Unexpected sudden death resulting from anomalous ...

Legal Medicine 9 (2007) 25–29 www.elsevier.com/locate/legalmed

Case report

Unexpected sudden death resulting from anomalous origin of the right coronary artery from the left sinus of Valsalva: A case report involving identical twins Morio Iino a,*, Takeshi Kimura b, Hitoshi Abiru a, Richard H. Kaszynski a, Qing-Hua Yuan a, Tatsuaki Tsuruyama a, Keiji Tamaki a b

a Department of Legal Medicine, Kyoto University Graduate School of Medicine, Kyoto 606-8501, Japan Department of Cardiovascular Medicine, Kyoto University Graduate School of Medicine, Kyoto 606-8501, Japan

Received 18 May 2006; received in revised form 4 August 2006; accepted 18 August 2006

Abstract An anomalous origin of the coronary arteries had been implicated as a cause of sudden cardiac death in a case involving a 16-year-old student who suddenly collapsed while running track at school. An autopsy revealed that the right coronary artery arose from the aorta in the left sinus of Valsalva. In order to determine whether the same anomaly was inherent in his brother – an identical twin – a complete cardiac medical examination was conducted. Multi-detector-row computed tomography (MDCT) coronary angiography showed no anomaly at the sinus of Valsalva, which indicates that the anomaly, in this case, was not hereditary. This case exemplifies instances where forensic medicine may intervene to prevent sudden deaths in surviving family members. Ó 2006 Elsevier Ireland Ltd. All rights reserved. Keywords: Coronary artery anomalies; Congenital abnormalities; Sudden death; Identical twins; MDCT

1. Introduction Approximately 60–80 sudden deaths occur under school supervision in Japan, each year. Among these: 71% of them are sudden cardiac deaths [1]. Sudden cardiac deaths per 100,000 students occur at frequencies of 0.3 in elementary school students (6–12 years old); 0.8 in junior high school students (13–15 years old); and in 0.9 of high school students (16–18 years old) [1]. For adults, stenosis and occlusion of coronary arteries due to atherosclerosis are the main causes of ischemic heart attack and, in addition, an anomalous origin of the right or left coronary artery has been also implicated as a cause of sudden death [2]. However, the genesis of sudden death is still unknown. In this report, we illustrate and discuss an autopsy performed on

*

Corresponding author. Fax: +81 75 761 9591. E-mail address: [email protected] (M. Iino).

a high school student with a right coronary artery originating from the left sinus of Valsalva. 2. Case report A 16-year-old, male, high school freshman had no history of cardiac disease. He has an identical twin brother who has no subjective symptoms of disease but has been diagnosed with a cardiac murmur. The student, who was a member of his school’s track team, started running on his school track with many of his teammates on a winter morning. After 1.5 h of warm-ups – which included stretching, jogging, jumping hurdles, jumping, etc. – they moved into a training segment consisting of eight, 600-m laps. Although he seemed to be in good physical condition at the end of the 7th lap, he suddenly pitched forward towards the ground while nearing the completion of his 8th and final lap. His teammates ran toward him and found him pale in a non-responsive state and having convulsions.

1344-6223/$ - see front matter Ó 2006 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.legalmed.2006.08.006

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M. Iino et al. / Legal Medicine 9 (2007) 25–29

On the way to the emergency room (ER) in the ambulance, an electrocardiogram showed ventricular fibrillation. On arrival at the ER, he was in cardio-pulmonary arrest (CPA). Although he regained his heartbeat once, he went back into CPA. An arterial blood gas analysis showed metabolic acidosis. A biochemical examination of the blood turned up the following results which suggest myocardial ischemia: creatine phosphokinase (CPK) 1320 U/l, lactate dehydrogenase (LDH) 478 U/l, glutamate oxaloacetate transaminase (GOT) 140 U/l and glutamate pyruvate transaminase (GPT) 164 U/l. An X-ray photograph of the chest showed edema of the lung. A CT of the chest showed congestion of the lung and no dissecting aneurysm of the aorta. The CT of the head showed brain edema. The ER team decided to treat him with percutaneous cardio-pulmonary support (PCPS). A blood transfusion was done since anemia was noticed after starting PCPS. The first time the ER team inserted the PCPS catheters, the amount of blood removal was as low as 1 l/min, which was not sufficient for oxygenation. After they replaced the catheters, the blood flow increased to as much as 3 l/min. Finally, concentrated red blood cells from 1600 ml of whole blood was transfused. Three hours after the student entered the ICU with PCPS, his general condition deteriorated and he became bradycardic with cyanosis of the inferior limbs. He was pronounced dead an hour later.

a

3. Autopsy findings

c

The deceased was 172 cm tall and 59.5 kg in weight. Slight livor mortis was evident on his back. Excoriation on the right malar part was thought to be caused by the fall on the track. Sutures were found on the bilateral inguinal region where the PCPS catheters were inserted. There was 1300 ml of blood inside the abdominal cavity and a hematoma in the retroperitoneum. The damaged blood vessels included the right femoral artery and the bilateral femoral veins. The heart weighed 245 g and was as large as the fist of the deceased. The thicknesses of the cardiac muscles were: 1.4 cm in the left ventricle; 0.5 cm in the right ventricle; and 1.5 cm in the ventricular septum. The width of the origin of the aorta was 5.5 cm. Fig. 1a shows a section of the aortic root that includes the origin of the coronary arteries. The left coronary artery (LCA) originates from the correct position in the left sinus of Valsalva. However, the right coronary artery (RCA) also originates from the left sinus of Valsalva. The ostium of the RCA is circular in shape. Fig. 1b is a diagram of the origin of the coronary arteries and shows the abnormal course of the left coronary artery. From its origin, the LCA goes upward along the aorta about 0.8 cm, and then shifts in direction 180° to the ventricle region and divides into the left anterior descending coronary artery (LAD) and the circumflex coronary artery (LCX). Fig. 1c shows a view from the top of the aorta. Although part of the proximal RCA has been removed to make the pathologic specimen, the white dotted line illustrates location of the RCA prior to removal.

LCA

RCA

b

aorta

LMT LCX 0.8 cm

RCA

LCA

LAD

PA RCA

aorta origin of the RCA Fig. 1. (a) A section of the aortic root that includes the origin of the coronary arteries. The right coronary artery (RCA) originates from the left sinus of Valsalva. An enlarged view of the ostium of the RCA is shown in the smaller box. (b) The left coronary artery (LCA) goes upward along the aorta about 0.8 cm and then shifts in direction 180° to become the left main trunk (LMT) that divides into the left anterior descending (LAD) coronary artery and the left circumflex (LCX) coronary artery. (c) A view from the top of the aorta (the proximal RCA has been removed to make the pathologic specimen). The white dotted line shows the location of the RCA prior to removal. The RCA originates saliently from the origin of the aorta then travels between the aorta and pulmonary artery (PA).

The RCA originates saliently from the origin of the aorta and then travels between the aorta and pulmonary artery. The left lung weighed 800 g, and the right lung weighed 910 g. Both showed congestion and edema. The trachea was filled with a red, foamy liquid that was believed to have been caused by left cardiac failure. There was hemorrhage


on the mucosa of the trachea. Other organs, such as the liver, kidney, and brain showed ischemic change due to bleeding into the abdominal cavity.

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Based on histological examinations, part of left main coronary artery appeared to have a 60% reduction in diameter (Fig. 2a). Very little stenosis of the LAD or the LCX was observed. There was a slight fibrous stenosis on the right coronary artery (Fig. 2b). Fig. 2c shows the pathologic histology of the anterior wall of the left ventricular cardiac muscle in Azan stain. There is fiber disarray and a zone of shrinkage necrosis. The similar histological findings are observed in the anterior wall of the right ventricular cardiac muscle. There are extensive colliquative myocytolysis characterized by intracellular vacuolization and loss of cross striations in the posterior wall of the left ventricular cardiac muscle (Fig. 2d) and thickened endocardium with areas of fibrosis in the right ventricular apex. 4. Medical examinations of the surviving twin brother After the student’s death, the family requested that a medical examination of the heart be conducted on the surviving twin brother. Therefore, he was brought to our university hospital for a cardiac medical examination. A non-invasive work-up was performed that included ECGs, echocardiography and CT coronary angiography. There were no abnormal findings on the 12-lead ECG and exercise ECG, while a Wenckebach type 2 A-V block was observed during sleep on a Holter ECG. Echocardiography showed that heart function was normal and no valvular regurgitation or hypertrophy of the myocardium was present. In order to confirm if an anomalous origin of the right coronary artery was present, the surviving twin brother underwent multi-detector-row computed tomography (MDCT) coronary angiography. MDCT was performed using a SOMATOM Sensation 16 (16 detector-row, Siemens Medical Solutions, Forchheim, Germany). The MDCT revealed the cardiac lumen and the coronary arteries, clearly. Not only that, but the MDCT also revealed that the LCA originates from the left sinus of Valsalva and the RCA originates from the right sinus of Valsalva. No anomalous origin of the coronary arteries and no evidence of coronary arterial stenosis could be confirmed (Fig. 3). 5. Discussion We describe a case of sudden death occurring in a high school student while running track at school. When classifying the ratio of sudden deaths occurring under school

b Fig. 2. (a) A portion of the left main coronary artery that traveled upward along the aorta with severe stenosis (Elastica-van Gieson method). (b) Slight fibrous stenosis on the right coronary artery (Elastica-van Gieson method). (c) Fiber disarray and a zone of shrinkage necrosis of the anterior wall of left ventricular cardiac muscle (Azan stain). (d) Extensive colliquative myocytolysis characterized by intracellular vacuolization and loss of cross striations found in the posterior wall of left ventricular cardiac muscle. An enlarged view of the intracellular vacuolization is shown in the smaller box. (Hematoxylin and Eosin stain).

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a

b

Fig. 3. (a and b) MDCT coronary angiography image of the surviving identical twin brother showing the right coronary artery (arrow) and the left coronary artery (arrow head). MDCT revealed that the coronary arteries were correctly positioned with no evidence of stenosis.

supervision in Japan by academic levels, we see that 20% occur in elementary school students; 30% occur in junior high school student; and 50% occur in high school students. For the most part, these deaths occur within the 10 a.m. to 12-noon timeframe. Of all of the relevant age groups, first year students in high school most frequently die as a result of sudden death under school supervision. The 41% of sudden deaths at school occurred at a time of running – including short track and long distance [1]. The present case coincides with this data, because the deceased was a first year student in high school and the incident occurred at 11:30 a.m. while running track. The most common cause of sudden deaths occurring at school is congenital heart disease (48%) including preoperative and postoperative ones. The second most common cause

is various types of cardiomyopathy (24%) [1]. Though this was a typical sudden death case which occurred at school, the cause of the sudden cardiac disorder was anything but typical. As to the cause of his collapse while running on the track, we assume this was due to ischemic heart disease since the biochemical examination of blood showed patterns of myocardial ischemia. In addition, the fiber disarray and a zone of shrinkage necrosis were found in the anterior walls of the left and right ventricular cardiac muscle which have been linked to ventricular fibrillation and sudden death [3]. We also found extensive colliquative myocytolysis characterized by intracellular vacuolization and loss of cross striations in the posterior wall of left ventricular cardiac muscle. Myocytolysis is considered a helpful marker of significant myocardial ischemia in sudden death [4]. Though the pathogenesis of it is not known, it is considered an intermediate phase between reversible ischemic changes is the myocardium and irreversible coagulation necrosis [4]. In this case, 1300 ml of blood was found inside the abdominal cavity during autopsy. It was thought to be leaked from the right and left femoral arteries during PCPS. We do not assume that blood loss was related to the cause of death because sufficient amount of blood was transfused during and after PCPS. One cause of ischemic heart disease was based on the anomalous origin of the right coronary artery since the fiber disarray and a zone of shrinkage necrosis were found in the anterior walls of the right ventricular cardiac muscle which is fed by the RCA. The other cause was based on coronary atherosclerosis since there was 60% reduction in diameter in the left main coronary artery. There are some reports in the literature of the anomalous origin of the coronary arteries [2,5–9]. Since Roberts et al. first described sudden death from an anomalous origin of the RCA in the LSV in 1982 [5], this anomaly has been implicated as a cause of several cases of sudden cardiac death [2,6–8]. In 1996, Ohshima reported a case of a single coronary artery in a 12-year-old boy whose mother and grandmother had died suddenly which suggested that the condition might be hereditary [9]. An arrhythmia secondary to acute myocardial ischemia was presumed to be the cause of sudden death in patients with an anomalous RCA originating from the LSV [2]. Several mechanisms of myocardial ischemia have been postulated to explain it. First, because of the acute take-off from the aortic wall, the ostium of the anomalous coronary artery is slit-like when, under normal circumstances, should be circular in shape. Second, the first segment of the anomalous coronary artery runs between the ascending aorta and the pulmonary trunk. Thus, during physical effort, compression and squeezing of the anomalous coronary artery by expansion of both the aorta and pulmonary trunk, and the flap-like closure of the orifice, may occur simultaneously [2]. MDCT that appeared in 1998 rapidly improved the temporal and spatial resolution in diagnostic imaging


techniques of the heart and the large arteries. It has recently been introduced as a method for non-invasive visualization of coronary artery stenosis [10,11]. MDCT with a detector of 16 rows appeared in 2002 and it has been widely spread to domestic hospitals. At present, 64 row MDCT has been introduced into medical practice [12]. The recent development of MDCT constitutes an important step forward in non-invasive angiography and has produced remarkable results in identifying high-grade coronary stenosis [13]. Nowadays MDCT is considered the most useful tool in diagnosing anomalous origin of the coronary arteries [14–16]. The surviving twin brother had no anomalous origin of the coronary arteries based on MDCT coronary angiography, suggesting the anomaly of the deceased was not hereditary. Based on the exercise ECG and the MDCT results, the surviving brother has not been placed under restriction of physical activity. This is a rare case in which forensic pathologists could prevent sudden deaths from occurring in surviving family members. Acknowledgments The authors wish to thank the surviving family for their understanding and cooperation and for supplying invaluable input essential to the formulation of the paper. We would also like to express our gratitude to the Morishita Heart Clinic for conducting the MDCT examination. References [1] Ito S, Harada K. Sudden cardiac death of school-age children (in Japanese). Nippon Rinsho 2005;63:1261–71. [2] Bunai Y, Akaza K, Tsujinaka M, Nagai A, Nakamura I, Ohya I. Anomalous origin of the right coronary artery from the left sinus of Valsalva: report of two cases. Forensic Sci Int 2001;123:254–6. [3] Baroldi G, Silver MD, Parolini M, Pomara C, Turillazzi E, Fineschi V. Myofiberbreak-up: a marker of ventricular fibrillation in sudden cardiac death. Int J Cardiol 2005;100:435–41. [4] Adegboyega PA, Haque AK, Boor PJ. Extensive Myocytolysis as a Marker of Sudden Cardiac Death. Cardiovasc Pathol 1996;5:315–21.

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[5] Roberts WC, Siegel RJ, Zipes DP. Origin of the right coronary artery from the left sinus of Valsalva and its functional consequences: analysis of 10 necropsy patients. Am J Cardiol 1982;49:863–8. [6] Frescura C, Basso C, Thiene G, Corrado D, Pennelli T, Angelini A, Daliento L. Anomalous origin of coronary arteries and risk of sudden death: a study based on an autopsy population of congenital heart disease. Hum Pathol 1998;29:689–95. [7] Blanco Pampin J, Taboas AR. Unexpected sudden death resulting from anomalous origin of the left coronary artery from the right sinus of Valsalva. Legal Med 2000;2:156–8. [8] Aoki Y, Saigusa K, Nakayama Y. Sudden infant death with anomalous origin of the left coronary artery from the pulmonary artery. Legal Med 1999;1:250–3. [9] Ohshima T, Lin Z, Sato Y. Unexpected sudden death of a 12-year-old male with congenital single coronary artery. Forensic Sci Int 1996;82:177–81. [10] Kopp AF, Schroeder S, Kuettner A, Baumbach A, Georg C, Kuzo R, Heuschmid M, Ohnesorge B, Karsch KR, Claussen CD. Noninvasive coronary angiography with high resolution multidetectorrow computed tomography. Results in 102 patients. Eur Heart J 2002;23:1714–25. [11] Ropers D, Baum U, Pohle K, Anders K, Ulzheimer S, Ohnesorge B, Schlundt C, Bautz W, Daniel WG, Achenbach S. Detection of coronary artery stenoses with thin-slice multi-detector row spiral computed tomography and multiplanar reconstruction. Circulation 2003;10:664–6. [12] Hara M, Oshima H, Suzuki H, Shiraki N, Kitase M, Shibamoto Y, Tamaki T, Nishio M. The frontiers of diagnostic radiology – PET/CT, 3DCT – (in Japanese). Nippon Geka Gakkai Zasshi 2005;106:677–84. [13] Leber AW, Knez A, von Ziegler F, Becker A, Nikolaou K, Paul S, Wintersperger B, Reiser M, Becker CR, Steinbeck G, Boekstegers P. Quantification of obstructive and nonobstructive coronary lesions by 64-slice computed tomography: a comparative study with quantitative coronary angiography and intravascular ultrasound. J Am Coll Cardiol 2005;46:147–54. [14] Sato Y, Ichikawa M, Masubuchi M, Yoda S, Furuhashi S, Takahashi M, Koyama Y, Saito S. MDCT of the anomalous origin of the right coronary artery from the left sinus of Valsalva as a single coronary artery. Int J Cardiol 2006;109:125–6. [15] Sato Y, Inoue F, Kunimasa T, Matsumoto N, Yoda S, Tani S, Takayama T, Uchiyama T, Tanaka H, Furuhashi S, Takahashi M, Koyama Y, Saito S. Diagnosis of anomalous origin of the right coronary artery using multislice computed tomography: evaluation of possible causes of myocardial ischemia. Heart Vessels 2005;20:298–300. [16] Fineschi V, Maresi E, Di Padua M, Riezzo I, Neri M. Sudden cardiac death due to anomalous origin of the right coronary artery: a case report in a child. Int J Cardiol 2006;108:426–8.