The athlete’s heart

The human heart is an enigma, and the athlete’s heart especially so. It is no accident that the heart is the body part that acts as the final defender keeping mortality at bay while serving as the icon for our aspirations and passions.  It is no accident because this mundane but crucial pump beats autonomously, but is also modulated by subtle, ethereal influences.  It is governed by the non-conscious autonomic nervous system – the exciting sympathetic division often dominating in the duel with the soothing parasympathetic division – and also by a multitude of hormones: adrenaline and the adrenal steroids; insulin and growth hormone; and also the sex steroids, oestrogen and testosterone, which might explain the greater vulnerability of the male runner’s heart – a topic we shall return to later.   Oxytocin, the hormone released in response to human touch that fosters not only the bond between a mother and her infant but also the bonds between lovers, can reduce the inflammatory processes that appear to contribute to the over-training syndrome, and even prevent cell death in an injured heart – at least in rats[1].

Perhaps to the non-runner, the enigma is why runners are so devoted to their sport.  It is of course relatively easy to comprehend the mind of the elite athlete striving for Olympic glory, but a surprising passion is found  across the entire spectrum for those whose ambition is to run 10 Km in an hour to those aiming to run a half-marathon in that time.  In the internet era, running has become a major social event.  On web-sites such as Fetch Everyone, hundreds of runners not only record hundreds of thousands of training miles, diverse races and numerous hard-won PB’s,  but also engage in a wide range of chatter, most of it mutually supportive but sometimes it is bitchy and at other times ribald.   The austere amateur spirit that permeated athletics when it was largely the preserve a small group of dedicated, almost monastic, individuals in the 1950’s has given way to something of a carnival.  Though of course the ribald graffiti occasionally uncovered on medieval monastic cell walls suggest that monasticism has always been only a thin veil over seething passion.

John Hadd

But to runners the enigma of the heart is more profound.   Sadly, this was illustrated by the recent death of John ‘Hadd’ Walsh.  He was the founder and a guiding spirit of the Malta marathon in the 26 years since its inception, but by virtue of his generous spirit, thoughtful analysis of heart physiology, and pugnacious writing, his influence extended far beyond the island of Malta and shaped the training programs of runners worldwide.    He was devoted to his wife, the marathon runner, Carol Galea.   He was 8 years her senior, and declared that he would train with a dedication sufficient to ensure that he lived to be 108, so they would not be separated prematurely.  Tragically, his promise was not fulfilled as he died, apparently of a totally unanticipated heart attack, during an early morning run at age 56 [2].  Though a personal tragedy, his death, along with the occasional reports of other untimely deaths of athletes and coaches, might merely be taken as confirmation of the widespread acceptance that running does indeed place an immediate stress upon the heart, but overall, the health benefits of running far outweigh the risks [3].

However the picture is a little more complex.   While at least some premature cardiac deaths among athletes are due to previously unidentified congenital defects, or to unsuspected coronary artery disease in those who take up running in middle age, the challenging question is: does endurance training actually produce persisting damage to the heart?

Two of the greats

The evidence is extensive and controversial, but before dipping into the vast body of scientific evidence, it is illuminating to look at the cases of two other athletes.  The first, Wally Hayward, a legendary figure in the history of the Comrades Marathon, did almost make it to his hundredth birthday.    Hayward first won that gruelling hilly 90 Km ultra-marathon between Durban to Pietermaritzburg  in 1930 at age 21; he was the winner again on four occasions in the 1950’s; and became the oldest person to complete the race when he staggered across the finishing line at age 80 in 1989.    He died in 2006 a few months before his 98th birthday.   At age 70, at a stage when he had engaged in regular training for 52 years, he underwent extensive physiological testing [4]. A treadmill exercise test revealed no ischaemic ECG abnormalities and an excellent functional capacity (VO2max = 58.6 ml/kg/min).  His overall fitness was exceptional for a 70 year-old.  The only two abnormalities reported were frequent premature atrial contractions (PACs) and moderately increased thickness of the left ventricular wall.

The second case is that of Emil Zatopek, world record holder at 5000m and 10,000m in the 1950’s and winner of gold medals in the 5000 m, 10,000m and marathon in the Helsinki Olympics in 1952.   Unlike Wally Hayward, he retired from competitive running at age 35, after 17 years of training that had included a hitherto unheard of combination of intensity and volume.   He continued to be active in the Communist Party in his native Czechoslovakia, but due to his support for the democratic wing of the party during the Prague Spring in 1968, he was banished to work in a uranium mine.  At age 71, three years after his after his rehabilitation as a national hero by Vaclav Havel in 1990, he underwent extensive medical and physiological testing at the Institute of Sports Medicine in Prague [5].   Perhaps as a legacy of the privations of the uranium mine his muscles were flabby and he was a pale shadow of his former self, though it is noteworthy that his joints were remarkable free of the degenerative changes common in his age group.   Of particular interest in the current context, his heart showed some ischaemic changes and he had both atrial fibrillation and ectopic ventricular contractions.

Ventricular hypertrophy and PACs

General conclusions should not be drawn from anecdotes of exceptional athletes.  Nonetheless, the two abnormalities reported in Wally Hayward, hypertrophy of the muscular wall of the left ventricule and frequent premature atrial contractions are both well documented features of the elderly athlete’s heart.  For example, in a study comparing 11 elderly male athletes (mean age 73) with a life-long history of strenuous exercise with matched controls (mean age 74), Jensen-Urstad and colleagues [6] found that 9 of the 11 athletes had more than 100 premature atrial contractions in24 hours compared with 4 of the controls, while 8 of the athletes had multiform ventricular ectopics (indicating multiple maverick electrical sources in the ventricles) compared with 2 of the controls.

Of course ventricular hypertrophy in athletes is only to be expected.  It contributes to the powerful contraction of the well-trained heart.  Unlike the hypertrophy associated with pathological conditions in non-athletes, in which there is decreased blood supply to the heart muscle via myocardial capillaries,  the hypertrophy in athletes is usually accompanied by normal or increased capillary density [7].

Cardiac damage and remodelling

Nonetheless it is probable that the remodelling of cardiac muscle produced by endurance training involves some breakdown of muscle cells, similar to that which can readily be observed in skeletal muscle following intense training.  For example, following demanding endurance events, increased levels of the cardiac enzyme troponin are found in the blood stream, implying damage to heart muscle cells.  Immediately after the 2004 Otztal Radmarathon, troponin levels in the cyclists’ blood were increased 10 fold relative to baseline, and returned to baseline one week later [8].

In skeletal muscle, the muscle cells damaged by training are rebuilt stronger than before.  The persistence of collagen fibres that formed a scaffold during repair is of little importance provided the fibres become well aligned along the direction of pull of the muscle.  On the other hand, heart muscle is different.  Cardiac muscle performs not only physical work of contraction, but the muscle cells themselves from part of the conducting system that initiates and transmits the electrical signal that triggers contraction.   If the heart is to pump efficiently, this electrical signal must be transmitted across the myocardium from the sinoatrial node in the right atrium via the atrioventriclar node to the ventricles, in a well coordinated manner.  It is plausible that misplaced collagen fibres might upset the orderly transmission of the signal and perhaps even cause maverick muscle cells to take over the pace-maker role, generating ectopic beats.  As reported by Jensen-Urstad [6], premature atrial beats and also multiple maverick ventricular sources are substantially more frequent in elderly athletes than in age-matched non-athletes.

Atrial fibrillation

Premature atrial contractions are of little functional importance, but the crucial issue is whether they can lead to the chaotic ill-coordinated contraction that is atrial fibrillation.  In a large population-based study of men and women aged 55-75 in Denmark, Binici and colleagues found that a frequency of premature ectopic atrial contractions greater than 30 /hour, or runs of more than 20 consecutive atrial ectopic beats, was associated with an almost three fold increased risk of hospital admission for atrial fibrillation in the follow-up period of approximately 6 years [9].  There is also worrying evidence of a similar risk in endurance athletes.    The anecdotal account of Emil Zatopek’s atrial fibrillation is consistent with the findings of several large, well designed scientific studies.  For example in an 11 year follow-up study of 252 marathon runners, with mean age 39 at recruitment, the risk of symptomatic atrial fibrillation, based on an observed annual onset rate of 0.48 per 100,  was 8.8 times greater than in a comparison sample of 305 sedentary men, after adjusting or other risk factors such as high blood pressure [10].

Although far less serious than ventricular fibrillation (which is usually lethal) atrial fibrillation has some life-threatening consequences.  It predisposes to the formation of blood clots in the atrium which can subsequently be released into the blood stream, causing a myocardial infarction if they lodge in the coronary arêtes or a stroke if they lodge in the brain.   However, despite the quite compelling evidence for an increased incidence of atrial fibrillation in middle-aged and elderly runners, the balance of evidence does not indicate that the commonly observed heart rhythm abnormalities lead to an increase rate of serious adverse cardiovascular events in middle-aged athletes.   For example, in a 5 year follow-up of 117 middle-aged and elderly cross-country skiers, Lie and Erikssen [11] found that while persisting abnormalities of heart rhythm and also ventricular hypertrophy were common, only 2 developed angina and none suffered a myocardial infarction.  They concluded that the ECG abnormalities were mainly related to physiological adaptation to training and that training seems to protect against coronary heart disease.

Coronary obstruction

So far, we have focussed mainly on possible disturbances of heart rhythm.  In contrast, we have noted that capillary blood supply to the myocardium is often enhanced in athletes, and coronary disease might in fact be reduced.   However, perhaps the most disconcerting study of all is a recently reported investigation of calcified plaques furring-up the coronary blood vessels of elderly men who have participated in multiple marathons.  Schwartz and colleagues found that the prevalence of calcified plaques in the coronary arteries of men who had run in the Twin Cities Marathon annually for at least 25 years was almost twice as high as in age matched sedentary comparison subjects [12].  Enigmatically, the same research group carried out a similar study in female marathoners, with the opposite result: namely, the female runners had far fewer calcified plaques than the matched comparison subjects, though it is noteworthy that the female runners had run at least one marathon annually for only a period of 10 years.   The results of both of these studies should be treated with extreme caution until they have been replicated.  Despite the evidence that the male heart is generally more vulnerable to injury than the female heart, the diametrically opposite findings in the two sexes raise doubt about the generalizability of the findings.  Furthermore, it should be noted that the finding in males might reflect the consequences of running a larger number of marathons.

At least for the time being, the majority of the evidence suggests that despite the fairly high likelihood that long term endurance training will lead to an increased number of premature atrial contractions, the overall effect of endurance training is to increase life expectancy.    In future posts I will examine the evidence in greater detail, and also describe my discoveries about my own heart rhythm since acquiring a heart rate monitor that records the time intervals between consecutive beats.   More formal investigations have demonstrated that my heart is functioning well.  Nonetheless, in light of the growing evidence that elderly endurance athletes face a significant risk of atrial fibrillation, my current opinion is that monitoring heart rate beat by beat is indeed a sensible way of screening for possible increases in frequency of premature atrial contraction.  It would of course be foolish to make any definitive diagnosis based on one’s own observations using equipment that is demonstrably fallible.  It would be similarly foolish to curtail an activity that I enjoy passionately, when even the risk of atrial fibrillation is less daunting than the risk of a sedentary life style.

References

[1] Jankowski M, Bissonauth V, Gao L, Gangal M, Wang D, Danalache B, Wang Y, Stoyanova E, Cloutier G, Blaise G, Gutkowska J. 2010 Anti-inflammatory effect of oxytocin in rat myocardial infarction. Basic Res Cardiol. 105(2):205-18.

[2] Times of Malta, Saturday, September 17, 2011. Malta marathon founder dies  [http://www.timesofmalta.com/articles/view/20110917/athletics/malta-marathon-founder-dies.385085]

[3] Thompson PD, et al. (2007) Exercise and acute cardiovascular events placing the risks into perspective: a scientific statement from the American Heart Association Council on Nutrition, Physical Activity, and Metabolism and the Council on Clinical Cardiology. Circulation. 115(17):2358-68.

[4] Maud PJ, Pollock ML, Foster C, Anholm JD, Guten G, Al-Nouri M, Hellman C, Schmidt DH. (1981) Fifty years of training and competition in the marathon: Wally Hayward, age 70–a physiological profile. S Afr Med J. 31;59(5):153-7.

[5] Novotný V, Brandejský P, BaráckováM, Boudová L, Vilikus Z, Streda A, Novotný A.(1994) Medical and anthropological study of a world and Olympic champion, long-distance runner, 35 years after the end his racing career. Sbornik Lekarsky (Journal of Czech Physicians and the Czech Medical Society) 95(2):139-55.

[6] K Jensen-Urstad,F Bouvier,B Saltin,M Jensen-Urstad (1998) High prevalence of arrhythmias in elderly male athletes with a lifelong history of regular strenuous exercise.Heart 79:161–164

[7] Hudlicka O, Brown M, Egginton S. (1992) Angiogenesis in skeletal and cardiac muscle.  Physiol Rev. 72(2):369-417.

[8] Neumayr G, Pfister R, Mitterbauer G, Eibl G, Hoertnagl H. (2005) Effect of competitive marathon cycling on plasma N-terminal pro-brain natriuretic peptide and cardiac troponin T in healthy recreational cyclists. Am J Cardiol.;96(5):732-5.

[9]  Binici Z, Intzilakis T, Nielsen OW, Køber L, Sajadieh A. (2010) Excessive supraventricular ectopic activity and increased risk of atrial fibrillation and stroke. Circulation. 121(17):1904-11.

[10] Molina L, Mont L, Marrugat J, Berruezo A, Brugada J, Bruguera J, Rebato C, Elosua R. (2008)  Long-term endurance sport practice increases the incidence of lone atrial fibrillation in men: a follow-up study. Europace. 10(5):618-23.

[11] Lie H, Erikssen J. (1984)  Five-year follow-up of ECG aberrations, latent coronary heart disease and cardiopulmonary fitness in various age groups of Norwegian cross-country skiers. Acta Med Scand. 216(4):377-83.

[12] Schwartz JG, Merkel-Kraus S, Duval S, Harri K, Peichel G, Lesser JR, Knickelbine T, Flygenring B, Longe TR, Pastorius C, Roberts WR, Oesterle SC, Schwartz RS (2010) Does long term endurance running enhance or inhibit coronary artery plaque formation? A prospective multidetector CFA study of men completing marathons for least 25 consecutive years.  J. Am. Coll. Cardiol. 55;A173.E1624

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9 Responses to “The athlete’s heart”

  1. Ewen Says:

    Interesting reading Canute. The study with the different results for men and women was an odd one. I wonder what’s going on there? Also, I noticed that most of the studies (and your elite athlete examples) were of marathon runners. I wonder if there’s something inherent in marathon training and racing that produces such results?

    Anyway, like you, I have a passion for running and hope to continue to enjoy it for many years to come. Thanks again for your writing — always thought provoking. All the best with your running in 2012. Hope the 5k training is progressing well.

  2. canute1 Says:

    Ewen
    Thanks for your comment. As you note, most of the evidence I discussed refers to marathon runners, some of whom trained and raced for very extensive period of time. There is fairly clear evidence that endurance athletes have a greater risk of atrial fibrillation than other athletes – though the studies demonstrating increased rates of atrial fibrillation have included not only marathon runners but also Nordic skiers, orienteers and cyclists. However it is not all bad news for endurance athletes. In a study comparing 1282 male athletes who represented Finland between the years 1920 and 1965 at least once in international competition, with a comparison group who had been classified as healthy in a medical examination at age 20, the athletes had a lower prevalence of diabetes, hypertension and ischaemic heart disease than the comparison subjects, and in particular, former endurance athletes had the lowest rates of diabetes and ischemic heart disease (Kujala et al. Metabolism 43:1255-1260; 1994). On balance, I think the evidence suggests that the benefits outweigh risks for most athletes, including endurance athletes, though there is a serious question mark about the balance of risks and benefits of very extensive endurance training and racing, such as marathon training and racing for 20 years.

    The question of whether the risk is a direct consequence of the training, the racing, or of some other, perhaps avoidable, feature, is unknown. As far as practical steps one might take, to me it makes sense to avoid the over-training syndrome and also to ensure adequate recovery after very strenuous training or racing, though as far as I know there is no direct evidence that either over-training or inadequate recovery lead to cardiovascular damage.

    With regard to your enquiry about my own 5K training, I am making slow but steady progress with fitness (eg reduction from 720 to 690 b/Km in typical training runs in the mid-aerobic zone) but various circumstances have prevented me from assessing progress in a race since early November.

  3. Daniel Says:

    I think the question you need to ask in your lit search is that are endurance athletes having higher mortality due to cardiac arrhythmia than general population? vs non-endurance athletes (weight lifters, sprinters, boxers, etc), both overall and adjusted against other co-morbidities like HTN or diabetes and what not. Not entirely sure if any research has look at this, and I’m assuming the evidence is probably not great since there probably isn’t enough interest in the subject for long term survival studies. But in terms of all cause mortality, the evidence seems quite clear that endurance exercising is good for you as you mentioned.

  4. canute1 Says:

    Daniel,

    Thanks fr your comment.

    As you imply, it would be very difficult to answer the question of whether endurance runners have a greater risk of death due to heart rhythm abnormality than other sports people, because such deaths are likely to be very rare (therefore requiring a study of many individuals). In addition, establishing that death is attributable to heart rhythm abnormality is often difficult. However, the most important issue is the rarity of such events.

    This can be seen by considering the evidence regarding outcome of atrial fibrillation, which is the most common of the potentially serious rhythm disturbances in runners.

    First of all, in the general population, atrial fibrillation in the absence of other heart disease, does not appear to be associated with substantially increased mortality. In a 30 year follow-up study of 76 patients with lone AF (i.e. atrial fibrillation without other heart disease) compared with age and sex matched individuals from the general population, Jahangir and colleagues found a 68% survival after 30 years in the AF group compared with 57% survival in the matched subjects in the general population (Circulation 2007;115:3050-3056). Risk for stroke or transient ischemic attack (TIA) was similar to the expected population risk during the initial 25 years of follow-up (12% of AF cases suffered stoke or TIA, compared with 11% from the matched general population at 25 years), but the risk increased more in the AF cases after 25 years. By 30 years, 5 of the 76 AF cases had suffered stoke and 12 had suffered TIA. However, the stroke or TIA was attributable to embolism (the expected mechanism by which AF causes stroke or TIA) in only 4 cases and to probable embolism in the presence of atherosclerotic disease in a further 3 cases. All who suffered a strole or TIA had an additional risk factor such as high blood pressure, diabetes or heart failure. Since risk of diabetes and of high blood pressure is reduced in athletes compared with the general population, these data suggest that in athletes, the risk of either death, stroke or TIA , due to AF is likely to be small.

    With regard to a comparison between runners and other sports people, in their study of former international sportsmen and women, Kujala et al found that endurance runners had the lowest rates of diabetes and ischaemic heart disease (Kujala et al. Metabolism 43:1255-1260; 1994). However with regard to hypertension, the evidence is less clear cut. Aerobic exercise, including running, helps lower blood pressure but so too does progressive resistance exercise helps lower blood pressure (Kelley and Kelley, Hypertension, 2000, 35:838-843.)

    Overall, there little doubt that running is more healthy than a sedentary lifestyle, and the risks of serious adverse events are small, except perhaps at the extreme ends of the spectrum of endurance running. With regard to comparison between endurance running and sports such as sprinting or weight lifting , I think that the differences in mortality or overall risk of high blood pressure, diabetes and ischaemic heart disease are likely to be very small. Therefore, I think you should do what you enjoy most.

  5. Is prolonged vigorous training bad for your health? « Canute’s Efficient Running Site Says:

    […] 5)       In at least some cases, especially males who have run many marathons over a period of many years, there is evidence of increased calcification of the coronary arteries, potentially predisposing to heart attack (reviewed in my post of Jan 2012). […]

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