Sudden death in triathlon: Prevalence and mechanisms
Martin Bonnevie-Svendsen
Prosjektoppgave ved profesjonsstudiet i medisin UNIVERSITETET I OSLO
09.02.2018
© Martin Bonnevie-Svendsen 2018
Sudden death in triathlon: Prevalence and mechanisms Martin Bonnevie-Svendsen
http://www.duo.uio.no/
Trykk: Reprosentralen, Universitetet i Oslo
Sudden Death in Triathlon: Prevalence and Mechanisms
Introduction
Triathlon is a competitive endurance sport that involves swimming, cycling and running. The standard triathlon race consists of a 1500 meter swim, 40 kilometer cycling and a 10
kilometer run. However, the distance of triathlon competitions varies depending on the race, ranging from 400 meter, 10 kilometer and 2.5 kilometer (swim, bike and run, respectively) for a super sprint up to 3.8 kilometer, 180 kilometer and 42 kilometer (swim, bike and run,
respectively) for an Ironman distance. (1) The physical and mental challenges involved in triathlon has made the sport popular with athletes gravitating towards extreme sporting events. In recent years, triathlon has received increased attention and become a mainstream sport for recreational athletes. (2)
Over the last decade there have been numerous media reports of deaths among competitors during triathlon races. (3, 4) The sudden death of athletes is particularly difficult to accept, as these are often young and healthy individuals without prior medical history of significance.
(4) In Norway, this was last experienced during the National Triathlon Championship in 2015, where a 58-year-old competitor came in distress during the swim segment of the race.
Although he was rescued ashore within a minute of the event, resuscitation attempts were unsuccessful. (5) Reported events of sudden deaths have raised concerns regarding the safety of participation in triathlon events. (6)
The prevalence of sudden death in triathlon has been estimated to 1.5 in 100 000 participants.
(4) This is approximately two to three times higher than what is reported from marathon running. (7, 8) This begs the question why there seems to be a higher risk involved with triathlon than other extreme endurance sports. Answering this question necessitates reviewing proposed mechanisms of sudden death in triathlon. These have already received quite some attention in the literature.
Hypothermia is recognized as a medical risk factor associated with open water swimming. (9, 10) The definition of hypothermia varies between references, encompassing a decrease in core temperature to less than 35.0-36.0°. (9) Such levels of drop in body temperature is associated with increased risk of cardiac arrhythmia, hyperventilation with aspiration and hypoglycemia. (11-13) These conditions would pose a severe risk of drowning if they occurred in a swimming athlete. The physiological phenomenon of afterdrop is commonly referred to as the continued cooling of core temperature after removal from cold exposure. (9, 14) Afterdrop is reported to take place in cold water swimmers for up to 33 minutes after exit from the water. (9) This mechanism could be of particular interest to triathlon-related
fatalities seeing how triathletes might continue to work at high intensities, not uncommonly in extreme weather conditions, for hours after exiting the water.
Another proposed cause of deaths in triathlon is related to cardiac pathology. There are several proposed mechanisms as to how cardiac abnormalities could trigger a fatal event
during a triathlon race. Submersion has been demonstrated to result in bradycardia and arrhythmias. (15) What is more, triathletes have been shown to have different cardiac morphology and higher incidence of ventricular premature beats at the end of maximal exercise tests than controls. (16) Finally, forensic data obtained from deceased athletes suggest this group demonstrate a higher occurrence of cardiac abnormalities when compared to the general triathlete population. (17)
Several questions remain to be answered pertaining to the potential involvement of cardiac pathology in triathlon deaths. Are such events caused by pre-existing and undetected cardiac pathology which clinical debut happens to coincide with the event of a triathlon race? Or might the nature of triathlon races increase the risk of triggering pre-existing cardiac pathology?
There are numerous reports of documented cases of pulmonary edema in triathletes. (18-20) Swimming induced pulmonary edema (SIPE) is thought to result from an overfilling of the pulmonary vascular system due to the increased central blood pressure and volume while swimming. (21) SIPE will lead to a slowing of the alveolar gas exchange in the affected parts of the lungs, and subsequent dyspnoea. Continuing swimming with shortness of breath can ultimately lead to swimming failure and potentially drowning. A recent review has suggested SIPE might be a cause of death during the swimming phase of triathlon races. (17)
Several authors have raised the question if the environment in which triathlon races are organized poses a risk in itself. (22-24) Triathlon mass starts can be notoriously chaotic, as explained by one triathlete: “Nothing can prepare a newbie for the start. It can be like jumping into a washing machine. You will get swum over, kicked, hit and banged into.” (25)
Numerous mechanisms for how these conditions could trigger a fatal event have been proposed. Authors have argued that a simple blow to the head rendering an athlete
unconscious could lead to drowning. (22) The arrhythmogenic effect of water may result in ventricular beats due to increased sympathetic and parasympathetic activity. (22, 26) Such co- activation of both divisions of the nervous system is coined autonomic conflict (AC). Tipton suggests that emotional responses such as anxiety, anger or overcompetetiveness during a competition might contribute to AC. (24)
In a publication of 2016, Asplund et al reviewed potential mechanisms involved in
swimming-related deaths. (27) However, this review included data from triathlon and open- water swimming events alike. Although both sports involve swimming, they can differ substantially in distances and nature. Furthermore, recent publications containing data of substantial gravity to the matter has been published since the review of Asplund et al. (17, 28) This warrants a re-visit of the topic with specific emphasis on triathlon-related deaths. Thus, the aim of this paper is to systematically review reported sudden deaths and
pathophysiological mechanisms of sudden death in triathletes.
Methods
This literature review adhered to the guidelines outlined in the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement. (29)
Eligibility criteria
This literature review was limited to studies with level 4 evidence or higher according to the Oxford Centre for Evidence-Based Medicine published in peer-reviewed journals. (30) Commentaries and expert opinions were excluded from this review. Language was restricted to English, German, Norwegian, Swedish and Danish.
Eligible studies had to report on sudden deaths or pathology of relevance to hypothesized mechanisms of sudden death in triathlon races or during triathlon-specific training. Studies not involving triathletes or related to the sports of swimming, running and cycling were excluded.
Search strategy
A comprehensive search of the literature was conducted. This included electronic searches of the MEDLINE and EMBASE databases from 1946 and 1946, respectively, to January 12th 2018. In addition, the Cochrane Library was searched from its infancy (1993) to January 12th 2018 to identify any relevant Cochrane Reviews. Keywords used in the literature search were
“triathlon”, “ironman”, “swimming”, “open water swimming”, “competitive swimming”
AND “death”, “drowning”, “pulmonary edema”, “hyperthermia”, “hypothermia”, “sudden death”, “cardiac arrhythmia” and “sudden cardiac death”. Alternative spellings, synonyms, variations and truncations of keywords were included. Furthermore, bibliographies in the included studies were hand searched to identify potentially eligible studies not captured by the electronic searches. An example of a full electronic search for the database EMBASE is available in Appendix 1.
Study selection
Citation from the electronic searches were collected and compiled in a single list. Duplicate records were discarded. All titles and abstracts were screened for eligibility by a single reviewer. Obviously irrelevant studies were removed. Full text versions of all potentially relevant studies were retrieved and evaluated for inclusion by a single reviewer.
Data extraction process
Data from eligible studies was extracted and included in a spreadsheet. Data extracted for this literature review included the following: (i) study design; (ii) study population (e.g. age, gender, sport, and sample size); (iii) activity performed during event; (iv) outcome measure;
and (v) main findings.
Data analysis
Owing to the heterogenous nature of the included studies (i.e. varying study designs, outcome measures and quality) a meta-analysis was deemed not feasible. Therefore, in this review only a qualitative analysis of the included studies was undertaken.
Assessment of methodological quality
Due to several different study designs being included in this review, the NHLBI Study Quality Assessment Tools were chosen for assessment of methodological quality of eligible studies. (31) These tools comprise of sub-sets specific to individual types of study designs and
consists of 9-14 questions evaluating potential methodological flaws and risks of bias in the assessed studies. Each question is answered “yes”, “no” or “cannot determine/not reported/not applicable”. The percentage of items answered “yes” was calculated from the total number of questions. If a question was considered “not applicable” this was discarded from the total number of questions. In accordance with existing practice with similar assessment tools, cut off percentage values were set arbitrary to < 50% (poor), 50-80% (fair) and > 80% (good).
(32) A single reviewer assessed the methodological quality of each study included in this review.
Results
The initial search returned 4129 hits. A further 16 items were identified via additional hand searches. After removal of duplicate records 2180 titles and abstracts were screened for eligibility. 2114 irrelevant items were discarded. A total of 66 articles were evaluated for inclusion in this review. 38 did not meet the inclusion criteria and were excluded from this review. Figure 1 contains a flow diagram of the study selection process.
The included studies comprised one randomized controlled trial, one cross-sectional study, two case-control studies, ten cohort studies, four case series and ten case reports.
Prevalence of sudden death
Two of the included studies reported on the prevalence of sudden deaths in triathlon (Table 1).
Harris et al reported on the incidence of sudden deaths among participants in triathlons sanctioned by USA Triathlon (USAT) from January 2006 through September 2008. (4) They also reviewed available autopsy reports. A total of 959 214 participants, of which 59% were men, were analyzed. 14 deaths were identified (rate, 1.5 per 100 000 participants; 95% CI, 0.9-2.5). 13 deaths occurred during swimming (11 men, and 2 women) and one during biking.
The mean age of victims was 44 ± 10 years (range, 28 to 65 years). Triathlons with fatal events had greater participation (n = 1319; 95% CI, 1084-1584) than races without deaths (n
= 318; 95% CI, 302-334).
In a more recent publication, Harris et al identified sudden deaths and cardiac arrests during triathlons in the United States in the period 1985 to 2016. (28) They also calculated the incidence of deaths and cardiac arrests in USAT-sanctioned races from 2006 to 2016 and reviewed autopsy reports. A total of 135 race-related sudden deaths (n = 107), resuscitated cardiac arrests (n = 13), and trauma deaths (n = 15) were identified. 90 (67%) events occurred during swimming, 22 (16%) during biking, fifteen (11%) while running and eight (6%) took place after race completion. Of the 22 bike-related deaths, 15 were result of blunt trauma by collision, of which ten involved motor vehicles. Sudden death and cardiac arrests were most frequent during short-distance triathlons, with an occurrence of 66 (49%), 33 (24%) and 23 (17%) in short-, intermediate- and long-distance triathlons, respectively. Average air temperature during events was 21.9 °C ± 13.1 °C (range, 6.7 °C to 28.9 °C). Water
temperatures were available for 41 swimming-related fatalities, with an average of 22.1 °C ± 13.2 °C (range, 10.6 °C to 31.7 °C). 23 victims were known to be wearing wetsuits.
Study Design Population Involved activity
Outcome Main findings Quality
& LOE
Comments Harris
2010
Cohort study
Deaths among participants completing USAT triathlons from 2006-2008 (n=14 of 959 214 participants)
Short, intermediate and long (Ironman) triathlons events.
Incidence and risk factors of race-related sudden deaths in triathlon events.
14 deaths in 959 214 participants (1.5 per 100 000). 13 swimming deaths.
Cardiovascular abnormalities identified in 7 of 9 autopsies.
Q: Fair LOE: 3
Retrospective design.
Brief methods and results description. Possibility that same athlete is counted more than once due to multiple race entries. Non-sanctioned events not included.
Harris 2017
Cohort study
Deaths and cardiac arrests among participants completing USAT triathlons from 1985-2016 (n=135 of 4 776 443)
Short, intermediate and long triathlon events.
Incidence and risk factors of race-related sudden deaths and cardiac arrests in triathlon events.
135 deaths and cardiac arrests in 4 776 443 participants (1.74 per 100 000). 90 swim, 22 bike, 15 run and 8 post-race events.
Cardiovascular abnormalities identified in 27 (44%) of 61 autopsies.
Q:Good LOE: 3
Prospective and
retrospective design. Non- finishers not included.
Incidence rate calculated for period 2006-2016 only. Possibility that same athlete is counted more than once due to multiple race entries. Non- sanctioned events not included.
Table 1
Between 2006 and 2016, the incidence of sudden deaths in USAT-sanctioned races was 1.47 per 100 000 participants. There was no statistical difference in incidence between short, intermediate and long races (1.61, 1.41, and 1.92 respectively). The mean age of the involved athletes was 50 ± 11 years. Of the 135 victims, 115 (85%) were men and 20 (15%) were women. The rate of death and cardiac arrests was greater in men aged 40 and above compared to men under 40 (8.25 and 2.49 per 100 000, respectively). The risk of death increased with increasing age. For athletes aged 40 years and older, 50 years and older, 60 years and older, incidence rates per 100 000 were 6.1, 9.6 and 18.6, respectively.
A further case series by Moon et al identified 58 triathlon-related deaths in the USA and Canada from October 2008 to November 2015. (17) No calculation of incidence rates was provided. Of the 58 deaths, 48 events occurred during competition and ten during training. 42 (72.4%) events happened during swimming, 11 (19.0%) during cycling and five (8.6%) during running. The age distribution across the 42 swimming deaths spanned younger than 40 years (n = 4, 9.5%), 40-49 years (n = 16, 38.1%), 50-59 years (n = 13, 31.0%) and 60 and older (n = 9, 21.4%). These involved 36 males (85.7%) and 6 females (14.3%).
Cardiac abnormalities
Harris et al reviewed autopsy reports from sudden deaths in USAT-sanctioned triathlons with regards to cardiac abnormalities in 2010 and 2017. (4, 28) In addition, a further six of the included studies reported on mechanisms of cardiac abnormalities related to hypothesized causes of triathlon deaths and near fatal cardiac events in triathletes (Table 2).
From the fourteen sudden deaths identified by Harris et al from 2006 to 2008, nine autopsy reports were obtained (4). Downing was declared the cause of death in all swimming deaths.
Seven out of nine athletes had cardiovascular abnormalities identified post-mortem. Six athletes had mild left ventricular hypertrophy, including one with a clinical history of Wolff- Parkinson-White syndrome. One athlete had a congenital coronary artery anomaly.
Harris et al also obtained 61 autopsy reports from 122 cases of sudden deaths identified from the period between 1985 and 2016. (28) Cardiovascular abnormalities were identified in 27 cases (44%). These consisted of 18 cases with significant atherosclerotic coronary artery disease (18 male), three with evidence of hypertrophic cardiomyopathy and two cases with mitral valve prolapse. One of the latter had a history of Wolff-Parkinson-White syndrome. In addition, single cases of ascending aortic dissection with rupture, spontaneous renal artery dissection, arrhythmogenic right ventricular cardiomyopathy and congenital coronary anomaly were identified.
Moon et al retrieved 23 autopsy reports from 58 triathlon deaths identified in the USA and Canada between 2008 and 2015. (17) Five athletes had significant coronary artery disease (≥70% narrowing), one athlete each had renal artery dissection, acute dissection of the descending aorta, atrial fibrillation, acute myocarditis and prolonged QTc interval following ventricular fibrillation. After excluding the athletes with obvious possible causes of death, six of the remaining 16 athletes had excessive heart mass. The proportion of athletes with
thickened left ventricle was significantly increased (p < 0.001) compared with the general triathlete population.
The general population who served as control in the above study was that of Douglas et al.
(33) They examined cardiac morphology and function in 135 exceptionally well-trained
Ironman participants between 1985 and 1995. Approximately 25% of the athletes displayed evidence of left ventricular hypertrophy. However, marked increases in cardiac dimensions were rare. Concentric and eccentric remodeling was present in four (2%) and 15 (7%) athletes, respectively.
In a study comparing triathletes with healthy controls, Claessens et al found that triathletes displayed a higher occurrence of ventricular premature beats at exhaustion. (16) They also found evidence of concentric and eccentric left ventricular hypertrophy in the triathlete cohort. There was no clear association between performance level or training volume and left ventricular hypertrophy or functional cardiac changes.
Warburton et al measured the occurrence of late potentials (LP) in healthy triathletes before and after completion of a half-Ironman triathlon. (34) While no LPs were observed pre-race, two out of nine athletes displayed pre-race SAECG anomalies associated with LPs. 2-3 hours post-race, LPs were observed in the same two athletes. These remained after 24-48 hours of
Study Design Population Involved activity
Outcome Main findings Quality &
LOE
Comments Douglas
1997
Cohort study
Very well- trained triathletes (n=235), 160 ♂, 67♀, age 39 yrs ± 1 (range 18- 74)
Ironman- triathlon
Cardiac morphology and fuction
Marked increases in left ventricular mass were common. LVH in approx. 25% of athletes. Most athletes had cardiac
morphology and function within normal limits.
Q: Fair LOE: 3
Prospective design. No control group. No statistics presented on subject fitness level or training history.
Claessens
1999 Case
control Triathletes (n=52), ♂, and healthy controls (n=22)
Stationary bicycle maximal exercise test
Ventricular premature beats (VPB) at end of maximal exercise test, cardiac structure and function
Statistically significant increase of (VPB), ventricular hypertrophy and altered diastolic left ventricular function in triathletes.
Q: Fair
LOE: 4 Non-randomised case control design. VPBs only recorded during last 2 minutes of maximal effort test.
Warburton
2000 Cohort
study Triathletes (n=9), ♂,
Half-ironman
triathlon Prevalence of late potentials (LP) pre- and post-race
2 out of 9 athletes displayed SAECG anomalies associated with LPs pre- competition that worsened post-race.
Q: Good
LOE: 3 Prospective design with individual cross-over. Small sample size. Excluded subjects with heart disease or family history of sudden cardiac death.
Pearce 2007 Case
report Triathlete (n=1), ♂, age 44 yrs
Ironman
triathlon Pulmonary function testing, ECG, blood samples,
echocardiogram
In-race confusion, nausea, hemoptysis.
Post-race ECG changes consistent with pericarditis.
Q: Good
LOE: 4 Retrospective, single case report. Limited data reported from clinical investigations.
Leischik 2014
Cohort study
Half- Ironman and Ironman finishing triathletes (n=87)
Outside of competition testing
Cardiac function (eccocardiography) and cardio- pulmonary performance (spiroergometry)
Concentric cardiac remodeling in 43 (49.4%) and
concentric hypertrophy in 27 (31.0%) of 87 athletes.
Q: Fair LOE: 3
Prospective design. No follow up. No control group.
Alexander 2016
Case report
Triathlete (n=1), ♂
Training run Vital signs, eccocardiogram, ECG, blood samples, cardiac MRI, coronary angiography
Chest pain, coronary artery vasospasm and ventricular fibrillation.
Successfully resuscitated.
Q: Good LOE: 4
Thoroug description of clinical course. Remote patient history of cocaine use and recent marijuana and energy drink use.
Table 2
recovery in one athlete. A moderate correlation was observed between left ventricular mass and prolonged filtered QRS (r = 0.67, P < 0.05).
Following eccocardiography of 87 Ironman and half-Ironman finishers, Leischik and Spelsberg observed left ventricular concentric remodeling and concentric hypertrophy in 26 and 21 males, respectively. (35) 17 female athletes displayed left ventricular concentric remodeling and six females had concentric hypertrophy. No evidence of right ventricular dysfunction was observed. Triathletes with left ventricular hypertrophy displayed
significantly higher bike training volume (p = 0.034) and systolic blood pressure during exercise (p = 0.037). No signs of right or left ventricular dysfunction were observed.
Pearce reported a case of suspected acute pericarditis in an Ironman participant who dropped out of the race with confusion, dyspnea, nausea, shivering and hemoptysis during the bike segment. (36) A case of coronary vasospasm and ventricular fibrillation is described by Alexander et al. (37) The involved athlete presented with a history of multiple recent episodes of chest tightness and dyspnea during training runs. Neither of the above cases resulted in deaths.
Pulmonary edema
13 of the included studies reported cases or examined mechanisms of pulmonary edema in triathletes (Table 3).
Caillaud et al investigated the occurrence of pulmonary edema in triathlon finishers (n = 8) by measuring pulmonary diffusing capacity for CO and performing thorax CT scans. (38) Their results demonstrated evidence of mild subclinical pulmonary edema in triathletes post-race.
In a survey of 1400 USA Triathlon members, Miller et al evaluated the prevalence of symptoms compatible with swimming-induced pulmonary edema (SIPE) and identified risk factors for this condition. (39) They found a prevalence of symptoms compatible with SIPE of 1.4% (95% CI, 0.9-2.2%). Statistically significan risk factors for SIPE after multiple logistic regression were hypertension (OR, 5.38), female gender (OR, 2.75), long course event (OR, 3.30) and a history of fish oil use (OR, 2.66). Wearing a wetsuit was a statistically significant univariate risk factor (OR 2.73), but dropped out of the model after an adjusted analysis.
Pingitore et al investigated signs of pulmonary edema by pulmonary water content in 31 Ironman finishers. (40) They identified a significant increase in pulmonary water content immediately post-race (p < 0.01). Ultrasound lung comet-tail (ULC) artifacts, as a sign of extravascular lung water, was present in 68% of athletes post-race, and mostly resolved within the first 12 hours.
After identifying 58 triathlon-related deaths, Moon et al screened 23 available autopsy reports for signs of left ventricle hypertrophy, a proposed marker for SIPE susceptibility. (17) They found a significant increase in occurrence of left ventricle hypertrophy in the deceased athletes when compared with healthy triathletes.
Ma and Dutch reported five consecutive cases of suspected exercise-induced pulmonary edema (EIPE) during an Ironman triathlon with a total of 1594 competitors. (20) At this event, a total of 147 athletes were assessed by the onsite medical team.
Study Design Population Involved
activity Outcome Main findings Quality
& LOE Comments Caillaud
1995
Controlled observational cohort study
Triathletes (n
= 8, ♂) age 20- 28 yrs and sedentary controls (n = 4)
Triathlon race
Spirometry, pulmonary diffusing capacity (DLCO) and mean lung density (MLD) pre and post triathlon race.
Mild subclinical pulmonary edema suggested by significantly reduced DLCO and increased MLD post race
Q: Fair LOE: 3
Prospective controlled design. Double-blinding protocol. Very small population. No monitoring of exercise intensity.
Biswas
2004 Case report Triathlete (n=1), 36 yrs
♂
Swim
training Blood samples, ECG, chest radiograph, echocardiogram, 24-h cardiac monitoring w.
treadmill test
Increased troponin I levels and clinical diagnosis of SIPE.
Q: Good
LOE: 4 Retrospective report.
Training-case only.
Boggie- Alarco 2006
Case report Triathlete (n=1), 36 yrs
♂
Triathlon race swim
Signs and
symptoms of SIPE, vital signs, blood samples, ECG, chest CT and x-ray, bronchoscopy
Stridor, cough, hemoptysis, SpO2 90%, lung infiltrates.
Diagnoses with SIPE.
Q: Good LOE: 4
Retrospective report.
Thoroughly reported examination findings.
Deady 2006
Case report Triathlete (n=1), ♀, 38 yrs
Swim training, cold water (15°C)
Vital signs, blood samples, d-Dimer, troponin I, ECG chest radiograph, echocardiogram
Dyspnoea, wheeze, tachypnea. Clinical diagnosis of SIPE.
Q: Fair LOE: 4
Retrospective report. Cold- water swimming. Training- case only.
Miller
2010 Cross
sectional / case control
USAT members (triathletes) (n=1400), aged 20 yrs and above.
Swim Association between risk factors and symptoms of swimming-induced pulmonary edema (SIPE)
Symptoms of SIPE identified in 1.4%
of pupulation.
Associated symptoms: history of hypertension, fish oil use, long course triathlons and female gender.
Q: Poor
LOE: 4 Poor. Retrospective survey study. Self-reported symptoms. Second phase case-control again retrospective. Non- validated pulmonary edema questionnaire.
Carter 2011
Case series Triathletes (n=3), ♀, age 43-58 yrs
Training swim and half- Ironman race swim
Vital signs, chest radiograph, ECG, stress ECG
Dyspnoea, cough, haemoptysis, fatigue. Clinical diagnosis of SIPE.
Q: Fair LOE: 4
Retrospective design. Non- consecutive events.
Pingitore 2011
Observational cohort study
Healthy triathletes (n=31), 29 ♂, 2 ♀, mean age 41 yrs
Ironman triathlon
Arterial pressure, echocardiography, chest
ultrasonography, pulmonary function, blood samples
Ultrasound lung comet-tail artifacts and increased plasma level anti- inflammatory mediators post race.
Q: Good LOE: 3
Thoroughly reported prospective cohort study.
Ma 2013 Case series Triathletes (n=5), ♂, age 37-57 yrs
Triathlon race
Vital signs, chest x- ray, blood samples, ECG, CT
angiogram, Doppler ultrasound
Exercise induced pulmonary edema in 5 of 147 assessed competitors.
Q: Fair LOE: 4
Retrospective series of consecutive cases during a single triathlon race.
Casey 2014
Case series Triathletes (n=2), age 60 and 55 yrs, 1
♂, 1 ♀
Triathlon race swim and training swim
Vital signs, ECG, chest X-ray, blood samples,
echocardiogram, coronary CT-scan
Dyspnoea, probable diagnoses of SIPE.
Q: Fair LOE: 4
Retrospective series of non- consecutive events.
Yamanashi
2015 Case report Triathlete (n=1), 38 yrs
♂
Long- distance triathlon swim
Symptoms and signs of SIPE, vital signs, chest CT, blood samples
Dyspnea, SpO2 82%, ground-glass appearance CT scan. Diagnosed with SIPE/EIPE
Q: Fair
LOE: 4 Retrospective report.
Limited reporting on athlete background and test results.
A further three case series and five case reports included in the review reported on a total of 14 cases of SIPE. (18, 19, 41-46) Ten events occurred during the swim stage in a race setting while four events happened during swim training. One of the above cases was described as
“near-drowning”. No sudden deaths were reported among these cases.
Hyperthermia
Two of the included studies investigated hyperthermia in triathletes (Table 4).
Kerr et al examined the effect of mild heat stress induced by wearing a wet suit while swimming in warm water (25.4 ± 0.1 °C) on five male triathletes. (47) They found a significant difference in skin temperature throughout a simulated triathlon when comparing wet suit to swim suit use. However, no difference in core temperature was observed between groups.
Core temperature and its association with markers of hydration status was examined in ten male triathletes at an Ironman triathlon by Laursen et al. (48) On a race day with ambient conditions of 23.3 °C (range 19-26 °C) and ocean temperature of 19.5 °C, the mean core temperature of athletes was 38.1 °C (± 0.3 °C). No association was found between body mass loss and core temperature or the development of hyperthermia.
Of 107 deaths during USAT-sanctioned triathlons between 1985 and 2016, the cause of death was attributed to heat stroke in two cases. (28)
Beale
2016 Case series Triathletes (n=4), ♂, age 25-50 yrs
Ironman and half- Ironman races
Chest X-ray, blood samples, ECG, CT angiogram, stress echocardiogram, cardiac MRI, V/Q scan, CT pulmonary angiogram
Dyspnoea, haemoptysis, clinical diagnosis of EIPO.
Q: Fair
LOE: 4 Retrospective series of non- consecutive events.
Moon 2016
Case control Triathletes (n=23), mean age 49.5 yrs, range 33-68
Triathlon training and triathlon races
Autopsy reports for cardiac pathology, heart mass, ventricular wall thickness, coronary artery disease
Increased prevalence of IPO susceptibility markers (LVH) in autopsied triathletes compared to healthy triathletes.
Q: Fair LOE: 4
Retrospective case series.
Controls again retrospectively selected from a different population.
Smith
2017 Case report Triathlete (n=1), ♀, age 55 yrs
Sprint triathlon swim
Signs and
symptoms of SIPE, vital signs, blood sample, ECG, chest x-ray, CT
angiogram, eccocardiogram
Cough, dyspnea, SpO2 93%, type I repiratory failure, CT-diagnosed pulmonary edema
Q: Good
LOE: 4 Retrospective case series.
Well described prior medical history.
Table 3
Hyponatremia
Five of the included studies reported on or investigated the occurrence of hyponatremia in triathletes (Table 5).
Rüst et al identified asymptomatic exercise-associated hyponatremia (EAH) in eight (26%) of 31 finishers in a Triple Iron ultra-triathlon. (49) The prevalence of EAH in Triple Iron ultra- triathlon finishers was higher compared to reports on Ironman finishers.
In the period between 2005 and 2013, Danz et al examined 1089 participants in the Ironman European Championship for hyponatremia. (50) They observed post-race hyponatremia in 115 (10.6%) finishers. Mean plasma sodium levels were 140.5 (±4.2) mmol per liter (range, 111 to 152). Of the 115 cases, 95 (8.7%) were categorized as mild hyponatremia, 17 cases (1.6%) were deemed severe and three cases (0.3%) were considered critical. There was a significant association between hyponatremia and female gender or longer race time.
This review included a further three case reports reporting death and near fatal events involving hyponatremia.
Hohmann-Jeddi reports a case of a 30-year-old male triathlete collapsing after finishing an Ironman race. (51) The cause of death was attributed to cerebral edema secondary to hyponatremia.
A case of near-fatal hyponatremia was reported by Richter et al. (52) This involved a 45-year- old female athlete who developed seizures after completing her first Ironman triathlon. She was found to have critical hyponatremia (111 mmol/L), pulmonary- and cerebral edema. The athlete was successfully treated in hospital and completed her next Ironman with normal post- race sodium levels one year later.
A second case of near-fatal hyponatremia was reported by Severac et al. (53) The 42-year-old female athlete in question presented to the emergency department with headache, nausea, confusion and a reduced Glasgow Coma Scale score after completing an Ironman race in hot
Study Design Population Involved activity
Outcome Main findings Quality &
LOE
Comments Kerr 1998 Randomized
controlled trial
Triathletes (n=5), ♂
Simulated triathlon in laboratory setting. Water temperature 25.4
°C
Core and skin temperature changes during bike and run following swimming with either wetsuit or swimsuit
Significant differences in skin temperature during swim, but no significant changes in core temperature throughout trial.
Q: Fair LOE: 3 *
Very small sample size.
Prospective cross-over design. Subjects served as their own controls.
Laursen 2006
Observational cohort study
Triathletes (n=10), ♂, mean age 34.7 yrs
Ironman triathlon event
Core temperature during Ironman event and association with markers of hydration status.
Core body temperature averaged about 1°C above normal. No link found between body mass loss and core temperature.
Q: Fair LOE: 3
Prospective design.
Small sample size.
Hydration status only assessed after event.
Some loss of data points during events (55 of a possible 72 valid data points obtained).
Table 4
and dry conditions. She was found to have severe acute hyponatremia (123 mmol/L) and quickly developed seizures, cerebral edema and intracranial hypertension. She was successfully treated in hospital and was able to return to work six months later.
Methodological quality and level of evidence
The general methodological quality of the included studies was fair (n = 15) to good (n = 10).
Three studies were deemed of poor methodological quality. There was an overweight of retrospective studies, with only 11 of the 28 included articles applying a prospective study design.
Ten articles represented level 3 evidence, whereas 17 articles were deemed level 4 evidence.
One trial was categorized as level 3 evidence, despite using a randomized controlled design.
This decision was based on lacking description of several important assessment criteria and a very small sample size. (47)
Study Design Population Involved activity
Outcome Main findings Quality
& LOE
Comments Richter
2007
Case report Triathlete (n=1), ♀, age 45 yrs
Ironman triathlon
Blood samples, chest radiograph, ECG,
echocardiography, head CT scan
Post-race severe hyponatremia, pulmonary- and cerebral edema.
Q:Good LOE: 4
Single case. Thorough description of subject, symptoms,
investigations, intervention and outcome.
Rüst 2012 Observational cohort study
Triathletes (n=45), ♂, mean age 42.1 yrs
Triple Ironman triathlon
Prevalence of hyponatremia, anthropometric measurements
Post-race asymptomatic hyponatremia in 8 of 31 finishers (26%).
Higher prevalence compared to reported prevalence in Ironman races.
Q:Good LOE: 3
Thoroughly reported prospective cohort study. Lacking measurements from non-finishers, no fluid or NSAIDs control.
Leplatois 2014
Case report Triathlete (n=1), ♀, age 42 yrs
Ironman triathlon, hot and dry conditions
Cerebral CT scan, blood samples, transcranial Doppler ultrasonography.
Post-race confusion, seizures, cerebral edema, intracranial hypertension and severe acute hyponatremia. Near fatal event with successful recovery.
Q: Fair LOE: 4
Single case, retrospective report from emergency department. Scarce description of subject characteristics and precipitating event.
Hohmann-
Jeddi 2015 Case report Triathlete (n=1), ♂, 30 yrs
Ironman
triathlon Fatal event Post-race collapse,
leading to death. Q: Poor
LOE: 4 Lacking description of subject, course of events, interventions and time course.
Danz 2016 Observational
cohort study Triathletes (n=1089), 932 ♂, 157
♀
Ironman European Championship
Prevalence of
hyponatremia Among 1089 finishers, 115 (10.6%) had post- race hyponatremia.
Significant association was observed between hyponatremia and female gender or longer race time.
Q: Poor
LOE: 3 Prospective design, scarce population description, lacking reporting on outcomes and statistical analyses.
Table 5
Methodological quality and level of evidence appears to be evenly distributed between the included studies with regards to year of publication (range 1995 to 2017). Common
methodological weaknesses included no use of control groups, small sample sizes, missing sample size justification, no description of drop-out rates and lack of adjustment for
confounding variables.
Of note, only three studies reported on sudden deaths in triathletes in sizeable cohorts. (4, 17, 28) It is likely that these studies reported on several of the same events, as their inclusion criteria and timeframes contained some overlap. The recent publication by Harris et al stood out in applying good methodological quality, a partly prospective design and a large cohort (n
= 4 776 443). One study only applied a cross-sectional design to investigate potential risk factors for a hypothesized mechanism of sudden deaths in triathlon (SIPE). (39) This study applied a retrospective design and only met five of 12 relevant quality assessment criteria.
Discussion
Epidemiological data identified in this review suggest a prevalence of sudden death in triathlon of approximately 1.47 per 100 000 participants. This is approximately two to three times higher than what is being reported in other extreme endurance sports, such as marathon.
(7, 8) Accounting for the fact that Harris et al suggest a probable underreporting of triathlon deaths in the early period of their observed cohort, it appears sudden deaths are more prevalent at triathlon events compared to other extreme endurance races.
The vast majority of triathlon deaths occur during swimming. (4, 17, 28) Several possible explanations for this can be discussed. Cardiac abnormalities, such as coronary artery narrowing and left ventricle hypertrophy (LVH) is not an uncommon finding in autopsy reports from triathlon deaths. Indeed, the frequency of LVH is reported to be greater in deceased triathletes compared to the general triathlete population. (17) Moon et al also demonstrated an increased prevalence of pathological causes of cardiac hypertrophy in the same cohort. They argue that such conditions, beyond the physiological changes expected from hypertrophy due to “athlete’s heart”, would increase the chances of abnormal diastolic filling properties in affected athletes. The authors propose that abnormal diastolic filling might increase susceptibility to immersion pulmonary oedema by increasing pulmonary vascular pressure (IPO). (17)
Cardiomegaly has been proposed as an independent risk factor for cardiac arrhythmias. (54, 55) A different proposed risk factor for cardiac arrhythmias is ventricular premature beats (VPB). (16) Although VPBs are usually considered benign, the physiological nature of this entity is challenged by Claessens et al. They demonstrated an increased risk of VPBs during maximal effort in triathletes compared with healthy controls. Claessens argue that VPBs in association with structural and functional heart adaptations seen in triathletes, might increase the risk of ventricular arrhythmias in this population.
A third hypothesized mechanism of cardiac arrhythmias involves impaired left ventricular systolic function as a result of fatigue from prolonged, strenuous exercise. (56, 57)
Furthermore, athletes with ventricular arrhythmias are reported to display late potentials (LP), which was not seen in healthy athletes without arrhythmias. (58) Warburton et al suggest that the presence of LPs might be useful in identifying problems related to cardiac fatigue in athletes. (34) They identified presence of LPs in two of nine triathletes following completion
of a half-Ironman triathlon. However, they were not able to conclude whether these athletes carried increased risk of ventricular arrhythmias or sudden cardiac death.
Significant coronary artery disease (CAD) has been reported in approximately 25-30% of autopsy reports reviewed following triathlon-related sudden deaths. (17, 28) Of note, Harris et al highlights that of the 18 athletes with CAD in their cohort, all were men. (28) Furthermore, in the same study the risk of sudden death and cardiac arrest increased incrementally with age for each decade from the age of under 30 to 60 years and above. Although this trend occurred for both sexes, incidence within the before-mentioned age groups were approximately 2 to 18 times higher in the male compared to the female population. This is no surprise, given the fact that the incidence of coronary artery disease in the United States is approximately twice as high in men as in women. (59) While this does not explain the entire discrepancy between male and female deaths in the cohort of Harris et al, it should be mentioned that the number of deaths and cardiac arrests in female athletes was very low. As such, an additional few cases would have altered this relationship considerably.
Somewhat surprisingly, Harris et al found no statistically significant difference in incidence of sudden deaths or cardiac arrests between short, intermediate and long triathlon events. (28) One might expect that inexperienced swimmers would be at greater risk of death by
drowning. Harris et al reported that, of the deceased athletes whose race experience was known, 26 (38%) partook in their first triathlon. (28) Interestingly, in their earliest report on deaths in USAT-sanctioned races, Harris et al found that triathlons with deaths included more participants than races without deaths. (4) One could propose that a crowded swim leg might further increase the risk for inexperienced swimmers. Unfortunately, this distinction was not reported on in their more recent study of a larger cohort. While it is difficult to exclude level of experience as a relevant factor in swim-related triathlon deaths at this stage, the current review has revealed no convincing evidence of such an association.
An additional number of hypothesized mechanisms for swimming related deaths have been proposed. Hypothermia is recognized as a medical risk factor associated with open water swimming. (9, 10) Harris et al has reported water temperatures during triathlon events as low as 10.6 °C. (28) The phenomenon of afterdrop involves continued temperature decrease after exiting the water. Afterdrop has been documented to occur in the majority of open-water swimmers after exiting water temperatures of 11.7 °C. (9) What is more, afterdrop has also been associated with exercise after immersion in water. (60) It is also proposed that vigorous exercise after immersion could potentially worsen afterdrop. (9) This suggest that triathletes could potentially be at risk of hypothermia both during and following the swim leg.
Submersion is known to induce two opposing nervous autonomic responses, the cold shock response, and the diving response. (61-63) This simultaneous activation of conflicting limbs of the nervous system has been coined autonomic conflict (AC). Shattock and Tipton propose that such autonomic conflict might induce cardiac arrhythmias in predisposed individuals.
(63) If such a mechanism is indeed involved in triathlon deaths one could speculate whether the race setting itself contributes to such conflict. Triathlon starts are notorious for being crowded events with frequent body contact between athletes in the fight for positions during the swim. Interestingly, anger is an emotion associated with ventricular fibrillation and co- activation of the two branches of the autonomic nervous system. (64, 65) In light of the increased frequency of sudden deaths in triathlon events with large number of competitors, it is tempting to speculate if the combination of cold water and the stressful environment of the triathlon start would negatively influence autonomic nervous system activity. In regards to
potential risks of racing in cold water temperatures, it is difficult to extrapolate results from open-water swimming to triathlons, because these events can differ vastly in duration and nature. The effect of cold water temperatures on triathletes has yet to be investigated in the triathlon population.
Reflex laryngospasm from liquid penetration into the naso- and oropharyngeal airways has been proposed as a possible mechanism for cases of drowning without significant aspiration of liquid. Such a causative mechanism is however controversial, and the issue of “dry- drowning” has been reappraised and questioned in more recent literature. (66) One could, however, speculate whether racing in extreme water temperatures could possibly initiate laryngospasm and contribute to the process of drowning.
Although the mechanisms of sudden deaths during the swim leg of triathlons are yet to be understood, it is apparent that cardiac arrests carry a greater mortality when they occur in water. Harris et al reports a ratio of cardiac arrest survival to sudden death of 11% in their cohort of triathletes. (28) This is less than that reported for marathons (29%) and can probably be attributed to the proximity of rescuers in marathons and the inherent difficulties of water rescues. (67-70) In order to minimize the risk of swim-related sudden deaths in triathlon events, race organizers should prepare equipment and trained personnel to allow for quick water rescue and resuscitation. This would include boats of sufficient size to initiate
resuscitation and to facilitate quick transport to shore as well as having on-site defibrillators.
Furthermore, distressed athletes are not always able to signal for help. (4) Having athletes wear brightly colored swim caps could help personnel identify swimmers in need of rescue.
With regards to sudden deaths during the cycling leg of triathlons, these are less common than swim deaths. Yet, a substantial number of cycling-related deaths in triathlons are due to trauma involving motor vehicles. (28) Race organizers should strongly consider the risk of allowing motor vehicles on course and take steps to minimize the exposure of athletes to motorized traffic.
When compared to swimming, the number of sudden deaths and cardiac arrests during bike, run and post-finish combined is lower. Yet, among the 13 survivors of cardiac arrests reported by Harris et al, a total of eight events occurred during bike, run and immediately after finish.
(28) This highlights the need for having defibrillators and personnel trained in resuscitation available throughout the entire race course.
The current review has identified cases of sudden deaths due to heat stroke, rhabdomyolysis and hyponatremia. In addition, pulmonary edema in triathletes is frequently reported in the literature. This review has not revealed any cases of sudden death where pulmonary edema has been assigned the cause of death. However, this would be a difficult connection to
establish post-mortem, seeing how cardiopulmonary resuscitation in terminal events involving water aspiration usually results in pulmonary edema. (71) Although pulmonary edema is most often self-limiting once exertion is aborted, one cannot rule out the possibility of increased mortality when the condition occurs while swimming. (72) Hyponatremia appears to be a not uncommon finding in Ironman finishers, in particular in athletes with longer race time. (50) Although hydration regimes during races have yet to be described, this could be interpreted as athletes having a tendency to overhydrate. While the subclinical presentation of hyponatremia is most frequent, severe cases might ultimately result in sudden death. Athletes, first aid- and medical personnel attending triathlons events should be aware of the frequency and risks of pulmonary edema and hyponatremia. Inexpensive equipment such as pulse oxiometers and
stethoscopes can greatly aid the diagnosis of pulmonary edema. Furthermore, medical race crews should be trained at recognizing and managing the above conditions.
Whether or not endurance athletes, including triathletes, should undertake pre-race cardiac screening has been a topic of discussion for some time. (71, 73) While the current review presents evidence that might implicate cardiac pathology in sudden deaths in triathlon, these results should be interpreted with caution. It is not yet possible to ascertain the mechanisms underlying these deaths, in particular with respect to swim-related events. There is limited prospective reporting on incidence and risk factors of sudden death in triathletes. While numerous hypothesized mechanisms of sudden death have been proposed, these have yet to be validated in prospective trials involving triathletes. To the best knowledge of this author, there are no registries specific to sudden deaths in triathlon. Establishing such registries, along with protocols for reporting on sudden deaths and near-fatal events could greatly facilitate the work of revealing potential risks factors in the triathlete population. Ultimately, this could aid the process of learning if and when athlete screening should be recommended, and help preventing future cases of sudden death.
Conclusion
Sudden death is a rare event in triathlons that occur with an estimated frequency of 1.47-1.49 per 100 000 race entries. The majority of fatalities occur during the swim segment. Evidence suggests there is a higher frequency of cardiac anomalies among victims of sudden death in triathlon compared to the general triathlon population. This might suggest cardiac implication, possibly by placing predisposed athletes at risk of arrhythmias. However, there is insufficient evidence to draw certain conclusions as to whether swimming-related triathlon deaths are caused by pre-existing cardiac pathophysiology, environmental factors of the triathlon swim or by other potential mechanisms. Deaths occurring during the bike segments are far less common, but frequently involve collisions with motor vehicles. Pulmonary edema is not uncommon in triathletes and is usually self-limiting condition. Hyponatremia is also not uncommon in long-distance events. There is a paucity of high-quality, prospective studies on potential risk factors of sudden death in triathlon. Future research efforts to identify potential risks related to cardiovascular pathology, cardiac arrhythmias, cold-water swimming and hypothermia is recommended. Race organizers could decrease the risk of sudden deaths by making defibrillators and trained medical personnel available along the course. Furthermore, safety boats should be of design to allow resuscitation to be started on site, or at the very least allow rapid transport of athletes to shore. Establishing registries and protocols for compulsory reporting of sudden deaths and near-fatal events by event organizers could facilitate the process of identifying potential risk factors associated with triathlon racing.
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