heat stroke. Unfortunately, delays in diagnosis will inevitably postpone the initiation of cooling therapy. A potential solution to this problem may be the use of ingestible thermistors that can reliably record body core temperature during physical activity (31). Technological refinements allowing for cheaper telemetry devices could eventually prove to be useful in monitoring large numbers of runners. Finally, there is an ongoing debate concerning the role of ECG pre-participation screening for the prevention of sudden death among athletes (32,33), and our findings place that debate in a different perspective.
It could be argued that heat strokes outnumbered arrhythmic events in our study only because pre-participation screening of athletes with resting ECG and exercise stress testing eliminated the risk of arrhythmic events. However, most race participants were not members of sports organizations and were not legally obliged to undergo any pre-participation screening. In fact, the only screening most of these runners underwent was a declaration of “good health” during registration. Specifically, only one-third of race participants answering our survey reported undergoing ECG screening during the year preceding the race. Moreover, we have evidence indicating that ECG screening has had no impact on athletes’ mortality in Israel (34).
In this study involving almost 140,000 athletes participating in endurance sports, fatal or life-threatening events during endurance races were caused exclusively by heat stroke. Serious cardiac events were extremely rare and outnumbered by heat stroke events by a factor of 10.
COMPETENCY IN MEDICAL KNOWLEDGE: The optimum strategy for detecting cardiovascular disease and preventing sudden death in recreational runners is controversial.
COMPETENCY IN PATIENT CARE: Prompt diagnosis of heat stroke and rapid implementation of cooling can avoid catastrophic injury and adverse cardiovascular outcomes in patients who collapse while running.
TRANSLATIONAL OUTLOOK: Additional studies are needed to validate technologies for continuous cardiovascular monitoring to prevent heat stroke and other causes of cardiovascular collapse in runners.
The authors thank Alex Pine, PhD, for his advice with statistics.
All authors have reported that they have no relationships relevant to the contents of this paper to disclose.
- Abbreviations and Acronyms
- Received January 11, 2014.
- Revision received April 13, 2014.
- Accepted May 12, 2014.
- American College of Cardiology Foundation
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