Discussion
Albeit the probability of death during a triathlon is low, when occurring in a highly publicised event it inevitably raises a great deal of public concern about the sport's safety. This impelled the largest North American triathlon organisation to initiate an inquiry into triathlon deaths.22 ,23 Unfortunately, good data are difficult to obtain and hence specific screening or aftercare recommendations could not be made. The current investigation was performed to test the hypothesis that, when compared with triathletes and the general population, individuals who died swimming during a triathlon or in training have a higher prevalence of cardiac anomalies that predispose to IPO.
IPO and its causes
Water immersion causes blood redistribution from the periphery to the heart and pulmonary vessels, causing an increase in central blood volume and pulmonary vascular pressures.24 This can be extreme and precipitate pulmonary oedema in IPO-susceptible individuals, even in those without any obvious comorbidities.25 The effect is augmented—especially during exercise—in cold versus warm water.26 Those triathletes susceptible to IPO are therefore believed to have abnormal myocardial diastolic compliance (lusitropy)—or stiff hearts. Abnormal LV diastolic compliance is partly responsible for elevated LV end-diastolic pressure during exercise in patients suffering from heart failure with preserved ejection fraction (HFpEF).27 IPO seems to be a form of HFpEF precipitated by increased preload due to immersion with heavy exertion. In the initial publication of IPO, a number of individuals exhibited a hypertensive response to cold exposure; thus, it is plausible that they had LVH.12 In a recent review of published cases, nearly 50% of published civilian IPO cases had identifiable predisposing factors, and most were cardiac.15 The association of IPO susceptibility with LVH and risk factors for LVH12–15 strongly implicates abnormal LV diastolic compliance.
Since most sudden deaths occur during the swim portion of the triathlon, it is certainly plausible that IPO is a cause. IPO tends to occur in susceptible individuals most frequently in cold water, and often during heavy exertion.12 ,28–30 Typical IPO symptoms—cough productive of pink frothy or blood-tinged secretions occurring during a swim—have been reported by 1.4% of triathletes,31 and in 1.8–60% during 2.4–3.6 km open sea swimming trials in young, fit naval recruits.29 ,32
The prevalence of LVH in the general population is estimated to be 12–21%.33 ,34 In well-trained triathletes, LV dimensions are usually within the normal range for the general population.19 ,35 ,36 In a group of 235 triathletes (168 men, 67 women) participating in the Hawaii Ironman Triathlon from 1985 to 1995, the overall prevalence of LVH by echocardiography was 24% (LV mass >294 g in men, >198 g in women).19 Chronic, high-intensity exercise can also lead to LVH (athlete's heart); this was the most likely cause of the enlarged LV in most cases in the quoted series. Diastolic filling properties in athlete's heart under dry, resting conditions are normal;37 ,38 thus, it is unlikely that athlete's heart is a precipitating cause of IPO. LV thickness in athlete's heart very rarely exceeds 13 mm.39 ,40 In contrast, in the current series, a pathological cause of enlarged hearts was more prevalent, including extreme values of septal thickness and estimated LV mass (figure 1), significantly beyond the range expected from hypertrophy due to athlete's heart.36 ,39 ,41 Thus, diastolic filling properties were more likely to be abnormal. All autopsied cases in this series had pulmonary oedema, which is usually the end result from any attempt at cardiopulmonary resuscitation and water aspiration during terminal event. Thus, the existence of pulmonary oedema at autopsy provides little insight.
Possible causes of death in triathlons
In some cases, cardiac anatomy at autopsy after a triathlon may occasionally provide clues to the cause of death.1 Of nine athletes autopsied after a triathlon-related death, only two had cardiac anomalies that could be construed as being a primary cause of death: one with Wolff-Parkinson-White syndrome, the other with a congenital coronary artery anomaly. On the other hand, six had LVH.1
IPO is a plausible cause of triathlon death, particularly since it has been suggested as one possible mechanism in the pathophysiology of drowning.4 In contrast, due to the rarity of IPO-related deaths and lack of known history of IPO in any triathlon death, some have concluded that it is an unlikely cause of death in triathletes.10 ,22 ,23 Nevertheless, several IPO-related deaths have been reported in other settings.42–47 Fatal cases of IPO may be rare but probably under-recognised; unless an episode is witnessed and survival is sufficiently long enough to obtain adequate clinical information to make the diagnosis, attribution of an in-water death to IPO is exceedingly difficult.48
It is impossible to exclude primary arrhythmia as the cause of death in these individuals. Indeed, it has been proposed that cardiomegaly is an independent risk factor for cardiac arrhythmia.35 ,49–51 However, in a series of cardiac arrests during long-distance runs (where diagnostic facilities are more likely to be available and thus early detection of an arrhythmia more likely), primary arrhythmia was the purported cause in only a minority of instances. Non-ischaemic ventricular tachycardia was observed in only 7%, with ‘presumed arrhythmia’ the attributed cause in an additional 7%.3 One individual in our series had a history of atrial fibrillation and was taking an antiarrhythmic. It is not possible to know whether his propensity towards atrial arrhythmias contributed to his death; however, any rhythm other than sinus rhythm is likely to cause a rise in pulmonary artery and capillary pressures in the face of increased preload as occurs during immersion. In fact, atrial fibrillation has been proposed as a predisposing condition for IPO.52 In another case in the present series, prolonged QTc was noted after resuscitation. Swimming can be a trigger for arrhythmias in long QTc syndrome;53 however, prolonged QTc could also be secondary to antiarrhythmic drug administration after cardiopulmonary resuscitation or the cardiac injury itself. Information about genetic predisposition was unavailable. On the other hand, additional information from bystanders and others suggests that at least some of the deaths in the current series were not sudden and had features consistent with IPO (eg, cases 2, 10, 23 in the online supplementary material).
It might also be argued that demand ischaemia might be more likely during swimming, even in those with minimal coronary narrowing, because of the central redistribution of blood and higher LV volume. For a given level of exercise, this might lead to greater myocardial wall tension and myocardial oxygen consumption compared to dry land. However, in patients with known CAD, a study of swimming in cold water versus cycling demonstrated that ST segment depression occurred at similar levels of exercise during both activities.54
The distribution of cardiac pathologies in this series is in marked contrast with other similar studies: in younger cohorts of sudden death cases, myocarditis, hypertrophic cardiomyopathy (HCM) and coronary artery abnormalities are more common.55 In case series with age distribution similar to the current series, atherosclerotic disease predominates.56 ,57 Of those in our cohort in whom coronary arteries were mentioned in the medical examiner's report, only four individuals had ≥70% coronary narrowing; six individuals had ≥50% narrowing. One additional person who did not have an autopsy but had coronary artery stents was presumed to have ≥50% narrowing. Whereas HCM is a common cause of sudden cardiac death in most series of land-based athletic events, no mention of it was made in any of the medical examiner reports in this series. While it can be difficult to distinguish HCM from undifferentiated LVH at autopsy,58 the apparent lack of HCM in this series is consistent with the physiology of swimming: blood redistribution during immersion dilates the LV and thus reduces the likelihood of LV outflow obstruction even when present.
Limitations
There are several limitations to our study showing that markers of IPO susceptibility are common among victims of sudden death during triathlons. It cannot be definitively concluded that the cause of death in individuals with LVH was IPO. IPO has been considered by some to be an unlikely cause of triathlon death due to lack of prior history among victims. However, instances of IPO are most likely under-reported. Most triathletes train for the swim portion in pools, which are generally warmer than open bodies of water where events are held, and during a pool swim mild IPO symptoms can be relieved at an early stage by exiting the water. Primary arrhythmias cannot be excluded; indeed, it has been suggested that arrhythmias are more common among individuals with LVH.34
Among those classified as having no obvious cause of death, one (woman aged 38 years, see online supplementary case 3) had histologic evidence for acute myocarditis. Two others (man aged 57 years, see online supplementary case 6 and man aged 48 years, see online supplementary case 18) had 50–60% coronary stenosis. Although this degree of stenosis is not conventionally considered to be critical, the true degree of narrowing could have been underestimated at autopsy. Another (man aged 46 years, see online supplementary case 10) had no CAD but did have areas of myocardial fibrosis and chronic inflammation suggesting remote infarction. Finally, one case (man aged 43 years, see online supplementary case 12) had scattered intramural adipose and focal loose interstitial fibrous tissue. Although not identified as such by the examining pathologist, this could be consistent with arrhythmogenic right ventricular dysplasia. We cannot exclude the possibility that these individuals might have died of an arrhythmia.
While there could be inconsistencies in attempting to compare LVH using echocardiography with heart mass determined at autopsy (table 6), we feel that gross errors are unlikely as echo has been validated against postmortem measurements.59
Among 775 sports-related sudden death cases during moderate-to-vigorous exertion among men and women, fewer deaths occur during swimming than cycling or jogging.60 This could be a consequence, in individuals at risk for athletic sudden death, of fewer person-hours spent swimming. However, in triathlons, a specific swimming-related mechanism for death would be expected to predominate where swimming is the first of three events.
Nevertheless, observations demonstrating that IPO is relatively common in competitive swimming such as military training and triathlons—and has been the cause of deaths42–47—implicate this condition as a likely cause of at least some deaths in triathlons. It would have been ideal to compare autopsies of triathletes dying during the bicycle or run portions; however, this was not possible due to fewer of those deaths, with a significant proportion due to motor vehicle trauma. Interestingly, scuba diving is another precipitating activity for IPO; indeed, LVH has been observed in a high percentage of scuba diving deaths.61
Conclusion
In a series of sudden deaths occurring during triathlon training or events, we found evidence on postmortem examination of a prevalence of IPO susceptibility markers (LVH) in excess of the prevalence expected among healthy triathletes. We suspect that IPO may be a significant cause of death in triathletes. Analogous to the management of HFpEF, the goal should be to seek and eliminate pertinent risk factors such as hypertension, obesity and obstructive sleep apnoea.62 Educational programmes to promulgate information about risk factors could raise awareness and reduce the risk in this population.
