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1Word count: 5699 SUDDEN DEATH AND EXERCISE 1 T D NOAKES, MB ChB, MD, FACSM LIBERTY LIFE CHAIR OF EXERCISE AND SPORT SCIENCE AND MRC/UCT BIOENERGETICS OF EXERCISE RESEARCH UNIT DEPARTMENT OF PHYSIOLOGY UNIVERSITY OF CAPE TOWN MEDICAL SCHOOL OBSERVATORY, 7925 SOUTH AFRICASudden death in athletes will always be an emotive topic for it suggests thatathleticism may not only not prevent the development of heart disease, but mayactually increase the likelihood that the athlete will die suddenly during exercise.The evidence at present is the following:• Persons who die suddenly during exercise have advanced heart disease of which they are frequently unaware. The commonest forms of heart disease associated with sudden death during exercise are coronary artery disease and hypertrophic cardiomyopathy. Less common cardiac conditions linked to sudden death in athletes include anomalous origin of the coronary arteries, aortic rupture associated with Marfans syndrome, myocarditis, mitral valve prolapse and various arrhythmias.• The incidence of these predisposing diseases in the athletic population is extremely low, possibly of the order of 1 per 10,000 to 1 per 200,000 athletes. Furthermore detection of some of these conditions in asymptomatic athletes may be difficult, if not impossible.1Based on an article previously published in abbreviated form inContinuing Medical Education 9(8): 958-969, 1991.
2• Regular exercise reduces the overall risk of sudden death in persons with latent coronary artery disease, yet acutely increases the risk of sudden death during exercise in that subset of persons with heart disease, who are predisposed specifically to sudden death.• In practical terms, only athletes with symptoms or clinical signs of, or risk factors for coronary or other forms of heart disease should undergo routine maximal exercise testing when they commence an exercise training program. However, once symptoms suggestive of cardiac disease are present in athletes, detailed cardiological testing is absolutely mandatory. Lack of habitual physical activity is now considered to be the fourth majorcoronary risk factor. Yet it is clearly apparent that, on occasion, trained andapparently healthy athletes die suddenly during exercise. Possibly the most recent graphic example of this tragedy was that of the57 year old American who collapsed and died within 1 minutes after setting aRegional Masters athletic record of 10 min 30.2 sec for 3000m run indoors. Thepatient had not previously reported cardiac symptoms and a maximal exercisetest performed 22 months before his death did not reveal any cardiacabnormalities. How is it possible to reconcile the apparently irreconcilable; that habitualphysical activity may protect from heart disease, yet exercise per se may be animportant risk factor for sudden death? It is a problem with which medicine hasgrappled since antiquity.Historical Background
3 The Greek physicians Hippocrates and Galen were among the first toexpress an opinion on the risk of exercise on the heart. Hippocrates attackedathleticism in his treatise on Nutrient writing that "...the condition of the athlete isnot natural. A healthy state is superior to all." Six centuries later Galen wrotethat `Athletes live a life quite contrary to the precepts of hygiene, and I regardtheir mode of living as a regime far more favorable to illness than tohealth....While athletes are exercising their professions, their body remains in adangerous condition but, when they give up their professions, they fall into acondition more parlous still; as a fact, some die shortly afterwards; others live forsome little time but do not arrive at old age. The first modern sport to attract a similar concern was rowing. In 1845,the seventh Oxford and Cambridge Boat Race was the first to be rowed on thecurrent course on the Thames between Putney and Mortlake. No sooner had itmoved to its longer course through the British capital than an irate letter writtenby one Frederick C. Skey, past president and Fellow of the Royal College ofSurgeons, appeared in the Times of London, charging that `the University BoatRace as at present established is a national folly. Skey claimed that rowing wasbringing young men to an early grave. A scientific study published shortly thereafter by John Morgan, aBirmingham physician, proved that Skey was in error. Morgan showed that thelife expectancy of university oarsmen was not reduced. If anything, it wasslightly longer than that of the average Englishman of the period. Almost a century later, in 1968, this issue was revived by a letter whichappeared in the Journal of the American Medical Association stating that allmembers of the 1948 Harvard rowing crew had since died `of various cardiac
4disease; an assertion that was enthusiastically denied by these oarsmen whoreported that they were all `alive and well. Surprisingly, cycling was the next sport to attract similar attention. Itseems that in the 1890s North Americans suddenly discovered the bicycle andmedicine had another sport about which to express its alarm. Prospectivecyclists were warned that prolonged bending over the handlebars could cause`kyphosis bicyclistarum or in lay terms `cyclists stoop or `cyclists figure or even`cyclists spine. Then, as expected, there was `cyclists heart. The working life of theheart was limited to only a certain number of heart beats, these physiciansasserted, and the faster heart rate during cycling would only waste theseprecious beats and so lead to premature heart failure. One of the first references to the dangers of running on the heart wasmade in 1909 by five eminent British physicians who started a correspondencein the Times of London by stating that `school and cross-country racesexceeding one mile in distance were wholly unsuitable for boys under the age ofnineteen, as the continued strain involved is apt to cause permanent injury to theheart and other organs. Again this view was easily refuted. From an analysis of 16,000schoolboys covering a period of twenty years, Lempriere could find only twocases of sudden death during exercise that were not due to accidents. Heconcluded that `heart strain through exercise is practically unknown, aconclusion echoed by Sir Adolphe Abraham who denounced the concept of thestrained athletic heart. Running again became a medical cause célébre in the 1970s as thepopularity of the sport mushroomed. One of the first articles to question the
5safety of such activity reported that half of fifty-nine sudden deaths occurredduring or immediately after severe or moderate physical activity, especiallyjogging. The authors questioned `whether it is worth risking an instantaneouscoronary death by indulging in an activity, the possible benefit of which.....has yetto be proved. They also considered `the possible lethal peril of violent exerciseto (heart) disease patients. More fuel was added to this controversy in the early 1980s by the suddendeath while running of James Fixx, the celebrated American runner and author.Fixx had achieved international celebrity status as author of the book thatbecame an international best-seller because it best captured the mood of therunning explosion that occurred in the late-1970s. Paradoxically, in a later book, Fixx had written an appropriate epitaphboth to himself and to the concept that runners could earn immunity from bothheart disease and death: "...runners are much like ordinary mortals. They can,sad to say, get sick. They can even die."Pathology Of Sudden Death The first component of this issue that needs attention is whether thesedeaths during exercise actually prove that exercise is the real culprit andtherefore a dangerous activity; or, stated differently, whether exercise andsudden death are causally related. The overriding conclusion from a large number of studies of sudden deathincluding sudden deaths that occur during exercise, has shown that virtually allpersons who die suddenly during exercise have a serious disease, usually of theheart, that adequately explains the cause of death.
6 While a large number of cardiac conditions have been associated withsudden death during exercise, the most common cause, by far, in Westernizedcommunities, is coronary artery disease. Thus coronary artery disease is thecause of death in the majority of such cases that occur in persons aged 40 orolder. Sportsmen below the age of 40 who die suddenly during exercise aremore likely to have hypertrophic cardiomyopathy. However, some youngathletes who die suddenly during exercise are likely to have severe coronaryartery disease as a result of familial hypercholesterolemia. Other less common causes of sudden death during exercise includecongenital anomalies of the coronary arteries, myocarditis and ill-definedconduction disturbances presumed to be related to pathological changes foundin the conduction pathways at autopsy (Table 1). But the more important point is that none of these conditions is caused byexercise, however vigorous. Rather, the evidence is clear that regular exerciseacts against the development especially of coronary atherosclerosis. There isalso no evidence that exercise accelerates the progression of these otherpotentially-lethal cardiac conditions. At present the exact mechanism causing exercise-related sudden death inpersons with established disease, especially of the coronary arteries is notknown. Whereas plaque rupture or thrombosis are present in up to 95% ofsudden cardiac deaths in the general population, the incidence would seem tobe lower in exercise-related deaths suggesting that exercise-induced ischemiaor coronary spasm may be involved.Does Exercise Increase Or Reduce The Risk Of Sudden Death?
7 Because athletes who die suddenly have advanced cardiac disease, theyare at high risk of dying suddenly, whether or not they exercise. A number ofstudies have attempted to determine whether or not exercise increases the riskthat persons with advanced heart disease will die suddenly during exerciserather than at rest. Some have found that moderate exercise does not increasethe risk of sudden death whereas other have found that more vigorous forms ofexercise such as cross-country skiing or running are associated with a five toseven fold greater risk of sudden death. Possibly the first detailed study of this question was reported byThompson and his colleagues. They found that in the state of Rhode Islandbetween 1975 and 1980, twelve men died while jogging, eleven from heartattacks. Five of these men were known to have heart disease before theirdeaths. They calculated that the incidence of death during jogging was onedeath per 396 000 man hours jogging which is about seven times the estimatedheart attack rate during more sedentary activities. Thus in that study theunequivocal evidence was that jogging increased the risk that the jogger withsevere heart disease would die while exercising. But this finding should not be used to overestimate the risk of exercise.For example, in the Rhode Island study, there was one death per 7 620 joggersper year - clearly an infinitesimal risk for each individual jogger. Furthermore, itwould be totally impractical to screen all 7 620 joggers in Rhode Island in anattempt to identify the one jogger at risk of sudden death each year. Forexample, on the basis of these data, it has been calculated that a middle-agedjogger with no known cardiac disease who decides to continue running for one
8more year is at considerably lower risk of sudden death than is a middle-agednon-runner who continues to ride in his car during that year. Similarly, it has been estimated that approximately 200,000 childrenwould need to be screened to identify the one likely to die suddenly duringexercise. Even then, that individual would have to be singled out from 1999others with similar cardiovascular findings but who would not die suddenly duringexercise. The next important question that needs to be answered is, if exercisedoes indeed increase the risk of sudden death, by how much did exerciseactually shorten the life expectancy of the patient who was in any case at highrisk of dying suddenly and unexpectedly? Indirect evidence that the exerciseprobably does not greatly decrease life expectancy under such circumstances,comes from a study of the 1978 Rhode Island blizzard. In February 1978 a severe blizzard struck Rhode Island causing the dailydeath rate from heart attack to increase from the usual February average of 27deaths.day-1, to 48 deaths.day-1. This rate remained high for three of the firstfive days after the storm, but subsequently decreased below the normal dailyaverage, so that the total heart attack deaths for February that year was thesame as for previous years. Thompson has concluded that: These resultssuggest that the added physical and emotional stress arising from the stormeliminated those who would have succumbed to ischemic heart disease (heartattack) in the near future. In the same way, jogging deaths may occur in thosewhose time is up and who were due to die within the next few day or weeks evenif they avoided all forms of exercise, including walking. The data of Siscovick and his colleagues clearly show that persons whohave undetected heart disease and who are therefore at risk of sudden death,
9reduce their overall risk of sudden death if they exercise regularly. Duringexercise, however, their risk is increased acutely. For their studies, Siscovick and his colleagues collected detailedinformation on all persons dying suddenly during a one year period in Seattle,Washington. They then excluded from their analysis all those persons who wereill, who had been off-work or who had experienced any symptoms before theirsudden deaths. They were left with a total of 145 sudden deaths in a group ofpersons who were for all intents and purposes, absolutely healthy right up to themoment that they suddenly died. Analysis of these data showed that thosepersons who exercised vigorously on a regular basis had an overall risk ofsudden death, approximately two-thirds lower than that of the non-exercisers. Interestingly, the risk that the smaller number of sudden deaths in theexercising group would occur while these persons were exercising wasincreased acutely for the duration of the exercise bout, above the overall risk ofthe non-exercisers. Thus although the total group of exercisers had a reducedrisk of sudden death, that subset of exercisers with advanced heart diseaseresistant to all preventive measures including exercise, and who would ultimatelydie suddenly, were more likely to die while they were exercising rather thanwhen they were at rest. This finding explains why the sudden death of athletes usually occursduring exercise and why such events must not be construed to indicate thatexercise is dangerous and should therefore be avoided. In fact, if the exerciserswere to stop exercising, their risk of sudden death would according to thesedata, increase about threefold. To put this in perspective, let us consider the following. Our studies showthat in the population of about 10,000 Comrades Marathon runners there are
10approximately 3 sudden deaths per year, most of which occur as predicted bythe data of Siscovick and his colleagues, during or shortly after exercise. If, onthe basis of these three deaths per year, it was decided that marathon runningwas too dangerous and was summarily and effectively banned, the annual risk ofsudden death in the group of ultra-marathon runners would approximately triple. Thus each year after the banning of marathon running, there would benine not three sudden deaths; clearly an undesirable result. But by encouragingthe cohort of 10,000 marathon runners to continue running, something like sixlives per year are being saved. In summary, the studies of Siscovick and his colleagues therefore confirmthe finding that the risk of sudden death is reduced in persons who exerciseregularly and suggest that this is almost certainly not due to the presence ofconfounding variables. However, these studies also show that there is anincreased likelihood that those persons who have heart disease in spite of theirregular exercise, will die during the short period that they spend exercising.Were such persons to avoid all exercise however, their overall risk of suddendeath would be increased, not decreased. Interestingly, the degree of benefit isactually greatest, the higher the level of coronary risk; persons who are at lowrisk of dying suddenly from coronary heart disease benefit less from vigorousphysical exercise than do those who are at high risk either because of a familyhistory of heart disease, or because they are smokers who have other riskfactors already described. As Siscovick and his colleagues have stated: `Efforts to discourageclinically healthy persons at risk of primary cardiac arrest from continuing toengage in vigorous exercise may be inappropriate.
11High Levels Of Physical Fitness Are Possible In Persons With Advanced HeartDisease It is important to stress that severe heart disease may be present even inperson who are extremely physically fit. For example, we have reported casesof marathon runners who completed the 90 km Comrades Marathon only weeksbefore their subsequent deaths from severe advanced coronary artery disease insome cases with associated hypertrophic cardiomyopathy. One 42 year oldrunner completed a 42,2 km standard marathon in 03:06:00 just three weeksbefore autopsy showed he had complete occlusion of one major coronary arteryand 75% narrowing, with atherosclerosis, of the other two. In addition, there wasevidence of hypertrophic cardiomyopathy. The case of the American runner whodied within a minute of setting a regional running record in the United States hasalready been described. Therefore, it is quite wrong to assume that because someone is fitenough to complete marathon races and even ultra-marathon races in quiterespectable times, that he cannot have very serious heart disease.The Presence Of Warning Symptoms Persons who die suddenly during exercise frequently have warningsymptoms of heart disease which they ignored, choosing to continue exercisingrather than to seek medical advice. Thus in our study of heart attacks andsudden deaths in marathon runners, we found that fully 81% of these cases hadwarning symptoms. Six athletes completed marathon races, and three theComrades Marathon, despite symptoms of chest or abdominal pain sufficientlysevere to force them to stop running and to walk and run intermittently. Despite
12severe chest pain, one athlete continued to run a 16 km race and collapsed atthe finish. Another runner continued training for three weeks, including a 64 kmtraining run with chest pain severe enough to force him to walk on numerousoccasions.
13 Lessons From James Fixxs Death Many of these points were rather tragically illustrated by James Fixxsdeath while running. Fixx was at high risk of heart disease because his fatherhad died from a heart attack at a relatively very young age (43 years). Inaddition, Fixx was a reformed smoker with a markedly elevated blood cholesterolconcentration. Fixx had also experienced warning symptoms which he chose toignore and had refused the option of undergoing a maximal exercise stress test. Autopsy showed that Fixx had severe coronary artery disease with neartotal occlusion by atherosclerosis of one and 80% occlusion of another coronaryartery. There was also evidence of a recent heart attack. In addition, the heartwas somewhat large suggesting the possibility of concurrent hypertrophiccardiomyopathy. On the day James Fixx died, 1 000 other Americans would also have diedof heart attacks. Unlike Fixxs death, few if any would have received nationwidecoverage. Yet the vast majority of those deaths would have occurred in personswho were sedentary, or were smokers, or with uncontrolled high blood pressureand elevated blood cholesterol concentrations. If only those sudden deathsoccurring in athletes are reported in the press, it is understandable why thepublic acquire a distorted impression of the relationship between exercise andheart disease. Thus James Fixxs death followed a familiar pattern and helps emphasizethe points already made. One interesting possibility not considered by many, isthat regular exercise actually allowed James Fixx to outlive his father by nineyears. This possibility would be supported by the scientific findings especially ofSiscovick and his colleagues.
14Mechanisms Whereby Exercise May Protect Against Coronary Heart DiseaseAnd Sudden Death At least in animals, exercise has been shown to reduce the rate ofdevelopment of coronary atherosclerosis in monkeys fed a high-fat atherogenicdiet and to increase the resistance of the trained heart to the lethal abnormalheart rhythm, ventricular fibrillation the common mechanism that causes personswith heart disease to die suddenly. Another potentially important mechanism forthis effect is simply the reduction of the coronary risk factors. For example, inone survey 81% of mean and 75% of women who were smokers, stoppedsmoking when they started running. Similarly, subjects taking up marathonrunning show important changes in coronary risk factors.Screening To Prevent Sudden Death During Exercise When approached by a patient who wishes either to commence exerciseor to establish that it is safe for him or her to continue exercising at their presentlevel, the clinicians first responsibility is to rule out the presence of the acute orchronic diseases associated with sudden death. The clinical problem is twofold;first, the incidence of such diseases in the exercising population is extremely lowwith estimated incidences varying from 1 per 10,000 active exercisers to 1 per200,000 in children and young adults. Second, it is extremely difficult to detectsome of these latent forms of heart disease. The analogy of searching for aneedle in a haystack is not inappropriate. Third, is the finding that most acutecoronary events occur due to rapid progression of disease at sites at which acritical lesion was not previously present. Furthermore, even when latentdisease is detected, it is not always possible to differentiate absolutely those with
15the disease who will die suddenly during exercise, from those with the samecondition who are not at risk. For it is clear that there are many people with latent heart disease,especially coronary heart disease, who are able to exercise quite safely withoutthe risk of sudden death. How these are to be distinguished on clinical groundsfrom those at risk of sudden death during exercise has yet to be established. Accordingly a more pragmatic approach would seem justified. Thefollowing guidelines probably represent the current consensus: All persons over 50 should undergo cardiovascular screening beforestarting any type of exercise program. Younger persons (less than 50 years ofage) who are either already participating or who wish to start exercising shouldfirst be interviewed for a family history of conditions associated with suddendeath and screened for symptoms and clinical signs of cardiovascular disease,and for risk factors for heart disease. When either the family history issuggestive, or clinical suspicion is raised, or risk factors such as hypertension,hypercholesterolemia or cigarette smoking are present, subjects should undergomaximal exercise testing for measurement of exercise performance and theelectrocardiographic response to exercise. When abnormalities are detected,further specialist cardiological investigation including echocardiography andpossibly coronary angiography is indicated. Subjects with identified cardiacdisease should then exercise under supervision, at least initially. But even when these guidelines are followed, less than 20% of subjects atrisk of developing a cardiac event during exercise will be identified. ThusSiscovick and his colleagues have argued that routine exercise testing is oflimited value for assessing the risk of exercise in middle-aged men.
16 Similarly Thompson and colleagues have suggested: `Physicians canrecommend exercise to asymptomatic adults without great concern for possiblecardiovascular complications. ...The risk of exercise is small and suggests thatthe routine exercise testing of healthy subjects before exercise training is notjustified.The recommendations that we have made specifically for persons who arealready active in sport are based on studies of sudden death in marathonrunners. These include:• Runners should not assume that completing a marathon will ensure total immunity from coronary heart disease or that reattainment of that distance after a heart attack will prevent progression of that disease;• Runners should seek medical advice and not force themselves when exertional symptoms develop;• When consulted by symptomatic runners, doctors should not exclude the possibility of coronary or other life-threatening heart diseases such as hypertrophic cardiomyopathy, simply because the athlete is `physically-fit. In brief, our experience is in agreement with the conclusion of Thompsonand colleagues to the effect that only athletes who are symptomatic should beexhaustively tested and discouraged from exercise should a life-threateningcardiac abnormality be discovered. Because in our experience the majority atleast of adults who die suddenly during exercise have, like James Fixx, havewarning symptoms, this simple procedure could possibly reduce the incidence ofsudden death during exercise by as much as 80%. Unfortunately the condition
17will never be completely prevented because in about 20% of persons, suddendeath remains the first symptom of heart disease that they experience, andsome may even have undergone maximal exercise testing without incidencewithin a reasonably short time before their subsequent deaths. While most emphasis is placed on the detection of latent coronary heartdisease, detection of other conditions is also important.Thus persons withhypertrophic cardiomyopathy are at increased risk of sudden death duringexercise. Current practice is that persons with this condition are encouraged toavoid all forms of physical activity, however gentle. Whether this is appropriate,and whether all forms of hypertrophic cardiomyopathy carry an equivalent risk ofsudden death is not yet known. Despite this, current practice is probably that thephysical activity of persons with this condition should be restricted. With regard specifically to rheumatic heart disease, it seems that severeaortic stenosis is the form of valvular disease most frequently associated withsudden death. Furthermore, deaths in persons with rheumatic heart diseasealmost always occur in those in whom the diagnosis of serious heart disease iswell established and whose exercise tolerance had already been severelyrestricted by their disease. Thus it would seem that the physical activity of only those patients withrheumatic heart disease whose exercise tolerance is already restricted, shouldbe further curtailed. There is no firm evidence that the physical activity ofasymptomatic persons with clinical evidence of (mild) valvular dysfunction as aresult of rheumatic heart disease needs to be restricted, nor that physical activitydetrimentally influences the course of their disease. It must be remembered that the heart of a person with rheumatic heartdisease must beat 24 hours a day despite unfavorable hemodynamic loading. It
18is unlikely that the additional hemodynamic stresses of even one hours exercisea day would materially influence the adaptations already made to compensatefor the hemodynamic abnormalities caused by the valvular disease. With regard to myocarditis, there is the question of the frequency withwhich myocarditis is a cause of sudden death in persons recovering from a viralinfection. It seems likely that this condition is an important, possibly under-recognized risk. Accordingly, persons who do suffer from a viral infection shouldbe encouraged not to exercise vigorously for at least 7-14 days after their bodytemperatures return to normal. A persistent increase in the resting heart ratewould also indicate continuing myocardial involvement and would be an absolutecontraindication to vigorous exercise. Finally, detection of many of the other conditions listed in Table 1 may bedifficult. When identified, the clinician must still decide whether the risk ofsudden death posed by that condition exceeds the benefits the patient mightexpect from continuing to participate in regular exercise.
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24TABLE 1. CAUSES OF SUDDEN DEATH DURING EXERCISE IN ATHLETESFactors that cause myocardial ischaemiaAtherosclerotic coronary artery diseaseCoronary artery spasmDe novo coronary artery thrombusIntramyocardial bridgingHypoplastic coronary arteryAnomalous coronary arteriesStructural abnormalitiesHypertrophic cardiomyopathyMitral valve prolapseValvular heart diseaseLipomatous infiltration of the right ventricleMarfans syndromeRight ventricular dysplasiaArrhythmiasWolfe-Parkinson-WhiteLown-Ganong-LevineVentricular arrhythmiasMedial hyperplasia and intimal proliferation of the main sinus node arteryMiscellaneousSubarachnoid haemorrhageGastrointestinal haemorrhageMyocarditis From: Sadaniantz and Thompson (1990).