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Historical Concepts of the Athlete???s Heart

2004; Lippincott Williams & Wilkins; Volume: 36; Issue: 3 Linguagem: Inglês

10.1249/01.mss.0000117117.67849.f6

1530-0315

Paul M. Thompson,

Cardiac electrophysiology and arrhythmias

American College of Sports Medicine (ACSM) President-Elect Larry Kenney first asked me to be the D. Bruce Dill Historical Lecturer in early August 2002. He asked me again in late September 2002, and I still did not have an answer. I was flattered to be asked, but thought that such honors were given to historians or to very senior individuals who were not historians. I am a clinical cardiologist and certainly no historian. I also did not consider myself sufficiently "historical" from either an academic or aging perspective, despite my advancing alopecia. After some pressure, and after being told by Dr. Kenney that no nominee had ever refused the honor, I accepted. In retrospect, I have no idea how Dr. Kenney would have known that no previous nominee had refused, but this tactic was successful. I will use the term, "Athlete's Heart," to refer to both the physiologic adaptations that occur with prolonged endurance training and to the generalized historical and present concerns about the cardiovascular risks of exercise and exercise training. No topic could be more appropriate for me as a cardiovascular clinician interested in exercise and as an ACSM member. That is because the history of the Athlete's Heart is a history of cardiovascular medicine in general and the ACSM in particular. In fact, I wonder if the ACSM would have been founded without the interest generated by concerns about the Athlete's Heart. THE ATHLETE'S HEART IN ANCIENT GREECE AND ROME The history of the Athlete's Heart mirrors the ongoing debate on the risks and rewards of vigorous exercise and of athletic training and competition, a debate existent since ancient Greece. These real and imagined risks of exertion are epitomized by the story of Pheidippides, the Athenian who in 490 BC reportedly ran 40 km (24 miles) from the battlefield at Marathon to Athens (24). He announced the Athenian victory, collapsed, and died. This story provides a dramatic introduction to the risks of exercise but is likely only partly true. Pheidippides was more likely named Philippides or Phidippus (24). His run was not solely from Marathon to Athens to announce victory, but from Athens to Sparta to solicit military aid and back to Athens with the bad news that the Spartans were not coming (Pheidippides. Internet Communication Accessed 5/2003). This distance was not 40 km, but closer to 500 km (300 miles) (24). Most distressing of all to those who would cite this event as evidence of the dangers of extreme exertion, our runner, name uncertain, probably survived because Herodotus, the major historian of the event, never mentioned the runner's demise, (24) and Herodotus "was too good a reporter to miss such a story." (13) The confusion probably arises from the mixing of the marathon story with that of a runner named Eucles who 50 years later also ran to Athens to announce victory and did die (3). The legend of Pheidippides attested to the dangers of prodigious exercise but did not undermine the Greeks' belief in the benefits of exercise. Herodicus (480–? BC) was a physician as well as a wrestling and boxing instructor who was among the first to integrate exercise with the practice of medicine (34). Herodicus' interest in exercise influenced Hippocrates (460–470), the author of the Hippocratic Oath and widely considered to be the father of scientific medicine, who dedicated a chapter in his book, "Regimens in Health," to the topic of athletic training (34). Hippocrates recommended a balance between dietary intake and exercise, (34) implying that exercise should be moderate and balanced with other hygienic interventions. Hippocrates in turn influenced Galen (129–210 AD), a Roman physician, who also wrote on the use and value of exercise (3). The influence of Hippocrates and Galen on medicine extended beyond their times, and their teachings and writings were used in medical schools through the mid 1700s. John Pugh in 1794, for example, quoted Hippocrates and Galen when he wrote on the value of exercise (34). Herodicus, Hippocrates, and Galen addressed the benefits of exercise, but little additional exercise was required in agrarian societies devoid of labor-saving devices. The Industrial Revolution, however, changed this and prompted concern among European and American physicians as to whether urbanites obtained sufficient exercise (47). THE ATHLETE'S HEART IN THE 19TH AND EARLY 20TH CENTURIES Almost simultaneously there emerged concerns about the dangers of overexertion. Jacob Mendez Da Costa studied Union Soldiers from that Civil War presenting with cardiac symptoms including palpitations, tachycardia, dizziness, and dyspnea (47). This constellation was called the "Soldier's Heart" and was attributed to the physical demands of long military campaigns. That report implied a danger from excessive exertion, even though modern clinicians would more likely attribute such symptoms to the hyperventilation, anxiety, and stress of combat. Later clinicians would refer to a similar constellation as the "Effort Syndrome," (47) again implying a danger from excessive exertion. Interestingly, the Soldier's Heart also has a role in the founding of the ACSM as will be discussed later. Interest in competitive sports increased in both the United States and abroad after the Civil War (47). This growth in competitive athletics was linked in no small measure to the concept that competitive athletes built what Professor James Whorton has called "the most prized of Victorian virtues, character." (47) This was coupled with religious overtones and the idea that competitive and physical fitness built moral fitness. Competition was considered central to this moral development. Consequently, for both British and American society, the Athlete's Heart was not solely a physiologic but also a moral concept (47). Indeed, Professor Roberta Park maintains that interest in the medical aspects of sports originated in England during the 1800s in preparatory schools such as Eton and Rugby and at universities such as Oxford and Cambridge, where the cream of the British Empire prepared for their roles in society (34). Pre-Victorian sports for the gentry included such activities as riding, hunting, and cricket. Other more competitive sports such as boxing, rowing, walking, and running were primarily activities of the labor class and often tested the skills required in manual labor. This changed during the Victorian period when events such as the Oxford-Cambridge boat race, first held in 1829 (47), became popular among the upper classes. Laboring-class athletes were formally excluded from amateur competitions in 1867 when a "mechanics clause" was added to the rules of the Amateur Athletic Club to exclude those whose employment required physical activity (34). Mechanics and laborers continued to engage in professional sports, but amateur sports dominated the competitive scene (34). With increased participation of the upper classes in competitive sports came increased concern over the medical risks of these activities, a concern that had not existed when only the laboring class was at risk. F. C. Skey, a London surgeon, was among the first to warn of the dangers of overexertion. In a letter to the London Times in 1867, he likened the Oxford-Cambridge boat race to cruelty to animals and remarked "… of this form of cruelty to animals no modern example is so great as the annual University boat race" (41). Dr. Skey also raised concerns that extreme exercise could lead to permanent injury: "I only desire to express my own conviction, and … that of my professional brethren … that young men … cannot perform a feat which compels them to put forth the absolute strength of their physical frame for 20 min without injury, often of a permanent nature" (41). Dr. Skey was especially concerned about cardiac effects of such exertion: "The late Dr. Hope, well known to our profession as the author of a work of great authority on diseases of the heart, has often declared that he knew no cause of disease of this organ so common as hard exercise in rowing" (41). Other clinicians were also concerned about the cardiovascular risks of exercise. The Clinical Society of London in 1873 published a report by Thomas Allbutt on "overstrain of the heart and aorta" (34). E. H. Bradford states that Benjamin Ward Richardson, an English physician, warned in the 1880s that all athletes over age 35 who had competed for more than 10 years were disabled (6). Initial medical concerns focused on the cardiac risks of rowing, but other sports also became suspect as they became popular. In the late 1800s, endurance bicycling included events covering 500 miles in 24 h or lasting 6 d (47). The British Medical Journal noted: "Several well-known French cyclists have lately, it is said, been rejected as unfit for military service by reason of hypertrophy and other diseases of the heart…. Lay opinion, professes astonishment at this result. But medical men will be rather surprised that the numbers are so small. There must be very few of us who have not seen the ill effects of over-exertion on a bicycle" (7). The revival of the marathon in the 1896 Olympic Games kindled an interest in distance running. The popularity of distance running was accompanied by concerns about Runner's Heart. The Journal of the American Medical Association in 1903 included an editorial on the dangers of competitive college athletics stating "That repeated exercise, such as prolonged training in successive yr, may lead to permanent injury is unquestionable…" (2). Consequently, rowers' heart, bicyclists' heart, and runners' heart each had their day. The possible danger associated with marathon running contributed to its appeal. The Boston Marathon was first run in 1897. According to author Tom Derderian, who has chronicled the history of the Boston Marathon: "The Boston Marathons run in 1897, 1898, and 1899 were not little, humble affairs but big sporting events in Boston. The newspapers reported the results on the front page. In the first decade of the 20th century, marathoners became major sports heroes in the world. They were the explorers, test pilots and astronauts of their era, boldly running where none had run before, and, in their perceptions and the public's, risking their lives and future health to do it…. The public lined the course to bet large sums on the outcome of the race and to watch whether any of the participants would actually drop dead from exhaustion" (13, p. xxiv). In the United States, interest in the marathon, and in runners' heart, intensified after Johnny Hayes won the 1908 Olympic Marathon in London's White City Stadium (47). Hayes's victory, and its effect on American distance running, was probably comparable to that of Frank Shorter's Olympic Marathon victory in Munich in 1972. Before Shorter's victory, an impostor entered the stadium first and ran around the track confusing the crowd, and Shorter (46). Before Hayes' victory, an Italian, Dorando Pietri, entered the stadium first (24). In contrast to Shorter's impostor, however, Pietri was in extreme distress. He turned the wrong way in the stadium, fell, but was assisted to his feet and pointed in the right direction. He staggered around the track and was helped across the finish line. He collapsed again and was carried off but subsequently disqualified for having received assistance during the race (24). All was not lost for Pietri, however. Jack Andrews, an Englishman most responsible for assisting the Italian, claimed that he had only caught Pietri as he fell across the line. The British were quite sympathetic with Pietri, and Queen Alexandra presented him with a gold cup identical to that won by Hayes (24). The combination of Hayes' victory and Pietri's collapse heightened interest in running in United States and Great Britain but did little to reassure physicians of its safety. As a sidebar, the 1908 Olympics are also of historical interest for establishing the Olympic Marathon distance. The race started at the Windsor Castle and finished opposite the Royal Box in London's White City Stadium. This arrangement was to ensure that the Royal family could watch the race. This distance from Windsor to White Stadium was 42,195 m or 26.219 miles. It would become the official Olympic Marathon distance 16 yr later (24). "MR. MARATHON"—CLARENCE DEMAR Although the perceived dangers of marathon racing stoked public interest and attracted some participants, this possible risk adversely affected some competitors. Clarence DeMar is a legendary figure in American distance running. He won the Boston Marathon a record seven times (12) and competed in the race 32 (15) times. D. Bruce Dill studied DeMar in the Harvard Fatigue Laboratory, (9) and DeMar is reportedly the first runner to undergo exercise stress testing (15). After DeMar died on June 11, 1958, from metastatic colonic cancer, Paul Dudley White, a renowned Boston cardiologist, examined DeMar's heart. The report, "Half a Century of Running: Clinical, Physiologic and Autopsy Findings in the Case of Clarence DeMar ('Mr. Marathon')" was published in the New England Journal of Medicine. DeMar's coronary arteries were found to be "unusually large and were estimated to be two or three times normal size." (9) The report notes that the necropsy was difficult because "the body had been embalmed and a trocar (for insertion of embalming fluids, author edit) had passed through the heart in several places." Furthermore, there is also an apocryphal story that I cannot confirm or deny, despite discussion with three senior Boston cardiologists, that the autopsy was performed after Dr. White had convinced DeMar's widow to permit exhumation of DeMar's remains. Nevertheless, DeMar, as a competitor in the first decades of the 20th century, was vulnerable to concerns about his sport and its effect on his health. His autobiography published in 1937 includes several events from prior years suggesting that comments about the risks of the sport had left their mark (12). DeMar described the following incident while training during the winter of 1909–1910: "All winter, regardless of weather, I kept my running, to or from work, or both. This made from 7 to 14 miles per day. Frequently the men in the shop showed an interest in my way of travel. Now and then one would advise me of the danger to heart and health. Once a man in the street offered me a dime for carfare; and again while passing through West Everett someone yelled insistently 'Hey! Hey! you running?' I stopped. Then he said, 'A year from now you'll be dead, running like that!' Twenty-seven years have passed by and the dire prophecy is still unfilled" (12; p. 18). After DeMar finished second in 1910 in his first BAA attempt, DeMar was again warned about his health, probably because a cardiac flow murmur, expected in such an athlete, had been misdiagnosed: "… a couple of athletic fans… had approached me about letting them help me get into shape…. These fellows aimed to be thorough … and so took me to be examined by an old doctor in Roxbury. He told me that I had a slight heart murmur and should not run more than a year or two. I asked him how I'd first notice anything wrong with my heart, and he said that in a few years I'd feel weak, going up and down stairs. I've been looking for these symptoms for over a quarter of a century! In less than 2 years I'd heard that the old doctor had died of heart failure himself, so I've often wondered if he wasn't listening to his own heart by mistake" (12; pp. 22–23). These concerns ultimately contributed to DeMar's taking a hiatus from the sport: "When the Brockton Fair marathon came around I didn't feel that I should waste a day's pay to run, so in the fall of 1912 began a rest from marathoning which was to last about 5 years. There were really other reasons. The frequent warnings of the doctors and fans of the danger to one's heart if he kept up running had left their impression. Second, as before indicated, I took my religion somewhat seriously…. I had a suspicion that the whole game of running was a selfish vain glorious search for praise and honor" (12; p. 58). GROWING CONCERN ABOUT THE ATHLETE'S HEART Description and concern. The term, Athlete's Heart, appears to have been coined by a Swedish physician, S. Henschen, writing in German in 1899 (38). Henschen examined cross-country skiers before and after a race. Using only percussion as his diagnostic technique, he concluded that there was both cardiac dilatation and hypertrophy and that both the right and left sides of the heart were enlarged. It is remarkable that Henschen's conclusions have only recently been confirmed by echocardiography. Henschen also thought that there was acute dilatation of the heart postexercise, which he attributed to acute cardiac failure from prolonged exertion. Many authors, including those most supportive of exercise, such as R. Tait McKenzie, a key person in the history of the founding of the ACSM, and Peter Karpovich, an ACSM Founder, shared Henschen's concern about possible acute cardiac dilatation with exercise. McKenzie encouraged vigorous exertion for youth but was concerned about the cardiac risks of exercise for older individuals (27). In an article arguing that concerns about exercise are overdone and asking "for a complete reconsideration of the whole question of exercise in relation to the heart," McKenzie states, "It is in those unprepared for violent exercise, and especially when approaching middle life, that the danger of heart strain is most imminent" (27). When describing the probable cause of symptoms in a middle-aged, former athlete who developed dyspnea and fatigue when he tried "to repeat the exploits of his former days," McKenzie suggests that, "This is undoubtedly an acute dilatation of a heart on which strain has been put in the unfounded expectation that the resiliency of twenty will be found fifteen years later" (27). Peter Karpovich as late as 1935 discussed the possibility that a fatigued or "burnt-up athlete" may be "a possible case of a dilated heart" (21). In most of these writings, the primary concern is with acute cardiac enlargement after exercise, because of concern that this represents acute cardiac decompensation and because "dilatation of the heart increases its weakness." (21) This cardiac enlargement, or dilatation, immediately after exercise was probably simply due to increased end diastolic volume, possibly more notable in athletes in the supine position because of their chronically enlarged hearts and expanded plasma volumes. Concerns about the risk of exercise were not universal during the later half of the 19th century. In response to questions on the dangers of rowing, John Edward Morgan, a physician from Manchester England and captain of the Oxford crew for 3 years, contacted 251 of 255 men who had rowed for Oxford between 1829 and 1869. Morgan published in 1873 that the oarsmen were in better health than the general population and that only three of the men had died from heart disease (29,34,47). E. H. Bradford in 1877 (6) and George Meylan in 1903 (47) reported similarly encouraging results for oarsmen who had competed for Harvard between 1852–1870 and 1852–1892, respectively. In retrospect, a concern about the deleterious effects of vigorous exertion and exercise training are perfectly understandable given the concepts and diagnostic techniques of physicians of the era. Before the introduction of the electrocardiogram, x-ray, and echocardiogram, cardiac diagnoses were made by palpation of the pulse, percussion of the chest to determine heart size, and cardiac auscultation to detect cardiac murmurs. The characteristics of the Athlete's Heart including sinus bradycardia, biventricular cardiac enlargement, and pulmonary as well as aortic flow murmurs were easily interpreted as pathological heart block, cardiomyopathy, and valvular obstruction. All of these maladies had terrible prognoses because they were virtually untreatable with the medical management then available. Also, because chronic cardiac dilatation associated with cardiomyopathy indicated myocardial dysfunction, the acute dilatation noted after exertion was assumed to indicate acute cardiac failure. THE ATHLETE'S HEART AND THE AMERICAN COLLEGE OF SPORTS MEDICINE. Despite information to the contrary, concern about the Athlete's Heart would persist into the middle of the 20th century. This concern would contribute to the formation of the ACSM on April 22, 1954, in the Hotel Stadler in New York City (4). One person who contributed to this process was R. Tait McKenzie. McKenzie was a physician trained in medicine at McGill who was Professor of Physical Education at the University of Pennsylvania from 1904 until his death in 1938 (4). McKenzie crusaded against the concept that vigorous exercise and exercise training could injure the heart. In 1912, he noted murmurs immediately after exertion in 28% of physical education students and concluded that murmurs associated with exertion were physiological and not pathological (27). In 1916, R. Tait McKenzie worked at the Soldier's Heart Hospital in England, an institution dedicated to the treatment of heart disease in soldiers from the Great War (4). Sir James Mackenzie of Scotland was a leading figure in this hospital and an advocate of exercise in the treatment of the soldiers' condition. Also working in the Military Heart Hospital was Sir William Osler, who would become the noted Johns Hopkins physician, and Sir Thomas Lewis, an expert in the newly discovered field of electrocardiography. Joseph Wolffe subsequently studied under Sir James Mackenzie (4). In Philadelphia, R. Tait McKenzie and his interest in the Athlete's Heart would influence both Grover Mueller and Joseph Wolffe, 2 of the 11 Founders of ACSM (4). Indeed, at least six of the ACSM founders, Joseph Wolffe, Herbert Mueller, Albert Hyman, Louis Bishop, Peter Karpovich, and Ernst Jokl had a direct interest in the Athlete's Heart. Mueller was a basketball coach who in 1927 became Director of Physical and Health Education for the Philadelphia Board of Education (4). Joseph Wolffe was not only a Founder and first President of ACSM but also a nationally prominent cardiologist (4). From 1932 to 1947, he was head of the Cardiovascular Division at Temple University. Wolffe was also a Founding Member of the American Association for that Study of Atherosclerosis and a Founder and Trustee of the American College of Cardiology. Dr. Wolffe left Temple to establish the Valley Forge Medical Center and Heart Hospital in Norristown, PA. The exercise facility at this Heart Institute was named the R. Tait McKenzie Gymnasium, demonstrating Wolffe's admiration for McKenzie (4). Mueller and Wolffe shared McKenzie's interest in the Athlete's Heart. In 1944, The Philadelphia Association for Health, Physical Education, and Recreation and a group of cardiologists formed a Committee on the Cardiovascular Study of Athletes. Grover Mueller was chair, and the committee's first round table discussion, "Athletics and the Heart," was held at Wolffe's offices in Philadelphia in December 1945 (4). Dr. Wolffe also encouraged the American Heart Association (AHA) to examine the issue of the Athlete's Heart (4). In 1947, Dr. Wolffe wrote to Dr. Howard Sprague of Boston noting that some cardiologists still believed that vigorous exercise could injure the heart. Dr. Wolffe requested that the AHA study the subject. Dr. Wolffe repeated his request in 1949. In 1953, Dr. Wolffe recruited Ernst Jokl, originally from Witwatersrand Technical College in Johannesburg, South Africa, to his Norristown, Heart Hospital where Jokl would serve as Director of Research and Head of Clinical Physiology (4). Dr. Jokl was an expert in the cardiac complications of exercise. Jokl's momongraph, "Acute fatal nontraumatic collapse during work and sport," published in 1971 with Dr. L. Melzer is a classic in the area of exercise-related cardiac events (20). Joseph Wolffe was friendly with two other cardiologists who would also become Founders of ACSM and ACSM's second and third Presidents (4). Dr. Albert Hyman was a cardiologist and graduate of Harvard Medical School who became interested in sports medicine from assisting in studies of runners in the Boston Marathon. He would succeed Wolffe as ACSM President. Dr. Lewis Bishop was the third cardiologist who is also a Founder of ACSM. Bishop shared an interest in the cardiovascular aspects of athletics and in 1930 coauthored a book with his father on "Athletics and the Heart" (4). Consequently, three cardiologists, interested in the problem of the Athlete's Heart, were Founders and the first three Presidents of ACSM. Three other ACSM Founders, Grover Mueller, Ernst Jokl, and Peter Karpovich shared this interest. I wonder if ACSM would have been founded without such a profound interest in the possible cardiovascular risks of exercise. The fourth President of ACSM was D. Bruce Dill, the first noncardiologist and first physiologist in this capacity and his election indicated a figurative, if not literal, redirection of ACSM from a cardiac to a more broadly physiological emphasis (4). PAUL DUDLEY WHITE The noted Boston cardiologist, Paul Dudley White, was not a Founder of ACSM but did influence scientific perceptions of the Athlete's Heart and the benefits of exercise in the first half of the 20th century. White's contributions to the study of athletes and his commitment to exercise almost certainly reinforced Wolffe, Bishop, and Hyman's interests in exercise and were acknowledged when he received an honorary ACSM fellowship in 1959 (4). White is considered by many to be the Father of American Cardiology (18). During his internship White, with Dr. Roger Lee, one of the Medical Chiefs of Service at Massachusetts General Hospital, develop the Lee-White clotting time to measure coagulation, (17) a technique I used as a medial resident in the mid 1970s. Dr. White's prominence in cardiology is due in part to his being among the first Americans to be trained in electrocardiography. In 1913, White received a traveling fellowship to study in England with Sir Thomas Lewis, a pioneer in the field. During his time in London, Dr. White visited the cardiology clinics of Sir James Mackenzie (18), the individual mentioned earlier who was interested in the Soldier's Heart. Dr. White would return to England in 1916 as a volunteer physician to assist the English war effort (35). He again worked with Dr. Mackenzie at the Hampstead Military Hospital and was almost certainly imbued with Dr. Mackenzie's therapeutic use of exercise for this condition. After his 1913 sojourn to England, however, Dr. White returned to Boston and Massachusetts General Hospital, where he developed and directed the cardiology service until 1949 when he resigned to become Executive Director of the National Heart Institute, the forerunner of the National Heart, Lung, and Blood Institute (18). Dr. White achieved international fame when he was consulted to assist with the care of President Eisenhower in 1955 after Eisenhower suffered a heart attack (39). Dr. White received formal national recognition in 1986 when a 3-cent postage stamp was printed in his honor (39). White made many contributions to both the science of the Athlete's Heart and the use of exercise in heart disease prevention. He measured the rate and contour of the radial pulse of Boston Marathoners in 1915 and 1916 using the "Mackenzie ink polygraph," developed by his English mentor (48). White's goal was to determine whether the cardiac dilatation produced by extreme exercise was associated with pulsus alternans, a sign of severe cardiac dysfunction. He concluded that "marathon racing does not exhaust the healthy heart sufficiently to produce alteration of the pulse." In 1942, he heard that a runner named Les (Mercury) McMitchell had been rejected for military service because of a heart rate < 40 beats per minute (25). White initially thought "that a heart rate under 40 per minutes does not normally exist, since I myself had not encountered or heard of such a bradycardia" (49), but after reviewing the electrocardiograms of four healthy athletes, including a miler, referred to only as "Cunningham," but presumably the famed American miler, Glen Cunningham, he concluded that such marked bradycardia could be normal especially in long-distance runners (49). McMitchell was reportedly reconsidered for military service and accepted into the Navy (25). Dr. White was personally committed to exercise. When White died in 1973, Dr. Francis Ingelfinger's obituary for White in the New England Journal of Medicine started with the statement, "Practically everyone knows that Dr. Paul Dudley White rode a bicycle and preached exercise." (19) Dr. William Proctor Harvey wrote the following in his remembrance of Dr. White: "A strong advocate of our need for exercise, Dr. White walked whenever he could, chopped wood, shoveled snow, and was a familiar sight riding his bicycle in his neighborhood. On one occasion after flying from Boston to Washington, he walked from National Airport to that White House, where he was scheduled to meet with President John Kennedy…. On arriving at the White House, the guard at the gate, the gentleman that met him at the front door, the office personnel and President Kennedy himself all independently asked: 'How did you get here?' When to each he replied: I walked from the airport, all of them, including the President, stood with mouths agape in utter amazement." (16) This was not an isolated incident. As retold by Dr. J. Willis Hurst: (17) "Albert M. Baer, of New York, relates that P.D.W. once asked how far it was from the American Heart Association office, which was located on the corner of 23rd Street and Madison Avenue in New York City to LaGuardia Airport. The answer was seven miles. Dr. White walked the entire d