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CLINICAL STUDIES

Clinical profile of congenital coronary artery anomalies with origin from the wrong aortic sinus leading to sudden death in young competitive athletes

Cristina Basso, MD, PhD^*, Barry J. Maron, MD, FACC, Domenico Corrado, MD and Gaetano Thiene, MD^*

^* Department of Pathology, University of Padua Medical School, Padua, Italy
Department of Cardiology, University of Padua Medical School, Padua, Italy
Minneapolis Heart Institute Foundation, Minneapolis, Minnesota, USA

Manuscript received October 1, 1999; revised manuscript received November 16, 1999, accepted January 7, 2000.

Reprint requests and correspondence: Dr. Cristina Basso, Cardiovascular Pathology, University of Padua Medical School, Via A. Gabelli, 61, Padua, Italy

	Abstract

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OBJECTIVES

The purpose of this study is to characterize the clinical profile and identify clinical markers that would enable the detection during life of anomalous coronary artery origin from the wrong aortic sinus (with course between the aorta and pulmonary trunk) in young competitive athletes.

BACKGROUND

Congenital coronary artery anomalies are not uncommonly associated with sudden death in young athletes, the catastrophic event probably provoked by myocardial ischemia. Such coronary anomalies are rarely identified during life, often because of insufficient clinical suspicion. However, since anomalous coronary artery origin is amenable to surgical treatment, timely clinical identification is crucial.

METHODS

Because of the paucity of available data characterizing the clinical profile of wrong sinus coronary artery malformations, we reviewed two large registries comprised of young competitive athletes who died suddenly, assembled consecutively in the U.S. and Italy.

RESULTS

We reported 27 sudden deaths in young athletes, identified solely at autopsy and due to either left main coronary artery from the right aortic sinus (n = 23) or right coronary artery from the left sinus (n = 4). Each athlete died either during (n = 25) or immediately after (n = 2) intense exertion on the athletic field. Fifteen athletes (55%) had no clinical cardiovascular manifestations or testing during life. However, in the remaining 12 athletes (45%) aged 16 ± 7, certain clinical data were available. Premonitory symptoms had occurred in 10, including syncope in four (exertional in three and recurrent in two, 3 to 24 months before death) and chest pain in five (exertional in three, all single episodes, 24 months before death). All cardiovascular tests were within normal limits, including 12-lead electrocardiogram (ECG) pattern (in 9/9), stress ECG with maximal exercise (in 6/6) and left ventricular wall motion and cardiac dimensions by two-dimensional echocardiography (in 2/2).

CONCLUSIONS

With regard to congenital coronary artery anomalies of wrong aortic sinus origin in young competitive athletes, 1) standard testing with ECG under resting or exercise conditions is unlikely to provide clinical evidence of myocardial ischemia and would not be reliable as screening tests in large athletic populations, 2) premonitory cardiac symptoms not uncommonly occurred shortly before sudden death (typically associated with anomalous left main coronary artery), suggesting that a history of exertional syncope or chest pain requires exclusion of this anomaly. These observations have important implications for the preparticipation screening of competitive athletes.

Abbreviations and Acronyms   ECG = electrocardiogram   LMCA = left main coronary artery   RCA = right coronary artery

While hypertrophic cardiomyopathy or arrhythmogenic right ventricular cardiomyopathy have been the most common diseases in these surveys, a variety of congenital coronary artery anomalies (particularly those with wrong sinus origin) also consistently represent common causes of exercise-related sudden death in young athletes 35 years of age (3–5,8–10). The mechanism of sudden death is believed to be episodic myocardial ischemia (11–16). Nevertheless, these coronary anomalies are amenable to surgical correction (17), thereby emphasizing the crucial importance of timely identification during life. However, at present, there is a paucity of clinical information available in the literature regarding trained athletes with these coronary malformations. Therefore, we have reviewed two large registries of young competitive athletes who had died suddenly, to systematically analyze clinical markers that would promote detection during life of coronary artery anomalies of wrong aortic sinus origin.

	Methods

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Selection of subjects.   Cases of sudden death in competitive athletes resulting from coronary artery anomalies with wrong aortic sinus origin were retrospectively assembled based on the review of two large registries in the U.S. and Italy. First, since 1990, the Minneapolis Heart Institute Foundation has developed a U.S.-based registry of sudden cardiovascular deaths in young competitive athletes (6), consecutively identified (largely from news media accounts) and tracked in a systematic fashion.

Second, since 1979, a clinicopathologic target project on sudden death in the young has been carried out in the Veneto region of northeastern Italy (including the cities of Venice, Padova, Treviso, Verona and Vicenza), which has a population of over four million (10). All hearts from cases of sudden death in young people (including athletes) in this geographic region are systematically assessed at the University of Padova.

Inclusion criteria.   For inclusion into the study group, each patient fulfilled the following criteria (6,10): 1) a diagnosis at autopsy of congenital coronary anomaly of wrong aortic sinus origin—with an absence of other cardiac and noncardiac causes of death—based either on direct examination of the heart or analysis of a complete and detailed autopsy report; 2) a competitive athlete at the time of death—one who participated in an organized team or individual sport that required systematic training and regular competition against others and that placed a high premium on athletic excellence and achievement (18); 3) an age of 35 years at time of death; and 4) no evidence of drug or alcohol abuse upon the postmortem toxicologic examination of blood and urine.

Clinical information.   Clinical data reported here were derived differently from the U.S. and Italian registries. Among U.S. athletes, medical evaluation and testing were stimulated by symptoms suggestive of cardiac disease and were not part of systematic preparticipation screening programs.

Italian athletes were clinically evaluated as part of the longstanding and systematic national preparticipation screening program for competitive athletes (10). Standard 12-lead electrocardiograms (ECGs) and limited exercise testing (step test) are routinely obtained as part of this program. Other cardiovascular testing, including maximal exercise stress ECG, may be obtained if judged to be clinically indicated. Myocardial perfusion imaging was not part of the evaluation of any patients in this study.

Statistical analysis.   Continuous variables are expressed as mean ± SD. Chi-square or Fisher exact test were used to assess the significance of differences between subgroups. Two-tailed p values <0.05 were regarded as statistically significant.

	Results

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Study patients.   Twenty-seven competitive athletes comprised this study group by virtue of sudden cardiac death from a congenital coronary anomaly characterized by wrong aortic sinus origin (and course between the aorta and pulmonary trunk). These coronary anomalies included origin of the left main coronary artery (LMCA) from the right aortic sinus (n = 23) and origin of the right coronary artery (RCA) from the left sinus (n = 4).

Demographics.   Of the 27 athletes, 22 were men and 5 were women; ages ranged from 9 to 32 years (mean 16 ± 5). Racial distribution was 16 whites (60%), 9 African Americans (33%) and 2 Asians (7%). Most athletes were competing either in junior high school (12; 44%) or high school (11; 41%); the remainder were professional (n = 3) or collegiate (n = 1) athletes. The athletes had participated in a variety of sports: basketball (n = 8), soccer (n = 7), football (n = 3), track-sprinting (n = 2), distance running (n = 2), as well as ice hockey, rugby, softball, cross-country and swimming (one each).

Each athlete died during (n = 25) or after (n = 2) intense exertion on the athletic field; 16 died during training, and 11 during organized competition. In 12 athletes (44%) the physical effort immediately before death was not only strenuous but also continuous and prolonged (>30 min). Nineteen of the 27 sudden deaths (70%) were clustered between 3 PM and 9 PM, corresponding to the peak time for participation in most competitive sports; only eight deaths (29%) occurred during the remaining 18 h of the day.

Clinical data.   Of the 27 athletes, 15 had no clinical manifestations or testing performed (Table 1, Fig. 1); however, clinical information was available for the remaining 12 patients (Table 2). These two groups did not substantially differ with respect to demographic parameters (Table 1).

View larger version (27K): [in this window] [in a new window]   Figure 1 Flow-chart showing clinical data available and findings in the present study group of athletes who died of wrong aortic sinus coronary artery anomalies.

Episodes of chest pain (either typical or atypical of angina) had occurred in five athletes, including three during physical exertion. Each of these athletes experienced single episodes, which occurred a few days to 24 months before death. Two other athletes reported palpitations unrelated to physical activity, and one other experienced dizziness and palpitations with exertion. None of the athletes with symptoms had a family history of premature sudden cardiac death or cardiovascular disease.

Clinical testing
Standard 12-lead ECGs were performed at rest in nine athletes, 6 to 18 months (mean 11 ± 3) before their sudden deaths. Electrocardiogram patterns, including voltages, intervals and T wave morphology, were within normal limits for each (Fig. 2A). Two of these athletes, however, had isolated (one and two) premature ventricular complexes.

View larger version (80K): [in this window] [in a new window]   Figure 2 A 15-year-old male Italian soccer player with a history of exertional syncope one year before death who died suddenly while running during the second half of a game. (A) A 12-lead ECG performed 10 months before death, as part of routine preparticipation screening, is within normal limits. (B) View of the aortic root; RCA arises normally from the right aortic sinus (arrow), and the LMCA arises anomalously from the right sinus with an acute angle take-off producing a slit-like lumen (arrowhead).

A two-dimensional echocardiogram was performed in two athletes and was normal with regard to left ventricular thickness and cavity dimension as well as segmental and global wall motion. These echocardiograms had not been interpreted prospectively with regard to coronary artery origin from the aorta.

When clinical and demographic variables were compared for athletes with an anomalous LMCA or an anomalous RCA, a statistically significant difference between the two subgroups was evident with respect to the prior occurrence of the major symptoms of syncope and chest pain (p = 0.04), which occurred exclusively in patients with an anomalous LMCA.

	Pathologic findings

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Each heart was characterized by both an acute angled take-off of the anomalous coronary artery, with a slit-like lumen at its point of origin from the wrong aortic sinus, and a proximal course between the aorta and pulmonary trunk (Fig. 2B). Heart weights were 240 to 410 g (mean 312 ± 87). Atherosclerotic narrowing of the major extramural coronary arteries (>50% of the cross-sectional area) was absent. Only one heart showed gross evidence of myocardial scarring suggestive of prior infarction.

Heart specimens were available for reexamination in 6 of the 27 athletes (all Italian), including three with anomalous LMCA and three with anomalous RCA. In three of these hearts, based on histologic examination, the course of the proximal portion of the anomalous coronary artery (LMCA in two, RCA in one) was documented to be intramural, i.e., contained completely within the aortic wall (Fig. 3, A and B), so that the coronary artery and the aorta shared the same media without an interpositioned adventitia. In addition, in each of the six hearts, the region of myocardium supplied by the anomalous coronary artery showed evidence of acute ischemia with contraction band necrosis, wavy fibers and early neutrophilic infiltrate (Fig. 3C), and focal evidence of chronic myocardial ischemic damage with patchy replacement-type fibrosis was present in three (Fig. 3D).

View larger version (78K): [in this window] [in a new window]   Figure 3 From the same Italian soccer player shown in Figure 2, with anomalous left main coronary artery (LMCA) and intramural course. (A) Transverse section of the aortic root at the commissural level. The anomalous LMCA shows an intramural aortic course just behind the commissure between the two coronary cusps. (B) Panoramic histology showing that the LMCA, which arises from the right sinus (RS) instead of from the left sinus (LS), and the aorta share the same media without an interpositioned adventitia, accounting for a collapsed coronary lumen (Weigert van Gieson stain, x3) (C = commissure). (C) Histologic section of the region of left ventricular myocardium supplied by the anomalous LMCA showing diffuse myocyte necrosis and neutrophilic infiltrates (Haematoxylin-Eosin stain, x240). (D) Multiple patchy areas of replacement-type fibrosis that stain blue are diffusely distributed throughout the myocardium (Heidenhain trichrome stain, x30).

	Discussion

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Among the congenital coronary malformations, coronary artery origin from the wrong aortic sinus (coursing between aorta and pulmonary trunk) appears to be the most common in young trained athletes dying suddenly. Indeed, we have previously reported that these malformations are associated with sudden death more commonly in competitive athletes than in non-athletes (10).

However, these anomalies are rarely suspected or identified during life and are usually first recognized at autopsy, largely because there is insufficient clinical suspicion as well as the difficulties implicit in routine examination or clinical testing for these malformations (10,20,21). Consequently, such coronary anomalies are not recognized during routine preparticipation screening (10,22,23). Therefore, we thought it would be important to develop a clinical profile and assess the utility of noninvasive testing in young competitive athletes who had died suddenly with anomalous coronary artery origin from the wrong aortic sinus. Previously published descriptions are largely represented by anecdotal case reports. Thus, we believe this study is unique because it represents the first consecutive series of young athletic field deaths due to these coronary malformations in which it is possible to systematically assemble clinical data collected during life.

Premonitory symptoms.   Premonitory symptoms occurred not uncommonly during life among our study patients (in about one third). Syncope or chest pain occurred in seven athletes within 24 months of sudden death. In our athlete series, these major symptoms were limited to anomalous LMCA origin, while anomalous origin of the RCA proved to be clinically silent. Other authors have, however, reported a few patients with anomalous RCA who experienced either angina or syncope before death (24,25). Therefore, although sudden death is frequently the first manifestation in patients with wrong sinus coronary artery origin, premonitory symptoms occur in a substantial proportion of these individuals (20). In both types of wrong sinus coronary artery anomalies described here, the vast majority of clinical events were related to exertion. These observations emphasize the pressing need to raise the index of clinical suspicion in an effort to identify during life any wrong aortic sinus coronary artery origin in young, physically active individuals (10).

Efficacy of ECG testing.   In the present retrospective study of trained athletes, we showed that neither routine 12-lead ECG nor exercise stress tests were particularly informative for the diagnosis of congenital coronary anomalies. In particular, each of the nine ECGs recorded under resting conditions were within normal limits. These findings in our series of patients are consistent with that of several case reports in which an ECG was recorded (unassociated with symptoms) (21). In addition, exercise ECGs were available in six of our athletes, and each was within normal limits. In a review of the literature, we found 18 young patients (35 years) with wrong aortic sinus coronary artery anomaly and reported exercise stress test findings (Table 3), of whom only three were competitive athletes (11,14,26–38). A positive stress test ECG was present in only four of the 18 patients (22%), including two who were symptomatic (but none of the athletes). Thus, a negative even maximal-effort stress ECG does not exclude a potentially lethal coronary anomaly.

View this table: [in this window] [in a new window]   Table 3 Previously Published Reports of Wrong Sinus Coronary Artery Anomalies in Persons Aged 35 Years in Whom ECG Data Were Available

Strategies for clinical identification.   On the basis of our findings, preparticipation screening, whether confined to standard history and physical examination or including 12-lead or exercise ECG (as is the practice in Italy), is limited in its power to identify coronary artery anomalies in young competitive athletes (10,22). Indeed, these lesions usually can be suspected only by prior symptoms such as syncope and angina, particularly if they occur during or immediately after exertion. Our observation that all 12-lead and exercise ECGs were within normal limits would seem to suggest that these tests are unlikely to provide clinical evidence of myocardial ischemia resulting from anomalous coronary artery origin, and they are therefore unreliable for clinical recognition of these coronary anomalies at preparticipation screening of competitive athletes (10).

A strategy for clinical identification of wrong sinus coronary artery anomalies in young athletes could be summarized as follows. If the index of suspicion is sufficiently high because of the presence of potential clinical markers such as exertional syncope or chest pain (even in the setting of both a normal 12-lead ECG and maximal exercise test), the anatomy of these malformations can be suspected or defined noninvasively by transthoracic or transesophageal echocardiography. Pelliccia et al. (41) demonstrated that echocardiographic imaging of left and right coronary arteries is feasible and reliable in a substantial proportion of young athletes (about 95%). Therefore, the failure to demonstrate that both the proximal left and right coronary arteries actually originate from their usual coronary sinuses in a young person with impaired consciousness or angina suggests the necessity of further anatomic definition with coronary arteriography (42) or possibly with magnetic resonance imaging (38,43,44) or computed tomography (45). An assessment of the diagnostic reliability of echocardiography in this regard for our patients was beyond the scope of the present paper. Two of our athletes had two-dimensional echocardiograms performed, but neither examination focused on the anatomy of coronary artery origin and course, as described by Pelliccia et al. (41).

Surgical management.   Timely clinical identification of wrong sinus coronary artery anomalies in young trained athletes is crucial for two reasons. First, these coronary anomalies should result in exclusion from participation in intense competitive sports to reduce the risk of a cardiac event or sudden death (10,18). Second, and more importantly, wrong sinus coronary artery anomalies are surgically correctable (46). Indeed, operation is probably mandatory in any young person, particularly if symptomatic—with or without evidence of myocardial ischemia. Coronary artery bypass grafting remains the standard procedure for restoring normal distal coronary flow with good long-term results (46). An alternative surgical approach involves reimplantation of the anomalous vessel in the proper coronary sinus, but the results are still preliminary (25). Recently, a new operative technique has been employed in the setting of a proximal aortic intramural course (such as described here), in which the ostium of the anomalous coronary artery is modified at the aorta by excising ("unroofing") the common wall located between the aorta and the anomalous coronary artery (36,37,47).

	Footnotes

 
This study was supported by Veneto Region Research Project on Juvenile Sudden Death, Venice and MURST and CNR Projects on Myocardial Infarction, Rome, Italy, and by a grant from the Minneapolis Heart Institute Foundation.

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				P. Angelini Coronary Artery Anomalies: An Entity in Search of an Identity Circulation, March 13, 2007; 115(10): 1296 - 1305. [Abstract] [Full Text] [PDF]

				S. Basavarajaiah, A. Shah, and S. Sharma Sudden cardiac death in young athletes Heart, March 1, 2007; 93(3): 287 - 289. [Abstract] [Full Text] [PDF]

				R. M. Campbell and S. Berger Preventing Pediatric Sudden Cardiac Death: In Reply Pediatrics, February 1, 2007; 119(2): 408 - 409. [Full Text] [PDF]

				A. K. Attili and P. N. Cascade CT and MRI of Coronary Artery Disease:Evidence-Based Review. Am. J. Roentgenol., December 1, 2006; 187(6 Suppl): S483 - S499. [Abstract] [Full Text] [PDF]

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				B. J. Maron and A. Pelliccia The Heart of Trained Athletes: Cardiac Remodeling and the Risks of Sports, Including Sudden Death Circulation, October 10, 2006; 114(15): 1633 - 1644. [Full Text] [PDF]

				D. Corrado, C. Basso, A. Pavei, P. Michieli, M. Schiavon, and G. Thiene Trends in Sudden Cardiovascular Death in Young Competitive Athletes After Implementation of a Preparticipation Screening Program JAMA, October 4, 2006; 296(13): 1593 - 1601. [Abstract] [Full Text] [PDF]

				E. Erez, V. K.H. Tam, N. A. Doublin, and J. Stakes Anomalous coronary artery with aortic origin and course between the great arteries: improved diagnosis, anatomic findings, and surgical treatment. Ann. Thorac. Surg., September 1, 2006; 82(3): 973 - 977. [Abstract] [Full Text] [PDF]

				S. A. Strickberger, D. W. Benson, I. Biaggioni, D. J. Callans, M. I. Cohen, K. A. Ellenbogen, A. E. Epstein, P. Friedman, J. Goldberger, P. A. Heidenreich, et al. AHA/ACCF Scientific Statement on the Evaluation of Syncope: From the American Heart Association Councils on Clinical Cardiology, Cardiovascular Nursing, Cardiovascular Disease in the Young, and Stroke, and the Quality of Care and Outcomes Research Interdisciplinary Working Group; and the American College of Cardiology Foundation In Collaboration With the Heart Rhythm Society J. Am. Coll. Cardiol., January 17, 2006; 47(2): 473 - 484. [Full Text] [PDF]

				S. A. Strickberger, D. W. Benson, I. Biaggioni, D. J. Callans, M. I. Cohen, K. A. Ellenbogen, A. E. Epstein, P. Friedman, J. Goldberger, P. A. Heidenreich, et al. AHA/ACCF Scientific Statement on the Evaluation of Syncope: From the American Heart Association Councils on Clinical Cardiology, Cardiovascular Nursing, Cardiovascular Disease in the Young, and Stroke, and the Quality of Care and Outcomes Research Interdisciplinary Working Group; and the American College of Cardiology Foundation: In Collaboration With the Heart Rhythm Society: Endorsed by the American Autonomic Society Circulation, January 17, 2006; 113(2): 316 - 327. [Full Text] [PDF]

				T. E. Paterick, T. J. Paterick, G. F. Fletcher, and B. J. Maron Medical and Legal Issues in the Cardiovascular Evaluation of Competitive Athletes JAMA, December 21, 2005; 294(23): 3011 - 3018. [Abstract] [Full Text] [PDF]

				B. J. Maron, P. S. Douglas, T. P. Graham, R. A. Nishimura, and P. D. Thompson Task Force 1: Preparticipation screening and diagnosis of cardiovascular disease in athletes J. Am. Coll. Cardiol., April 19, 2005; 45(8): 1322 - 1326. [Full Text] [PDF]

				T. P. Graham Jr, D. J. Driscoll, W. M. Gersony, J. W. Newburger, A. Rocchini, and J. A. Towbin Task Force 2: Congenital heart disease J. Am. Coll. Cardiol., April 19, 2005; 45(8): 1326 - 1333. [Full Text] [PDF]

				D. Corrado, A. Pelliccia, H. H. Bjornstad, L. Vanhees, A. Biffi, M. Borjesson, N. Panhuyzen-Goedkoop, A. Deligiannis, E. Solberg, D. Dugmore, et al. Cardiovascular pre-participation screening of young competitive athletes for prevention of sudden death: proposal for a common European protocol: Consensus Statement of the Study Group of Sport Cardiology of the Working Group of Cardiac Rehabilitation and Exercise Physiology and the Working Group of Myocardial and Pericardial Diseases of the European Society of Cardiology Eur. Heart J., March 1, 2005; 26(5): 516 - 524. [Abstract] [Full Text] [PDF]

				R. E. Eckart, S. L. Scoville, C. L. Campbell, E. A. Shry, K. C. Stajduhar, R. N. Potter, L. A. Pearse, and R. Virmani Sudden Death in Young Adults: A 25-Year Review of Autopsies in Military Recruits Ann Intern Med, December 7, 2004; 141(11): 829 - 834. [Abstract] [Full Text] [PDF]

B.