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ORIGINAL ARTICLES
Sudden Death in Young Athletes
BARRY J. MARON, M.D., WILLIAM C. ROBERTS, M.D., HUGH A. MCALLISTER, M.D.,
DOUGLAS R. ROSING, M.D., AND STEPHEN E. EPSTEIN, M.D.
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SUMMARY The causes of sudden and unexpected death in 29 highly conditioned, competitive athletes, ages
13-30 years, are summarized. Sudden death occurred during or just after severe exertion on the athletic field in
22 of the 29 athletes. Structural cardiovascular abnormalities were identified at necropsy in 28 of the 29
athletes (97%), and in 22 (76%) were almost certainly the cause of death. The most common cause of death in
this series was hypertrophic cardiomyopathy, which was present in 14 athletes. Other cardiovascular abnormalities that occurred in more than one athlete were anomalous origin of the left coronary artery from the
right (anterior) sinus of Valsalva, idiopathic concentric left ventricular hypertrophy, coronary heart disease
and ruptured aorta. Cardiac disease was suspected during life in only seven of the 29 patients, and in only two
of the seven was the correct diagnosis made clinically. Hence, in this series of young athletes, sudden death was
usually due to structural cardiovascular disease, and hypertrophic cardiomyopathy was a frequent cause of
sudden death; atherosclerotic coronary heart disease was relatively uncommon.
ALTHOUGH YOUNG, competitive athletes epitomize the conditioned, healthy segment of society,
sudden and unexpected death does occur in such individuals.1-4 However, no large series of sudden deaths
in athletes has been systematically compiled, and
therefore the principal causes of such deaths have not
been adequately defined. Because such information
might help to identify athletes who are "at risk" of
sudden death, the present study was undertaken. In
this investigation we have attempted to determine the
causes of sudden, unexplained death in a group of
highly competitive athletes.
initially referred to the NHLBI for consultation
because of the occurrence of sudden death and suspicion of heart disease; subsequently these patients were
identified as having been competitive athletes during
life. Six of the 29 study patients have been included in
published studies.2 5, 6
For inclusion in the study each patient must have
been an active and highly conditioned member of an
organized athletic team for at least 2 years at the
junior high school, high school, collegiate or professional level. Four of the 29 athletes had withdrawn
from organized team sports 1-5 years before death,
but had continued to maintain a high level of conditioning. It also was necessary that a complete
necropsy examination be performed in each patient to
exclude trauma-related causes of death and that, in
particular, the heart be in suitable condition to permit
examination.
Toxicologic tests for levels of alcohol, barbiturates
and amphetamines were performed postmortem on
blood from 15 patients, and the levels of each were
normal. None of the 29 athletes had a history of drug
usage.
Materials and Methods
Selection of Patients
The 29 athletes with sudden and unexpected death
who constitute the study group were initially identified
from the following sources: (1) prospectively from
news media reports of sudden death in competitive
athletes from 1976-1979 (17 athletes: two died in the
Washington D.C. metropolitan area and the other 15
died elsewhere); (2) retrospectively from review of the
autopsy registry of the Cardiovascular Division of the
Armed Forces Institute of Pathology, 1950-1978
(seven athletes who were military dependents and
whose hearts were referred for consultation because of
the occurrence of sudden death and suspicion of heart
disease); and (3) retrospectively from review of the
autopsy registry of the Pathology Branch, National
Heart, Lung, and Blood Institute (NHLBI) (five
athletes). The hearts of four of these patients had been
Necropsy Studies
In addition to gross visual examination, measurements were made of the maximum thickness of
the ventricular septum and posterior left ventricular
free wall. Trabeculae, papillary muscles and crista
supraventricularis were not included in the measurement of wall thickness. The extramural coronary
arteries were studied in the intact specimen by making
multiple cross sections of the vessels (3-5 mm apart)
and viewing the arterial lumens grossly.
Blocks of myocardium were taken from the ventricular septum for histologic study of cardiac muscle
cell arrangement. When pertinent, the extent of
cellular disorganization was assessed in tissue sections
by a previously described quantitative method.7
In four athletes (three with idiopathic concentric
From the Cardiology and Pathology Branches, NHLBI, NIH,
Bethesda, Maryland, and the Department of Cardiovascular
Pathology, Armed Forces Institute of Pathology, Washington, D.C.
Address for correspondence: Barry J. Maron, M.D., Cardiology
Branch, Building 10, Room 7B-15, NHLBI, Bethesda, Maryland
20205.
Received October 24, 1979; revision accepted January 30, 1980.
Circulation 62, No. 2, 1980.
218
SUDDEN DEATH IN YOUNG ATHLETES/Maron et al.
left
ventricular
hypertrophy
and
one
with
hyper-
trophic cardiomyopathy), the heart was in suitable
condition to permit removal of the sinoatrial and
atrioventricular node areas for histopathologic study
of the conduction system.8' 9 Serial sections 6 m thick
were cut from each conduction system block; every
tenth section was stained with hematoxylin and eosin
or elastic van Gieson.
Echocardiographic Studies
M-mode echocardiograms were obtained in a total
of 75 first-degree relatives (ages 4-58 years, mean 28
years) of 15 athletes in whom the necropsy diagnosis
was hypertrophic cardiomyopathy or idiopathic concentric (symmetric) left ventricular hypertrophy.
Thicknesses of the ventricular septum and posterior
left ventricular free wall were measured as previously
described.'0
219
curred during or just after severe exertion. Each of
these 22 deaths occurred during an athletic contest or
during training. Two of the remaining seven patients
died during or just after relatively mild exertion unrelated to participation in sports, and five athletes died
during sedentary activities.
Necropsy Findings: Causes of Sudden Death
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Structural cardiovascular alterations were identified
the 29 athletes (97%), but no
significant anatomic abnormality was found in an
organ other than the heart (fig. 1). The remaining
patient, -a 14-year-old high school football player, had
a normal heart by both gross and histologic examination. ECGs in five first-degree relatives of this athlete
showed no abnormalities (including no evidence of
prolonged QT interval syndrome), but a systematic
examination of the conduction system was not possible in his heart.
at necropsy in 28 of
Results
Demographic Data and Circumstances of Death
The 29 athletes ranged in age from 13-30 years
(mean 19 years). Twenty-six athletes were male and
three were female; 20 were white and nine were black.
Body surface areas ranged from 1.7-2.4 m2 (average
2.0 m2).
At the time of death the athletes had most commonly reached the high school or junior high school
level of competition (17 athletes), although eight were
participating in intercollegiate sports programs and
four were professional athletes. The athletes had participated in a wide variety of sports, but basketball
and football were most common (table 1). The duration of participation at competitive levels ranged from
2-18 years.
In 28 of the 29 athletes, death occurred suddenly
without warning and was virtually instantaneous; the
other athlete survived 12 hours in a terminal state
after her collapse. In 22 of the 29 athletes, death ocTABLE 1. Sports Participated in by 29 Competitive Athletes
n*
Sport
11
Basketball
Football
10
Running (track)
4t
3
Wrestling
1
Swimmring
1
Boxing
1
Hockey
1
Soccer
1
Tennis
1
Baseball
1
Gymnastics
*Each sport was tabulated for athletes participating in
more than one.
tIncludes one athlete who participated primarily in the
pole vault.
Patients with Unequivocal Evidence
of Cardiovascular Disease
Of the 28 athletes with structural cardiovascular
alterations, 22 were considered to have unequivocal
cardiovascular disease that caused sudden death (fig.
1); the diseases were congenital in 19 of the 22 patients
and acquired in the other three.
Hypertrophic Cardiomyopathy
The cardiovascular disease most commonly identified was hypertrophic cardiomyopathy, which was
present in 14 athletes (figs. 1 and 2; table 2). Each of
these patients had a hypertrophied, nondilated left
ventricle in the absence of another cardiac or systemic
disease that could produce left ventricular hypertrophy (such as valvular, hypertensive or coronary
heart disease or infiltrative cardiomyopathy).11 For
the diagnosis of hypertrophic cardiomyopathy to be
made, each of these patients also had to have at least
one of the following characteristic features of the disease: (1) asymmetric septal hypertrophy (ventricular
septal-to-left ventricular free wall thickness ratio
> 1.3; range 1.3-2.2);1o 12, 13 (2) marked disorganization of cardiac muscle cells in the ventricular septum,7' 14 involving at least 5% of the relevant areas of
the tissue section7; and (3) clinical or echocardiographic evidence of hypertrophic cardiomyopathy
in one or more closely related family members.", 16
Seven of the 14 athletes with hypertrophic cardiomyopathy had both asymmetric septal hypertrophy
and marked ventricular septal disorganization and
three had asymmetric septal hypertrophy without disorganization. The other four athletes had concentric
(symmetric) left ventricular hypertrophy (septal-free
wall ratio < 1.3), including two with marked septal
disorganization and two without disorganization; each
had echocardiographic evidence of hypertrophic cardiomyopathy in relatives.
The heart weights in these 14 patients were all increased
over
normal17 and ranged from 360-630
g
220
CIRCULATION
VOL 62, No 2, AUGUST 1980
1Lnan,neiv2cal
CV Disease,
22
1
Idiopathic
Hypoplastic
Concentric
LVH
Coronaries
~~~
Disease
Ruptured Atherosclerotic Anomalous Hypertrophic
Aorta
Origin of Cardiomyopathy
Coronary
Disease
Left Coronary
Artery
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FIGURE 1. Diagram summarizing the cause of death in 29 competitive athletes. CV= cardiovascular;
L VH = left ventricular hypertrophy.
*Includes one patient who also had anomalous origin of the left coronary arteryfrom the anterior sinus of
Valsalva. The hearts offour other patients in this subgroup were initially referred for evaluation because of
suspected cardiac disease; subsequently, these patients were identified as having been competitive athletes
during life.
tlncludes one patient who had gross and histologic findings at necropsy consistent with mitral valve
prolapse, as well as a family history of that condition. This patient (as well as one other with idiopathic concentric left ventricular hypertrophy) also had marked narrowing of the artery to the atrioventricular node.
(mean 475 g). None of the 12 patients in whom blood
pressure recordings were available had systemic
hypertension. Mild-to-moderate right ventricular dilatation was also present in five patients.
Abnormal intramural coronary arteries (two or
more per tissue section) were identified in the ventricular septal myocardium of four athletes. The abnormal arteries had thickened walls (due to intimal
proliferation or medial hypertrophy or both) and
narrowed lumens.'8 1' One other athlete with hyper-
FIGURE 2. Heart of a 13-year-old male football and
baseball player showing disproportionate thickening of the
ventricular septum (VS) with respect to the posterior left
ventricular free wall (L V). R V = right ventricular wall.
trophic cardiomyopathy showed marked narrowing of
the arteries to the sinoatrial and atrioventricular nodes
due to fibromuscular hyperplasia (figs. 3A-C); the
conduction system was otherwise normal, as were the
other intramural coronary arteries.
Anomalous Origin ofthe Left Coronary Artery
Four athletes had anomalous origin of the left coronary artery from the right (anterior) sinus of
Valsalva,2-4, 20-22 including one of the patients with
hypertrophic cardiomyopathy. Three were 17 years
old and the fourth was 22 years old. In these patients
the left coronary artery made an acute leftward and
posterior angulation from its origin in the right sinus
of Valsalva and followed a course through the narrowed area between the aorta and pulmonary artery
(fig. 4); the left main coronary artery appeared to be
narrowed and obstructed by virtue of its oblique
course. In each of the four patients with anomalous
origin of the left coronary artery, the distribution of
both right and left coronary arteries was normal, and
the entire coronary tree was free of significant
atherosclerosis.
Coronary Heart Disease
Three patients had acquired abnormalities of the
coronary arteries. These patients were 24, 26 and 28
years of age. Two of the three patients showed severe
atherosclerosis in each of the three major extramural
coronary arteries (> 75% cross-sectional area luminal
narrowing by atherosclerotic plaque). One of these
SUDDEN DEATH IN YOUNG ATHLETES/Maron et al.
221
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TABLE 2. Necropsy Findings in 19 Athletes with Hypertrophic Cardiomyopathy or Idiopathic Concentric Left Ventricular Hypertrophy
Ventricular
wall thicknesses
Heart
VS
Age
weight
LVFW¶
Thickened
% VS
ASH in
AML
Pt
(years) Sex
(g)
(mm)
(mm) VS/LVFW VS plaquet
disorganized7 relatives*
Hypertrophic cardiomyopathy
M
SD
21
14
13
450
1.5
0
0
49
+
M
18
DM
14
390
8
2.2
+
+
0
+
MM
M
14
360
18
12
1.5
0
0
53
+
AF
17
F
440
15
8
1.9
0
0
14
+
M
PB
17
530
21
12
1.8
+
0
75
0
M
JG
17
370
16
10
1.6
0
0
49
M
0
JD
17
14
460
21
1.6
+
+
M
17
490
23
18
1.3
0
+
13
+
SWt
M
AJ
19
475
23
20
1.2
+
0
+
+
M
EW
20
630
30
25
1.2
+
+
6
+
22
M
WD
0
89
500
21
0
13
1.6
+
OB
M
23
0
0
500
20
15
1.3
+
+
M
WH
24
0
490
15
15
1.0
0
0
+
KK
30
F
530
17
15
1.1
0
0
24
Idiopathic concentric LVH
M
RS
0
16
440
16
16
1.0
0
0
0
M
GL
16
420
18
18
1.0
0
0
0
0
M
0
KR§
17
530
20
20
1.0
0
0
0
M
BB
0
17
465
23
20
1.2
0
0
+
SC
M
28
0
465
21
19
1.1
0
0
*Echocardiographic identification of a septal-free wall thickness ratio of > 1.3 in at least one first-degree relative of the athlete.
tThickening involving the mural endocardium in left ventricular outflow tract, presumably resulting from contact of the free
edge of the anterior mitral leaflet with the ventricular septum.
tAlso had anomalous origin of the left coronary artery from the anterior sinus of Valsalva.
§Also had gross and histologic findings consistent with mitral valve prolapse, as well as a family history of that disease.
¶Measured behind the midpoint of the posterior mitral leaflet at the level of the inferior margins of the mitral leaflets.
Abbreviations: AML = anterior mitral leaflet; ASH = asymmetric septal hypertrophy; LVH = left ventricular hypertrophy;
LVFW = left ventricular free wall; VS = ventricular septum; VS/LVFW = ventricular septal-to-left ventricular free wall thickness ratio; + = present; 0 = absent;- = data not available.
patients had total occlusion of the right coronary
artery by an antemortem thrombus and hemorrhage
into an atherosclerotic plaque. This athlete, a 28-yearold professional football player, had a large myocardial infarct that was about 2 months old in the
posterior left ventricular wall at necropsy. The other
athlete with severe coronary atheroslcerosis also
showed extensive atherosclerotic plaque in the ascending aorta. There was no evidence of necrosis or scarring in this heart. The remaining patient had about
50% luminal narrowing of the left anterior descending
coronary artery by atherosclerotic plaque and no, or
only minimal, atherosclerosis in each of the other two
major extramural coronary arteries. There was no
myocardial necrosis or scarring. However, the left
anterior descending coronary artery was completely
occluded by an antemortem thrombus 2 cm from the
bifurcation of the left coronary artery. This thrombus
was 1 cm in length and adherent to the underlying
atherosclerotic plaque.
Aortic Rupture
Two athletes (ages 18 and 21 years) died of aortic
rupture, with massive mediastinal hemorrhage. In
each, the ascending aorta was markedly dilated (about
10 cm in diameter) (fig. SA) and had a linear tear in its
wall. In one patient the aortic rupture was associated
with a dissecting aneurysm of the ascending aorta.
Histologic examination of the aortic wall in both
athletes showed markedly diminished numbers of
elastic fibers in the media, compatible with "cystic
medial necrosis" (fig. SB). One of these athletes had
the typical physical stigmata of the Marfan syndrome;
the other athlete was tall (81 inches) and relatively thin
(210 pounds), but did not have the other physical
features of that syndrome.
Patients with Probable Cardiovascular Disease
Six of the 29 athletes had cardiovascular alterations
that were considered probable (but not definitive)
222
VOL 62, No 2, AUGUST 1980
CI RCULATION
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FIGURE 3. Small arteries in the conduction system of two
athletes who died suddenly. (A-C) The artery to the
sinoatrial node of a 24-year-old basketball player with
hypertrophic cardiomyopathy (hematoxylin and eosin
stain). (D and E) Arteries to the atrioventricular node of a
1 7-year-old basketball player with idiopathic concentric left
ventricular hypertrophy (elastic van Gieson stain). (A)
Artery to sinoatrial node has markedly narrowed lumen due
to extreme thickening of the arterial wall (magnification X
95). (B) Same artery as in panel A, but at a different level
and at lower magnification (X 55), showing calcium deposits
in adjacent myocardial fibers (outlined by broken line). (C)
Higher magnification view (X 400) of the calcium-containing fiber shown in panel B. (D) Low-magnification
view (X 40) of the portion of atrioventricular nodal tissue
that penetrates the centralfibrous body. Three distinctly abnormal small arteries are evident (arrows). (E) Highmagnification view (x 130) of one of the vessels shown in
panel D, but at a different level. The lumen is markedly
narrowed due to thickening of the arterial wall.
.!
h
SUDDEN DEATH IN YOUNG ATHLETES/Maron et al.
AORTA
L CIRC.
R.C.A.
PUL. A.
L.AD.
ANOMALOUS ORIGIN LEFT CORONARY
ARTERY FROM RIGHT (ANTERIOR) SINUS
OF VALSALVA
AORTA
L. CIRC.
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R.C.A
IR
C.
PUL. A.
L.A.D.
NORMAL
FIGURE 4. Diagrammatic representation of anomalous
origin of the left coronary artery from the right (anterior)
sinus of Valsalva. The left coronary artery may have a common (or separate) ostia with the right coronary artery that
also arises from the right sinus of Valsalva. Note the acute
leftward and posterior course of the left coronary artery
between the aorta and pulmonary artery. Normal origins of
the left coronary artery from the left sinus of Valsalva and of
the right coronary artery from the right sinus of Valsalva are
shown below for comparison. A = anterior coronary cusp;
L = left coronary cusp; P = posterior (noncoronary) cusp;
L.A.D. left anterior descending coronary artery; L.
CIRC.
left circumflex coronary artery; PUL. A. -
pulmonary artery; R. CA.
=
right coronary artery.
evidence of cardiovascular disease. Five had a hypertrophied, nondilated left ventricle unassociated with a
cardiac lesion that could produce left ventricular
hypertrophy; heart weights were increased over normal'7 and ranged from 420-530 g. However, each of
these five hearts differed from the other hearts in this
study considered to represent hypertrophic car-
FIGURE 5. (A) Posteroanterior chest radiograph obtained
from an 18-year-old male collegiate swimmer with the Marfan syndrome who died 2 months later of a ruptured aorta.
Note prominent dilatation of the ascending aorta. (B)
Histologic section of ascending aorta from the second
patient in this study who died of a ruptured aorta. Note the
markedly diminished numbers of elastic fibers (which stain
darkly) in the media. Intima is at the top and adventitia is at
the bottom. Elastic van Gieson stain; magnification
X
80.
223
224
VOL 62, No 2, AUGUST 1980
CIRCULATION
Normal
Arterial
Supply
Poor
Arterial
Supply
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FIGURE 7. Diagrammatic representation of coronary
arterial distribution to the posterior surface of the heart.
(left) Normal arterial distribution. (right) Markedly
decreased distribution of coronary arterial vessels in a 17year-old female distance runner who died suddenly.
FIGURE 6. Heart of a 17-heart-old soccer player showing
marked concentric (symmetric) thickening of the ventricular
septum (VS) and left ventricular free wall (L V). R V = right
ventricular wall; A V aortic valve.
=
diomyopathy by virtue of the absence of: (1)
asymmetric septal hypertrophy (septal-free wall
ratios ranged from 1.0-1.2) (fig. 6); (2) disorganization of cardiac muscle cells in the ventricular septum;
and (3) clinical or echocardiographic evidence of
hypertrophic cardiomyopathy in closely related family
members.
These five patients with idiopathic concentric left
ventricular hypertrophy ranged in age from 16-28
years. Two were normotensive, but blood pressure
recordings had not been obtained in the other three. In
three of these five patients the degree of left ventricular wall thickening was particularly marked
(average of ventricular septal and posterior left ventricular free wall thickness > 20 mm); in the other two
patients, left ventricular wall thickening was only
moderate (thicknesses of 16 mm and 18 mm) (table 2).
Mild-to-moderate right ventricular dilatation was
present in three of these patients.
Two of the five athletes with idiopathic concentric
left ventricular hypertrophy had associated cardiac
malformations. In one, a 17-year-old football player
with a 530-g heart, the anterior and posterior mitral
leaflets had an appearance consistent with relatively
mild mitral valve prolapse
thickened, gelatinous
and mildly scalloped leaflets with excessive mucoid
-
material, histologically. This patient's mother and two
siblings had clinical or echocardiographic evidence of
mitral prolapse. In addition, this athlete had an
anatomic alteration of the artery to the atrioventricular node, involving severe fibromuscular hyperplasia of the vessel wall and marked narrowing of the
lumen (figs. 3D and 3E). One other athlete with concentric ventricular wall thickening had a similar alteration in the artery to the atrioventricular node. The
conducting tissue was otherwise normal in these latter
two athletes. None of the athletes who had idiopathic
concentric left ventricular hypertrophy, with or
without alterations in the artery to the atrioventricular node, had abnormal intramural coronary arteries
in other areas of ventricular myocardium.
The remaining athlete with probable evidence of
cardiovascular disease was a 17-year-old distance
runner whose heart was of normal weight (280 g),
without luminal narrowing of the extramural coronary
arteries. The left main and left anterior descending
coronary arteries were normal. However, only two
small posterior descending branches to the posterior
left ventricular wall arose from the left circumflex coronary artery. The right coronary artery was short and
small in caliber and it gave off only two small
branches to the posterior wall of right ventricle and
none to the posterior wall of left ventricle (fig. 7).
Hence, the coronary arterial distribution to the
posterior wall of both ventricles was diminished.
Clinical Findings: Suspicion of
Cardiovascular Disease During Life
Of the 29 athletes, 21 had been entirely asymptomatic, even upon retrospective questioning of
closely related family members. The remaining eight
athletes had transient symptoms that may have been
due to cardiac disease, including syncope in three,
presyncope in one (a single episode 2 months before
SUDDEN DEATH IN YOUNG ATHLETES/Maron et al.
225
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TABLE 3. Findings in Seven Competitive Athletes in Whom Cardiovascular Disease Was Suspected or Identified During Life
Reason
disease
Age
first
Clincal
Necropsy
Cardiac cath
ECG
Patient (years) Sex suspected
diagnosis
diagnosis
14
M Syncope
WPW pattern; LAD;
Mild bilateral
DM
WPW syndrome
Hypertrophic
PA branch
T-wave abn. I, aVL,
cardiomyopathy
stenosis
V4-Ve; LVH
M Family
14
MM
LVH with "strain";
Rest LVOT grad. Hypertrophic
Hypertrophic
= 15 mm Hg;
history
Q waves II, III,
cardiomyopathy
cardiomyopathy
aVF, Ve
LVEDP = 24
mm Hg
M Heart
Q waves III, aVF,
None
VSD
17
JG
Hypertrophic
murmur
V5, VB; - LVH
cardiomyopathy
M
for
Marfan
SS
18
Exam
Normal
None
syndrome; Ruptured ascendMarfan
AR
ing aorta
syndrome
M Heart
20
EW
None
Normal athlete's
Deep, symmetric
Hypertrophic
T-wave inversion II,
murmur
heart
cardiomyopathy
III, aVF, Vs-V6; LVH
23
M VT on
Rest LVOT grad. Normal athlete's
OB
Deep, symmetric
Hypertrophic
= 0; LVEDP
routine
T-wave inversion I,
heart
cardiomyopathy
= 5 mm Hg;
exercise
II, III, aVF, V4-V6;
LVH*
LV cavity
test
oblteration
(EF
=
95%)
Rest LVOT grad. Normal athlete's
Hypertrophic
= 0; LVEDP
heart
cardiomyopathy
= 10 mm Hg
*Initially this patient underwent a treadmill exercise ECG as part of the preparticipation examination for his university basketball team. During exercise, ST-segment depression of 2 mm with negative slope and frequent premature ventricular complexes
were present. During the second minute of recovery, a 4-second period of ventricular tachycardia occurred (fig. 8). A subsequent
24-hour ambulatory ECG showed only occasional premature ventricular complexes and episodes of junctional rhythm; a second
24-hour ECG recorded during a basketball scrimmage showed no arrhvthmia.
Abbreviations: AR = aortic regurgitation; abn. = abnormality; cath = catheterization; EF = ejection fraction; grad. =
gradient; LAD = left-axis deviation; LV = left ventricular; LVEDP left ventricular end-diastolic pressure; LVH = left
ventricular hypertrophy; LVOT = left ventricular outflow tract; PA = pulmonary artery; WPW = Wolff-Parkinson-White
syndrome; VSD = ventricular septal defect; VT = ventricular tachycardia; t
probable.
KK
30
F
Mild
fatigue
LVH with "strain";
diffuse T-wave abn.
=
death), chest pain in two, periodic mild fatigue in one,
and mild fatigue, presyncope and palpitations in one.
In two athletes with transient symptoms, as well as
in five other asymptomatic athletes, cardiovascular
disease had been suspected by an examining physician
during life (table 3). In the latter five athletes, the
suspicion of cardiovascular disease initially arose
because of a heart murmur in two, a family history of
heart disease in one,5 identification of ventricular
tachycardia on an exercise ECG performed as a
routine part of a preparticipation athletic examination
in one (fig. 8B), and during evaluation for the Marfan
syndrome in one.
Six of the seven athletes in whom cardiovascular
disease was suspected during life had hypertrophic
cardiomyopathy confirmed at necropsy. However, in
only one of those six athletes with hypertrophic cardiomyopathy was the correct diagnosis made
clinically. In the other five athletes, the diagnosis
made during life was "normal athlete heart" in three,
ventricular septal defect in one and Wolff-ParkinsonWhite syndrome in one. Each of the latter five athletes
with hypertrophic cardiomyopathy had a distinctly
abnormal ECG (figs. 8A and 9). Two athletes with abnormal ECGs also underwent cardiac catheterization;
neither had a left ventricular outflow gradient under
basal conditions. (Provocative interventions were not
performed.) These findings led to the erroneous conclusion that hypertrophic cardiomyopathy was absent,
even though one of these athletes also had a markedly
hyperdynamic left ventricle (fig. 8C). The seventh
athlete had been identified as having the Marfan syndrome with aortic root dilatation (fig. 4A) and aortic
regurgitation during life; he had been advised not to
compete in intercollegiate sports, but died of a ruptured aorta 2 months later during swimming practice.
In the remaining 22 athletes there had been no
suspicion of cardiovascular disease during life.
However, clinical data in two suggested the presence
of coronary heart disease, even though it was not identified until necropsy. One of these two athletes was a
28-year-old professional football player who had an
abnormally elevated serum cholesterol (350 mg%;
normal < 280 mg%), as well as a family history
of premature coronary heart disease and death,
identified at a routine preparticipation examination
for professional athletes. Subsequently, type II
hyperlipoproteinemia was documented in two surviving first-degree relatives. Upon retrospective
analysis of the athlete's medical history, it was ap-
226
CIRCULATION
11
I
-.
..
..
V,
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VOL 62, No 2, AUGUST 1980
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Cont.
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O.B.
10/14/74
FIGURE 8. Electrocardiographic and angiographic finding.v in a 23-year-old collegiate basketball player (O.B.) in
whom the diagnosis of hypertrophic cardiomyopathy was
made at necropsy. (A) Standard 12-lead ECG obtained under basal conditions showing marked symmetric T-wave inversion (as much as 15 mm in depth), as well as left ventricular hypertrophy. (B) Four-second period of ventricular
tachycardia that occurred in the second minute of recovery
after a routine treadmill exercise test and terminated spontaneously. (C) Left ventricular angiocardiogram in diastole
(top) and end-systole (C1) showing marked cavity obliteration (ejection fraction of 95%). LV - left ventricular cavity.
The ECGs have been retraced for clarity.
parent that he had experienced symptoms compatible
with myocardial infarction about 45 days before death
(which was documented at necropsy), and frequent
episodes of chest pain with exertion thereafter. During
life, the acute myocardial infarction and chest pains
had not been considered evidence of heart disease, but
rather manifestations of a traumatic injury. An ECG
recorded before the acute myocardial infarction (the
only one obtained from this patient) was normal. A
second athlete who died of severe coronary atherosclerosis had an abnormal ECG and elevated serum
cholesterol (380 mg%) identified at a preparticipation
athletic examination, but no further diagnostic evaluation was undertaken.
Discussion
This study shows that most sudden and unexpected
deaths in young, competitive athletes are due to car-
c
diovascular disease. In 28 of the 29 athletes, a structural cardiovascular abnormality was identified at
necropsy, and in 22 athletes it was almost certainly
responsible for their sudden death. Although the
etiology of sudden death in one patient without structural cardiac disease is unknown, it is possible that a
primary rhythm disturbance was responsible.
While a wide variety of cardiovascular malformations (primarily congenital) was identified in our 29
athletes, the most frequently encountered disease was
hypertrophic cardiomyopathy, a condition known to
be responsible for sudden death in young, asymptomatic subjects.5 6,23,24 Although this disease accounted for almost one-half of the deaths in the present series, our data cannot be used to define precisely
the prevalence with which different diseases cause
sudden death in young athletes. First, our series is
relatively small, and cannot be assumed to be an en-
227
SUDDEN DEATH IN YOUNG ATHLETES/Maron et al.
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K.K.
FIGURE 9. ECGs showing the spectrum of abnormalities from four athletes who were identified as having
hypertrophic cardiomyopathy at necropsy. Although cardiovascular disease was suspected in each athlete
during life, another clinical diagnosis had been made in each. (top left) From a 14-year-old wrestler (D.M.)
showing Wolff-Parkinson- White pattern, left-axis deviation, diffuse T-wave inversion andflattening in leads
I, aVL and V4-V6, andprobable left ventricular hypertrophy. (top right) From a 17-year-oldfootballplayer
(J. G.) showing deep Q waves in leads III, aVF, V, and VB, and probable left ventricular hypertrophy. (bottom
left) From a 20-year-old basketball player (E. W.) showing deep symmetric T-wave inversion in leads II, III,
aVF and V-V6, and left ventricular hypertrophy. Compare with a similar ECG from another athlete shown
in figure 8. (bottom right) From a 30-year-old tennis player (K.K.) showing left ventricular hypertrophy with
"strain" and diffuse T-wave flattening and inversion. The ECGs have been retraced for clarity.
tirely representative sampling of sudden death in
athletes. Second, unavoidable biases, intrinsic to our
study design, may have influenced the selection of subjects for this investigation. For example, athletes with
unequivocal cardiac disease recognized at necropsy
may have been preferentially referred to the NHLBI
and the Armed Forces Institute of Pathology.
However, 17 of 29 subjects were obtained by follow-up
of news media reports describing sudden death in
athletes. Hence, most patients in this series were identified initially as competitive athletes who had died
suddenly, and not as patients with heart disease who
subsequently proved to have been athletes. Even
when this latter segment of our patient population was
considered separately, our conclusions were similar to
those from the entire study population. For example,
eight of the 17 athletes initially identified through the
news media had hypertrophic cardiomyopathy, compared with 14 of the 29 athletes in the overall study
were
group.
The fact th4t we chose to limit our investigation to
competitive athletes, who were necessarily relatively
228
CIRCULATION
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young, also importantly influenced the relative
prevalence of cardiovascular diseases found. In such
young athletes, atherosclerotic coronary disease
would be expected to be an infrequent cause of death.
Conversely, had we studied recreational athletes over
the age of 30 years at death, the frequency of coronary
heart disease would surely have been much higher.
Certain cardiovascular diseases, such as valvular
heart disease, coarctation of the aorta, fixed subvalvular aortic stenosis or other acyanotic or cyanotic
heart malformations, did not appear in our series of
athletes. Such lesions would likely have been identified
earlier in life due to the presence of a loud heart murmur or other obvious physical findings and, hence,
before participation in competitive athletics had
begun. Other known causes of sudden death, such as
prolonged QT-interval syndrome, probably did not
appear in our series due to their relatively low
prevalence in the population.
Cardiovascular disease was unrecognized during life
in most of our athletes, and suspected clinically in only
seven of the 29. In only two of these seven athletes was
the correct diagnosis established during life: one with
obvious stigmata of the Marfan syndrome and the second in whom hypertrophic cardiomyopathy was identified after his brother had died suddenly of that disease. The five other athletes in whom cardiac disease
was suspected clinically all died of hypertrophic cardiomyopathy. All five of these athletes had distinctly
abnormal ECGs and one had an abnormal left ventricular angiocardiogram. Thus, it is likely that if
high-quality echocardiograms had been obtained in
these athletes, the correct diagnosis of hypertrophic
cardiomyopathy would have been made during life.
Each of these five athletes, after examination for
possible heart disease, were permitted by their examining physician to continue participation in competitive athletics and each subsequently died on the
practice field or during an athletic contest.
The five athletes who had concentric (symmetric)
left ventricular hypertrophy without ancillary evidence
of a primary, genetically transmitted cardiomyopathy
represent a diagnostic dilemma. The significance of
the ventricular hypertrophy in these patients is unclear. First, we cannot exclude the possibility that the
increased cardiac mass identified at necropsy
represented only the "physiologic" hypertrophy that
would be expected in many highly conditioned competitive athletes.25 SO Indeed, in two of these athletes,
the degree of left ventricular wall thickening was consistent with that usually present in actively competing
athletes. However, in the other three athletes with
idiopathic concentric hypertrophy, the magnitude of
left ventricular wall thickening (> 20 mm) clearly exceeded that which would appear to be "physiologic"
hypertrophy, even after making reasonable allowances
for known discrepancies between ventricular wall
thicknesses assessed by echocardiography and at
necropsy.31 Second, systemic hypertension could not
be definitely excluded as the cause of left ventricular
hypertrophy in three patients because blood pressure
had not been recorded during life; however, two of
VOL 62, No 2, AUGUST 1980
these three were less than 20 years old at death, and it
is unlikely that hypertension played an etiologic role
in their disease process.
In two athletes with idiopathic concentric left ventricular hypertrophy, associated abnormalities (which
may have been primary or contributing factors in their
sudden deaths) also complicate interpretation of the
significance of the cardiac hypertrophy found in this
subgroup. One of these athletes had, at necropsy,
alterations of the mitral valve leaflets consistent with
mitral valve prolapse and a family history of that disease. The abnormality of the mitral valve in this
patient was relatively mild and therefore was probably
not responsible for significant mitral regurgitation or
the degree of left ventricular hypertrophy that was
present. In addition, this athlete and one other with
idiopathic concentric hypertrophy had severe narrowing of the artery to the atrioventricular node. Abnormal small intramural arteries in the atrioventricular
node (as well as in the sinoatrial node), morphologically similar to those present in our patients,
have been described in young, healthy subjects32' 33 or
in patients with hypertrophic cardiomyopathy34 who
died suddenly, as well as in patients with a variety of
other cardiac or systemic diseases.35 Unlike the findings in our athletes, the small-vessel abnormalities
described in these reports were usually associated with
significant fibrosis of the conducting tissue.
Our findings raise questions regarding the prospective identification of potentially lethal cardiovascular
diseases in competitive athletes during life. Screening
of athletes by personal and family history, physical examination, ECG and echocardiogram would have
identified most of the athletes in our study group.
However, routine comprehensive screening of this
type would probably be impractical. Although screening by personal history and physical examination
alone would identify many of the more obvious cardiovascular abnormalities (such as systemic hypertension or aortic valvular stenosis), it would be relatively
insensitive for detecting other diseases. For example,
the most frequent cause of death in this series, hypertrophic cardiomyopathy, is usually not associated with
a loud heart murmur,36" 37 or even always with an abnormal ECG38 when present in its nonobstructive
form. Definitive identification of hypertrophic cardiomyopathy without obstruction could be made noninvasively in athletes only by echocardiography.
Similarly, echocardiography could identify many of
the patients with aortic root dilatation who may be at
high risk of aortic rupture.
The data in this study do not provide definitive information regarding the feasibility of screening programs for detecting cardiovascular disease in competitive athletes. However, the basic knowledge and
awareness of the diseases that may cause sudden death
in athletes help to create the groundwork necessary for
the initiation of studies that will provide such answers.
References
1. James TN, Froggatt P, Marshall TK: Sudden death in
athletes. Ann Intern Med 67: 1013, 1967
young
SUDDEN DEATH IN YOUNG ATHLETES/Maron et al.
Downloaded from http://circ.ahajournals.org/ by guest on June 18, 2017
2. Cheitlin MD, De Castro CM, McAllister HA: Sudden death as
a complication of anomalous left coronary origin from the
anterior sinus of Valsalva. A not-so-minor congenital anomaly.
Circulation 50: 780, 1974
3. Jokl E, McClellan JT, Williams WC, Gouze F, Bartholomew
R: Congenital anomaly of left coronary artery in a young
athlete. Cardiologia 49: 253, 1966
4. Jokl E, McClellan JT, Ross GD: Congenital anomaly of left
coronary artery in a young athlete. JAMA 182: 572, 1962
5. Maron BJ, Lipson LC, Roberts WC, Savage DD, Epstein SE:
"Malignant" hypertrophic cardiomyopathy: identification of a
subgroup of families with unusually frequent premature deaths.
Am J Cardiol 41: 1133, 1978
6. Maron BJ, Roberts WC, Edwards JE, McAllister HA, Foley
DD, Epstein SE: Sudden death in patients with hypertrophic
cardiomyopathy: characterization of 26 patients without
previous functional limitation. Am J Cardiol 41: 803, 1978
7. Maron BJ, Roberts WC: Quantitative analysis of cardiac muscle cell disorganization in the ventricular septum of patients
with hypertrophic cardiomyopathy. Circulation 59: 689, 1979
8. Lev M, Widran J, Erickson EE: A method for the
histopathologic study of the atrioventricular node, bundle, and
branches. Arch Pathol 52: 73, 1951
9. Lev M, Watne AL: Method for routine histopathologic study of
human sinoatrial node. Arch Pathol 57: 168, 1954
10. Henry WL, Clark CE, Epstein SE: Asymmetric septal hypertrophy (ASH): echocardiographic identification of the
pathognomonic anatomic abnormality of IHSS. Circulation
47: 225, 1973
11. Maron BJ, Epstein SE: Hypertrophic cardiomyopathy: a discussion of nomenclature. Am J Cardiol 43: 1242, 1979
12. Roberts WC: Valvular, subvalvular and supravalvular aortic
stenosis: morphologic features. Cardiovasc Clin 5: 104, 1973
13. Menges H, Brandenburg RO, Brown AL: The clinical,
hemodynamic and pathologic diagnosis of muscular subvalvular aortic stenosis. Circulation 24: 1126, 1961
14. Teare D: Asymmetrical hypertrophy of the heart in young
patients. Br Heart J 20: 1, 1958
15. van Dorp WG, ten Cate FJ, Vletter WB, Dohmen H, Roelandt
J: Familial prevalence of asymmetric septal hypertrophy. Eur J
Cardiol 4: 349, 1976
16. Clark CE, Henry WL, Epstein SE: Familial prevalence and
genetic transmission of idiopathic hypertrophic subaortic
stenosis. N Engl J Med 289: 709, 1973
17. Gould SE: Pathology of the Heart and Blood Vessels, 3rd ed.
Springfield, Illinois, Charles C Thomas, 1968, p 1139
18. McReynolds RA, Roberts WC: The intramural coronary
arteries in hypertrophic cardiomyopathy. (abstr) Am J Cardiol
35: 154, 1975
19. James TN: Pathology of small coronary arteries. Am J Cardiol
20: 679, 1967
20. Benson PA: Anomalous aortic origin of coronary artery with
sudden death: case report and review. Am Heart J 79: 254, 1970
21. Benson PA, Lack AR: Anomalous aortic origin of left coronary
229
artery. Arch Pathol 86: 214, 1968
22. Cohen LS, Shaw LD: Fatal myocardial infarction in an 11year-old boy associated with a unique coronary artery anomaly.
Am J Cardiol 19: 420, 1967
23. Lambert EC, Menon VA, Wagner HR, Vlad P: Sudden unexpected death from cardiovascular disease in children. Am J
Cardiol 34: 89, 1974
24. Fiddler GI, Tajik AJ, Weidman WH, McGoon DC, Ritter DG,
Giuliani ER: Idiopathic hypertrophic subaortic stenosis in the
young. Am J Cardiol 42: 793, 1978
25. Parker BM, Londeree BR, Cupp GV, Dubiel JP: The noninvasive cardiac evaluation of long-distance runners. Chest 73:
376, 1978
26. Roeske WR, O'Rourke RA, Klein A, Leopold G, Karliner JS:
Noninvasive evaluation of ventricular hypertrophy in
professional athletes. Circulation 53: 286, 1976
27. Allen HD, Goldberg SJ, Sahn DJ, Schy N, Wojcik R: A quantitative echocardiographic study of champion childhood
swimmers. Circulation 55: 142, 1977
28. Morganroth J, Maron BJ, Henry WL, Epstein SE: Comparative left ventricular dimensions in trained athletes. Ann
Intern Med 82: 521, 1975
29. Gilbert CA, Nutter DO, Felner JM, Perkins JV, Heymsfield
SB, Schlant RC: Echocardiographic study of cardiac dimensions and function in the endurance-trained athlete. Am J Cardiol 40: 528, 1977
30. Ikaheimo MJ, Palatsi IJ, Takkunen JT: Noninvasive evaluation of the athletic heart: sprinters versus endurance runners.
Am J Cardiol 44: 24, 1979
31. Maron BJ, Henry WL, Roberts WC, Epstein SE: Comparison
of echocardiographic and necropsy measurements of ventricular wall thicknesses in patients with and without disproportionate septal thickening. Circulation 55: 341, 1977
32. James TN, Armstrong RS, Silverman J, Marshall TK: De subitaneis mortibus. VI. Two young soldiers. Circulation 49:
1239, 1974
33. James TN, Hackel DB, Marshall TK: De subitaneis mortibus.
V. Occluded A-V node artery. Circulation 49: 772, 1974
34. James TN, Marshall TK: De subitaneis mortibus. XII.
Asymmetrical hypertrophy of the heart. Circulation 51: 1149,
1975
35. James TN: An etiologic concept concerning the obscure
myocardiopathies. Prog Cardiovasc Dis 7: 43, 1964
36. Epstein SE, Henry WL, Clark CE, Roberts WC, Maron BJ,
Ferrans VJ, Redwood DR, Morrow AG: Asymmetric septal
hypertrophy. Ann Intern Med 81: 650, 1974
37. Braunwald E, Lambrew CT, Rockoff SD, Ross J Jr, Morrow
AG: Idiopathic hypertrophic subaortic stenosis. I. A description of the disease based upon an analysis of 64 patients. Circulation 30 (suppl IV): IV-3, 1964
38. Savage DD, Seides SF, Clark CE, Henry WL, Maron BJ,
Robinson FC, Epstein SE: Electrocardiographic findings in
patients with obstructive and nonobstructive hypertrophic cardiomyopathy. Circulation 58: 402, 1978
Sudden death in young athletes.
B J Maron, W C Roberts, H A McAllister, D R Rosing and S E Epstein
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Circulation. 1980;62:218-229
doi: 10.1161/01.CIR.62.2.218
Circulation is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
Copyright © 1980 American Heart Association, Inc. All rights reserved.
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