Coronary Artery Fistula: a Review Marios Loukas, Ashley St. Shane Tubbs, Diane Spicer

Germain, Abigail Gabriel, Alana John, R.

PII: DOI: Reference:

S1054-8807(14)00024-6 doi: 10.1016/j.carpath.2014.01.010 CVP 6752

To appear in:

Cardiovascular Pathology

Received date: Revised date: Accepted date:

25 November 2013 31 January 2014 31 January 2014

Please cite this article as: Loukas Marios, Germain Ashley St., Gabriel Abigail, John Alana, Tubbs R. Shane, Spicer Diane, Coronary Artery Fistula: a Review, Cardiovascular Pathology (2014), doi: 10.1016/j.carpath.2014.01.010

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ACCEPTED MANUSCRIPT Title: Coronary Artery Fistula: A Review Authors: Marios Loukas MD PhD1,4, Ashley St. Germain MD1, Abigail Gabriel MD MPH1, Alana John MD3, R Shane Tubbs Ph.D.1,2, Diane Spicer 5

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Running Title: Coronary Artery Fistula

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Department of Anatomical Sciences, St. George's University, School of Medicine, Grenada, West Indies 2 Pediatric Neurosurgery, Children’s’ Hospital, Birmingham, Alabama 3 Department of Internal Medicine, SUNY Downstate, New York 4 Department of Anatomy, Medical Faculty, University of Varmia and Masuria in Olsztyn, Poland 5 Department of Pediatrics-Cardiology, University of Florida, Gainesville, Florida 6 The Congenital Heart Institute of Florida, St. Petersburg, Florida

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Key Words: Coronary vessels, fistula, canine, congenital coronary artery fistula

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Correspondence: Marios Loukas M.D., Ph.D. Professor and Chair, Department of Anatomical Sciences, Dean of Research, St. George's University, School of Medicine, Grenada, West Indies. E-mail: [email protected] Tel: 473-444-4175 x3005 Fax: 473-444-2887

ACCEPTED MANUSCRIPT A Review of Coronary Fistulas

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Abstract-

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Coronary arterial fistulas are abnormal connections between the coronary arteries and the chambers of the heart or major thoracic vessels. Although first described in 1841, the true

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incidence is difficult to evaluate because approximately half of the cases may be asymptomatic and clinically undetectable. This review will discuss the history and prevalence of coronary

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artery fistulas, their morphology, histology, presentation, diagnosis, treatment options, and

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complications.

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History and Prevalence-

As the aorta exits the left ventricle two coronary arteries originate from its root, to supply the

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muscle and tissues of the heart . The left coronary artery originates from the left aortic sinus,

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whereas the right coronary artery originates from the right aortic sinus. As the right coronary artery descends it branches to give a sinuatrial nodal branch, right marginal branch and a

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posterior interventricular branch. On the other hand, the left coronary artery descends and gives an anterior interventricular branch (Fig. 1) and a circumflex branch.

A coronary artery fistula, however, is an abnormal connection that directly links one or more coronary arteries to a heart chamber or to major thoracic vessels without an interposed capillary bed[1]. Fistulas that arise from a coronary artery and then terminate into a chamber of the heart are known as coronary-cameral fistulas, while those terminating into a vein are coronary arteriovenous fistulas [2]. Coronary artery fistulas occur equally in both sexes and have a 0.002%

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ACCEPTED MANUSCRIPT incidence among the general population, [3,4] accounting for 0.1% of coronary anomalies with

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2%-17% occurring bilaterally [1,5].

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While relatively uncommon in the population, coronary abnormalities attributed to coronary artery fistulas have been recognized for hundreds of years. The first description of a coronary

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artery fistula occurred in 1841 by the Austrian anatomist Josef Hrytl [4,6]. Despite this initial

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discovery, many accredit German anatomist W. Kraus’s 1865 description of an aberrant connection between a coronary artery and a heart chamber as the first reported coronary artery

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fistula [4,6]. Much of the statistical data regarding the incidence, etiology, presentation, and treatment of coronary artery fistulas is derived from cohort data, both retrospective and

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prospective, as well as numerous case studies. These resources categorize them as either

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congenital or acquired anomalies. Congenital coronary artery fistulas are more common, but only

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account for 0.4% of congenital cardiac abnormalities [4,7].

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Acquired coronary artery fistulas develop from injurious events, iatrogenic or traumatic in nature, with a predominance of the former. Several cases report the appearance of acquired fistulas both postoperatively and after certain medical conditions, including the following: heart transplants, mitral valve replacements, percutaneous coronary interventions, septal myectomies, closed-chest ablations, coronary artery bypass grafts, permanent pacemaker placements, acute myocardial infarctions, and transbronchial lung biopsies [4, 6, 8]. In such cases, the sudden postoperative appearance of a continuous murmur is indicative of iatrogenic fistula formation [4]. Whereas, acquired coronary artery fistulas due to traumatic injury can occur in both thorax penetrating and non-penetrating accidents [4, 9]. In these, the most common point of origin is the

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ACCEPTED MANUSCRIPT right coronary artery, and the most common termination is within the right chambers of the heart [4, 10].

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Similar to humans, fistulas in mammals, especially cattle, usually occur between the

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coronary arteries and the ventricles of the heart [11]. In Michaelsson and Ho’s study, the right ventricle was the most common termination of these fistulas. In addition to cattle, coronary

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artery fistulas also occur in canines. This type of fistula is uncommon in dogs, just as they are in

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humans, and present with analogous symptoms, complications, and treatment options [12].

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Morphology-

While the exact percentage of morphological origins and terminations of coronary artery fistulas

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differ, the consensus is that fistulas are typically found on the right side of the heart. Studies

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show that the point of origin in 52-60% of coronary artery fistulas is the right coronary artery, 30% at the left anterior interventricular (left anterior descending) artery, and 18% at the left

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circumflex artery [2, 13, 14]. Regardless of point of origin, nearly 90% of fistulas drain to the

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right chambers of the heart [14]. In 2006, Qureshi and colleagues stated that in the right heart, drainage occurs most frequently to the right ventricle, in about 40%, followed by the right atrium (Fig. 2), coronary sinus, and pulmonary trunk [14] (Fig. 3). As these studies indicate, any of the three major coronary arteries can be the feeding artery for the coronary fistula and depending on the artery and point of origin, the tortuosity and dilation of the fistula will vary. Coronary artery fistulas that branch from a main coronary artery at a proximal location are more dilated when compared to other distally located coronary artery fistulas [15]. For example fistulas that originate proximally and drain into the right atrium are much more dilated, but less tortuous. The

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ACCEPTED MANUSCRIPT most anatomically complex coronary artery fistulas are those that originate at the right coronary

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artery and drain into the coronary sinus. These tend to be extremely large and tortuous [4].

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As with the point of origin, the drainage site introduces a certain degree of anatomic variation [16]. In 1974, a study by Ogden et al. was the first to categorize coronary artery fistulas based on

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their drainage site in the atriums, classifying them into 3 types.

Type 1 coronary artery fistulas can either terminate into the right or left atrium and these fistulas

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are physiologically similar to each other but different from those terminating in the high pressure ventricles. The thick walls of the ventricles allow for the closure of the fistula during ventricular

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systole whereas the thinner walls of the atriums have no effect on the fistula opening. Type 1

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classically has short, dilated arterial branches that extend from the right coronary artery and terminate in either the right appendage (Fig. 4) or the right atrial vestibule (Fig. 2). Right atrium-

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terminating Type 1 coronary artery fistulas usually only involve the right coronary artery (Fig. 5)

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whereas those terminating in the left atrium mainly involve the left coronary branches [16] (Fig.

Type 2 coronary artery fistulas are the most frequently encountered and are more variable than type 1, since both the left (Fig. 6) and right (Fig. 6) coronary arteries can feed the fistula. From its point of origin the fistula usually travels posteriorly between the atriums and drains at a point anterior to the superior caval vein. If it does not terminate at the superior caval vein, the coronary artery fistula will travel around the superior caval vein and terminate into the posterior surface of the atrium (Fig. 6).

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Type 3 includes coronary artery fistulas that terminate in the posterior surface of the right or left

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atrium, usually along the atrioventricular groove (Fig. 7). As with type 2, type 3 can involve

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either the right or left coronary arteries [16] however, the termination of the fistula determines the blood flow during diastole and systole. If the coronary artery fistula terminates in the right

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ventricle, it will pass through the myocardium and be closed upon systolic contraction and will

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cause increased hemodynamic stress on the heart [3, 17]. Far less hemodynamic difference is seen in fistulas terminating in the left ventricle (Fig. 8). However, if the point of origin of the

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fistula is the left coronary artery and it terminates in the left atrium (Fig. 7), the overall pressure in the left atrium will be increased when compared to those terminating in the right atrium [3]

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(Fig. 7). While hemodynamic changes can cause serious complications, several studies

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hypothesize that collateral circulation from the uninvolved coronary artery compensates for

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Histology-

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blood loss to the chambers and prevents myocardial infarction [3, 17-19].

In order to study the histology of coronary artery fistulas, Neufeld et al. removed a segment of the parent coronary artery involved in a fistula that terminated in the right ventricle. Microscopic analysis showed that most of the vessels studied had prominent muscle bundles and contained a duplicated internal elastic lamina dispersed between them. Additionally, the tunica intima layer had nonspecific fibrous thickening [17, 20]. A similar study also reported the same histological changes in other vessels around the coronary artery fistula [20].

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ACCEPTED MANUSCRIPT Presentation and SymptomsTypically coronary artery fistulas are often asymptomatic during childhood. Based on several

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studies, symptoms are present in 19%-63% of patients, with the majority occurring after 18 years

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of age [4, 21, 22]. The most common symptom reported is dyspnea, with exertion [4, 21]. Murmurs are also commonly reported with coronary artery fistulas, in fact, many otherwise

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asymptomatic fistulas are often found after angiographic investigation of continuous murmurs

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heard at the lower left sternal border. Studies report that the majority of adult patients with coronary artery fistulas usually present with a murmur, whereas only 9% of children via

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echocardiography, also have continuous murmurs [4, 23-25]. When fistulas terminate in a left-

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sided chamber, the aortic run-off mimics aortic insufficiency and its murmur [26].

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While dyspnea and murmurs are the most prevalent among reported symptoms, the following are also reported: fatigue, atrial arrhythmia, pulmonary hypertension, congestive heart failure,

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presence of aneurysms, rupture or thrombosis of the fistula, pneumonia, palpitations, upper

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respiratory infection, hemoptysis, edema, paroxysmal nocturnal dyspnea, endocarditis, and angina [4]. Angina experienced in coronary artery fistula patients is usually seen when the fistula is combined with other cardiac anomalies such as atherosclerotic coronary artery disease, obstructive cardiomyopathy, and aortic stenosis [4, 16, 27-29]. When compared to animal studies canine coronary artery fistulas may also be congenital or acquired secondary to trauma, bacterial endocarditis, mycotic infection, or atherosclerosis [30-32].

Pathophysiological Consequences

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ACCEPTED MANUSCRIPT According to Ata et al. (2009), coronary artery fistulas are a very rare cardiac anomaly; however they are the most hemodynamically significant lesions affecting the cardiovascular system. Ata

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et al. (2009), states that approximately half of all CAF patients are asymptomatic and some

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congenital fistulas may spontaneously regress during childhood [33]. In patients with symptoms, most report atypical chest pain and exertional dyspnea which is often due to the progressive

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enlargement of the fistula and the increasing left-to-right shunting [34].

Although coronary anomalies have been implicated in chest pain, sudden death and myocardial

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infarction among other symptoms a casual relationship can be suggested based on solid evidence. [35]. According to Angelini et al. (2002), there is a relationship between anomalous origin of the

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left coronary artery from the pulmonary artery (ALCAPA) and the acute anterolateral myocardial

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infarction in newborns [35]. However, because the coronary vessels primarily supply metabolic support to the dependent myocardium, physiological alterations in this function should be the

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main consideration. Mechleb et al. (2013), state that although the clinical presentation of CAF

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varies widely it is dependent on the size of the fistula, age of patient and presence of myocardial ischemia [36].

Although chest pain is one of the most common symptoms, dyspnea and

congestive heart failure were also very common and were mainly attributed to volume overload secondary to multiple CAF and large shunts [36]. They also suggested that although pulmonary hypertension has been reported to be the cause of dyspnea in some patients and exertional angina without angiographic evidence of coronary atherosclerosis has been attributed to a coronary steal phenomenon. This phenomenon suggests that there is a decrease in myocardial perfusion on exertion due to the inability of the coronary flow reserve to be augmented [36].

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ACCEPTED MANUSCRIPT ComplicationsThough the majority of coronary artery fistulas are etiologically congenital, complications

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typically do not present until after age 20 [37]. These complications display a wide range in

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severity, from being asymptomatic in 75% of cases to presenting with myocardial ischemia and aortic insufficiency [23, 38, 39]. Symptoms, when present, are usually secondary to congestive

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heart failure, which, in turn, is as a result of a left to right shunt. Arrhythmias can also occur due

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to excessive cardiac chamber load, as well as congestive heart failure in older patients. Infective endocarditis has been reported in incidences varying from 0-12% [26] and in 20% of patients

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with a coronary artery fistula, additional cardiac anomalies have also been reported [4]. These include tetralogy of Fallot, aortic atresia, pulmonary atresia, atrial and ventricular septal defects,

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and patent arterial duct [4, 40]. In rare cases, the initial manifestation was myocardial ischemia,

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Diagnostics-

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pericardial effusion, or sudden death [4].

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Due to the asymptomatic nature of coronary artery fistulas, many are incidental findings during routine examinations. The gold standard for identifying them remains coronary angiography, however, less invasive two- and three-dimensional imaging techniques are becoming more common [42-45]. The benefit of coronary angiography is that it helps to determine which coronary artery is involved in the fistula. Based on this it can help to identify the communicating chamber or vessel and the locations of the communications with respect to the proximal/distal portions of the vessel [4]. Although angiography sets the standard for coronary artery fistula diagnosis, new methods, including multidetector computed tomography (MDCT) or multislice computed tomography (MSCT), magnetic resonance imaging (MRI), transesophageal

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ACCEPTED MANUSCRIPT echocardiography, transthoracic echocardiography, and Doppler echocardiography have also

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been beneficial [43, 46-48].

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Transesophageal echocardiography provides a good view of the structures at the base of the heart and with this approach, the anatomy of the fistula, its point of origin, and its termination can

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often be visualized. Additionally, high-resolution transducers can often display the cardiac

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vessels with greater spatial resolution than other imaging methods, allowing evaluation of blood flow in the fistula [46-49]. However, transesophageal echocardiography is limited in that it best

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visualizes the left coronary artery and left atrium. With the high prevalence of aberrant fistulas on the right side of the heart, this technique may not be helpful in all coronary artery fistula

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cases.

Utilizing the combination of pulsed and two-dimensional Doppler echocardiography in suspected

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or confirmed cases of coronary artery fistula, coronary artery dilation, termination chamber, and

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turbulent flow can be observed [47, 4]. The non-invasive nature of Doppler echocardiography is a tremendous benefit, allowing it to be used pre- and post-treatment in order to monitor the status of the fistula. Additionally, color Doppler imaging is often utilized to determine the severity of blood shunting. Along with a high frequency transducer, transthoracic color Doppler echocardiography allows for the visualization of multiple microfistulas originating from the coronary artery and communicating with the left ventricle [4]. In one case study, involving canine coronary artery fistulas, Leach et al. reported multiple microfistulas in a dog diagnosed via Doppler echocardiography and radiographic studies. Using the same techniques as human medicine, the necessity for surgical repair was determined based on the degree of coronary steal.

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Other imaging techniques including CT and MRI scans have been used for both diagnostics and

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follow-up [50-54]. In the last decade, MDCT and MSCT with angiography have gained clinical

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significance in coronary artery fistula diagnostics due to their ability to provide detailed images with minimally invasive techniques [48, 53-56]. Several studies suggest that MDCT can provide

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a superior visualization of coroanry artery fistulas, possible aneurysms, and adjacent anatomical

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structures [48, 53, 54, 56]. In addition to MDCT, several cases suggest using MRI to determine what coronary vessels are involved in coronary artery fistulas [51]. In the cases reviewed, MRI

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was able to discern the location, course, blood flow, and function of the fistula [51, 57-63].

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If surgery for a coronary artery fistula proves necessary, transesophageal echocardiography can

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be used to determine the precise drainage site. This is an invaluable tool as such precise

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Pediatric-

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termination points are often not detectable through preoperative coronary angiograms [64].

In a retrospective study, Mavroudis et al. reviewed the diagnosis and treatment of pediatric coronary artery fistula patients. As in the general population, most of the pediatric patients were asymptomatic and the majority of fistulas were congenital. Only one of the patients studied had an acquired fistula as a consequence of tetralogy of Fallot repair. In addition to tetralogy of Fallot, other cardiac anomalies that present in the pediatric patient cohort were patent arterial duct and atrial septal defects [37, 41]. All of the pediatric patients that were studied underwent invasive surgical repair of their coronary artery fistula via a median sternotomy and epicardial or endocardial ligation. While postoperative angiographic studies deemed the surgical repairs

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ACCEPTED MANUSCRIPT successful, Mavroudis et al. set out to determine whether coil embolization could have been performed as an alternative therapy. Based on their research, criterion for choosing elective coil

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occlusion over median sternotomy surgical repair were established requiring fulfillment of the

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following: 1) the presence of only one coronary artery fistula, 2) a narrow drainage site upon termination, 3) the absence of large branch vessels, and 4) relatively safe accessibility to the

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coronary artery supplying the fistula [37].

Prenatal-

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Coronary artery fistulas account for 50% of pediatric coronary vascular aberrations and are believed to originate from the thebesian vessels [4, 7]. During prenatal life the coronary arteries

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communicate with the ventricles via intratrabecular spaces. As the fetus develops, these

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intratrabecular spaces become sinusoids that communicate between the coronary arteries and veins and the chambers of the heart. Fistulas are thought to develop if these intratrabecular

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spaces do not close to sinusoids [3, 65].

Due to the prevalence of complications of coronary artery fistulas in the adult years, most studies recommend treatment upon diagnosis [37, 66]. Imaging techniques can now be utilized to diagnose coronary artery fistulas prenatally, which enables swift treatment if the left-to-right shunt poses a significant hemodynamic problem to the heart. While these imaging techniques can be beneficial, fetal cardiac vessels are difficult to discern based on size and movement of the heart [67].

Studies reporting on prenatal diagnosis reveal that coronary artery fistulas are found using

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ACCEPTED MANUSCRIPT Doppler echocardiography to investigate other suspected cardiac anomalies, such as atrialseptal defects [41, 67, 68]. Color Doppler often confirms the existence of a fistula, and pulsed Doppler

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can determine blood flow through the fistula [67]. Prenatally diagnosed coronary artery fistulas

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can be monitored throughout pregnancy using echocardiography. After birth, angiography can confirm the diagnosis [67-70].

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As repair techniques and guidelines become more concrete, early intervention and higher

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survival rates for prenatally diagnosed cases may occur. Prenatal imaging allows for the proper perinatal follow-up and diligent monitoring of heart failure and other cardiac complications [68-

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70].

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Treatment -

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Due to the fact that CAF mostly remain asymptomatic, the treatment of CAF is essentially medical; conservative management with continued follow up [71]. While rare, there have been

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cases of spontaneous closure of coronary artery fistulas without surgical or catheter repair [4, 72-

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74]. Among these, most spontaneous closures occur in children diagnosed with a coronary artery fistula prior to 2 years of age, and these fistulas almost always drain into the right ventricle [75]. Surgical correction of coronary artery fistulas in asymptomatic patients is controversial. When fistulas are detected in young patients, several believe it best to repair the fistula prior to the development of more serious complications [66]. The main indication for closure of the fistula is the existence of a significant left-to-right shunt that causes ventricular overload [4]. This shunting is commonly known as the coronary steal phenomenon, in which the movement of blood from the high-pressure fistula into the low-pressure chamber causes hemodynamic stress

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ACCEPTED MANUSCRIPT on the heart. If severe, coronary steal can cause extreme cardiac damage including hypertrophy

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as well as ischemia due to re-routing of the coronary vessels.

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If large shunts are present but do not cause pathological problems or symptoms, treatment options remain controversial. If detected in pediatric patients, they are usually corrected in order

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to avoid late-onset complications. In fact, many retrospective reviews concluded that

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complications involved in surgical correction outweighed the risk of coronary artery fistula complications [4, 76-78]. In extremely mild shunts, however, Cheung and colleagues suggest

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that regular screening to monitor pathological changes should be utilized prior to elective

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surgical correction [25].

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Surgical Correction-

In coronary artery fistula patients where operative correction proves necessary, surgical ligation

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or percutaneous transcatheter occlusion are possible treatment options [44, 66, 79-80 ]. The type

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of operative correction for coronary artery fistulas depends on the location of the fistula, the coronary artery involved, and the termination of the connection. Typically, direct ligation of the fistula at the drainage site is preferred because it should eliminate the possibility of myocardial ischemia [4, 21]. However, if direct ligation of the coronary artery may compromise blood flow to the myocardium, grafting of the involved distal coronary artery is suggested.

If transcatheter occlusion is contraindicated, surgical closure or ligation of the fistulas are implemented [17-19]. The first such surgery was performed in 1947 by Bjork and Crafoord in which they closed a coronary artery fistula terminating in the pulmonary artery on a patient with

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ACCEPTED MANUSCRIPT a preoperative diagnosis of patent arterial duct [81]. Almost twenty years later, in 1963, the first successful bypass graft of a coronary artery was performed by Drs. Cooley and Hallman in order

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to treat a fistula between the left coronary artery and the right ventricle [82].

Prior to the development of these coronary bypass techniques, surgical correction of coronary

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artery fistulas involved direct ligation or tangential arteriorrhaphy. Ligation was associated with

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a high mortality rate, but arteriorrhaphy could be performed without cardiopulmonary bypass with the caveat that fistulas were easily accessible and lacked complex tortuosity. For this

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procedure, multiple horizontal mattress sutures were placed between the coronary artery and the

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Transcatheter Techniques-

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fistula to ensure that blood flow through the coronary artery remained unobstructed [82].

Studies suggest that transcatheter approaches are more beneficial than surgical approaches for

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eligible coronary artery fistula cases. Transcatheter techniques do not require median sternotomy

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or cardiopulmonary bypass, thus limiting potential iatrogenic complications. Transcatheter closure is also a less expensive procedure with decreased morbidity, decreased recovery time and better cosmetic results [44, 83-84]. On the other hand, the use of transcatheter approaches and coil occlusion techniques can also result in distal embolization or dissection of the fistula being corrected [83]. Reiday et al. performed the first successful transcatheter closure of a coronary artery fistula in 1983 however; several varying techniques and new products have since been used. These products included covered stainless-steal coils, detachable balloons, Gianturco coils, co-axial embolization with platinum micro-coils, double umbrella devices, Amplatzer duct occlusion, and the Gianturco Grifka vascular occlusion device [4, 78, 85]. The type of occlusion

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ACCEPTED MANUSCRIPT device used depends both on the surgeon’s preference and the anatomical features of the fistula being corrected. Depending on the tortuosity, length, and dilation of the fistula, varying degrees

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large fistulas and coils are used for small fistulas [4, 79-80].

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of flexibility in catheters is necessary. However, double-umbrella devices are typically used for

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In 2008, Kassaian et al. described one of only two reported coronary artery fistulas that were

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closed using a transcatheter approach and an Amplatzar vascular plug. In the case presented by Kassaian et al., a large fistula originating in the right coronary artery and terminating in the right

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ventricle was closed using a transcatheter approach and Amplatzar vascular plug that occluded the fistula at its narrowest part. The surgery was successful and follow-up continued to be

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positive at the time of publication [86]. Kassaian et al. suggested that Amplatzar vascular plugs

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provide one of the best transcatheter closure techniques due to the variety of available sizes, ability to reposition after initial placement, and overall safety; however, standard use criteria has

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not yet been established for these vascular plugs [86]. Since 2008, the use of Amplatzar plugs

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has gained popularity, and is now more commonly used [87-89], however little evidence appears in the medical literature regarding the safety and feasibility of this treatment and, a standard application technique has yet to be established.

Balloon stent grafts are also popular in coronary artery fistula closure techniques. Unfortunately, closures with these grafts have been associated with a high risk of in-stent thrombosis or restenosis. Due to this, they are often indicated when bypass grafting of the coronary artery involved is part of the corrective regimen [83-86].

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ACCEPTED MANUSCRIPT As with any surgical endeavor, coronary artery fistula surgical and catheter repair have associated risks. These risks include transcatheter embolization that may cause ischemic

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electrocardiographic changes including device embolization, arrhythmias, and myocardial

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infarction. Additionally, a case reported death after a catheter procedure for coronary artery fistula caused by a device that recoiled into the left main coronary artery. To avoid short- and

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long-term complications associated with transcatheter procedures, follow-up angiographic

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studies must be regularly performed. Myocardial scintigraphy after transcatheter or surgical closure of coronary artery fistulas is also an important technique in follow-up in order to

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recognize and/or avoid recanalization, aneurysm, or myocardial infarction [4, 90, 91]. The Texas Heart Institute reported that there is a 2% overall mortality rate in surgical coronary artery fistula

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closures [82]. The majority of the deaths were associated with comorbidities including cardiac

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Management-

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lesions [82].

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Luo and colleagues suggest that there is potential for thrombotic events that may lead to myocardial infarctions after coronary artery fistula closure. Prophylactic low dose aspirin is suggested in such cases. In large postoperative coronary artery dilations, anticoagulant therapy such as warfarin is recommended [4]. Angina secondary to coronary artery fistula is managed according to the standard-of-care guidelines for angina medical management. As such, betablockers, calcium channel blockers, and nitrates may be prescribed. If additional medical intervention is used, regular follow-up must be performed to prevent new fistulas ,increased dilation or shunting of existing fistulas [4].

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ACCEPTED MANUSCRIPT ConclusionCoronary artery fistulas, while rare, are pathophysiologically important and should be included

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in the differential diagnosis of cardiac-associated pathologies. Proper recognition, imaging,

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diagnosis, treatment, and symptom management can prevent potentially deadly cardiac complications associated with these anomalous communications. This review highlights the best

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the prevalence for both adult and pediatric patients.

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imaging and treatment techniques for coronary artery fistulas, along with information describing

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ACCEPTED MANUSCRIPT Figure Legends

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Figure 1. This figure is a lower cross sectional view of a normal heart exhibiting key anatomical

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landmarks; left and right ventricles, interventricular septum and anterior interventricular artery a branch of the left coronary artery. Source: Diane Spicer, Department of Pediatrics-Cardiology,

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University of Florida, Gainesville, Florida

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Figure 2. This figure is taken from a dissected right atrium showing the termination of a Coronary Artery Fistula into the wall of the atrium. Source: Diane Spicer, Department of

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Pediatrics-Cardiology, University of Florida, Gainesville, Florida

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Figure 3. This figure is an anterior view of the heart showing the anterior interventricular artery

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as it gives a fistulous communication terminating in the pulmonary trunk. Source: Diane Spicer, Department of Pediatrics-Cardiology, University of Florida, Gainesville, Florida

Figure 4. This figure is taken from a dissected atrial heart showing a fistulous communication from the right coronary artery to the right atrial appendage. Source: Diane Spicer, Department of Pediatrics-Cardiology, University of Florida, Gainesville, Florida

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ACCEPTED MANUSCRIPT Figure 5. This figure is an illustration of Type 1 classification of a Coronary Artery Fistula. It illustrates a superior and longitudinal view of the heart showing the termination of the coronary

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artery fistula from the right coronary artery into the right atrium (Top) and the left coronary

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Anatomical Sciences St. George’s University, Grenada

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artery into the left atrium (bottom). Source: Jessica Holland, Medical Illustrator, Department of

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Figure 6. This figure is an illustration of Type 2 classification of a Coronary Artery Fistula. It illustrates a superior and longitudinal view of the heart showing the termination of the coronary

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artery fistula from the right coronary artery to the right atrium (top left); left coronary artery to the right atrium (bottom left); right coronary artery to the left atrium (top right) and the left

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coronary artery to the left atrium (bottom left). This fistulous communication passes between the

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atriums to drains into the posterior aspect of the atria. Source: Jessica Holland, Medical

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Illustrator, Department of Anatomical Sciences St. George’s University, Grenada

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Figure 7. This figure is an illustration of Type 3 classification of a Coronary Artery Fistula. It illustrates a superior and longitudinal view of the heart showing the termination of the coronary artery fistula from the right coronary artery to the right atrium (top left); left coronary artery to the right atrium (bottom left); right coronary artery to the left atrium (top right) and the left coronary artery to the left atrium (bottom right). This fistulous communication terminates in the posterior surface of the atria after passing along the atrioventricular groove. Source: Jessica Holland, Medical Illustrator, Department of Anatomical Sciences St. George’s University, Grenada

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ACCEPTED MANUSCRIPT Figure 8. This figure is taken from a dissected heart showing the termination of a Coronary Artery Fistula into the left ventricle from the anterior interventricular artery (a branch of the left

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coronary artery). Source: Jessica Holland, Medical Illustrator, Department of Anatomical

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Sciences St. George’s University, Grenada

Acknowledgements: The authors wish to thank Jessica Holland, MS, Medical Illustrator at St.

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George's University, Grenada, West Indies, for the creation of her illustrations used in this

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publication.

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ACCEPTED MANUSCRIPT References1. Ashraf SS, Shaukat N, Fisher M, Clarke B, Keenan DJ. 1994. Bicoronary-pulmonary

RI P

coronary-pulmonary fistula. Eur Heart J 15:571-574.

T

fistulae with coexistent mitral valve prolapse: a case report and literature review of

2. Tiryakioglu S, Gocer H, Tiryakioglu O, Kumbay E. 2010. Multiple Coronary-Cameral

SC

Fistulae. Tex Heart Inst J 37:378-379.

NU

3. Vlodaver Z, Neufeld H, Edwards J. 1975. Coronary Arterial Variations in the Normal Heart and in Congenital Heat Disease. London: Academic Press, Inc, p 43-78. Luo L, Kebede S, Wu S, Stouffer, GA. 2006. Coronary Artery Fistulae. Am J Med Sci

MA

4.

332: 79–84.

ED

5. Yamanaka O, Hobbs RE. 1990. Coronary artery anomalies in 126,595 patients

PT

undergoing coronary arteriography. Cathet Cardiovasc Diagn 21: 28-40. 6. Gasser S, Gasser R, Bareza N, Klein W. 2003. Iatrogenic coronary fistula in post

AC

21.

CE

transplant patients: Pathogenesis, Clinical Features and Therapy. J Clin Bas Cardiol 6:19-

7. Burch GH, Sahn DJ. 2001. Congenital coronary artery anomalies: the pediatric perspective. Coron Artery Dis 12: 605–616. 8. Sandhu JS, Uretsky BF, Zerbe TR, Goldsmith AS, Reddy PS, Kormos RL, Griffith BP, Hardesty RL. 1989. Coronary artery fistula in the heart transplant patient: a potential complication of endomyocardial biopsy. Circulation 79: 350–356. 9. Atler B, Wheeling J, Martin H, Murgo J, Treasure R, McGranahan G. 1977. Traumatic Right Coronary Artery-Right Ventricular Fistula with Retained Intramyocardial Bullet. Am J Cardiol 40: 815-819.

22

ACCEPTED MANUSCRIPT 10. Hobbs RE, Millit HD, Raghavan PV, Moodie DS, Sheldon WC. 1982. Coronary artery fistulae: a 10-year review. Cleve Clin J 49:191–7.

T

11. Michaelsson M, Ho SY. 2000. Congenital Heart Malformations in Mammals. London:

RI P

Imperial College Press, p 60.

12. Leach S, Fine D, Schutrumpf R, Britt L, Durham H, Christiansen K. 2010. Coil

SC

embolization of an aorticopulmonary fistula in a dog. J Vet Cardiol 12:211-216.

NU

13. McNamara JJ, Gross RE. 1969. Congenital coronary artery fistula. Surgery 65: 59-69. 14. Qureshi S. Coronary arterial fistulas. 2006. Orphanet J of Rare Dis 1:51.

MA

15. Levin DC, Fellows KE, Abrams HL. 1978: Hemodynamically significant primary anomalies of the coronary arteries. Circulation 1978, 58:25-34. PubMed Abstract.

ED

16. Ogden J, Stansel HC. 1974. The Anatomic Variability of Coronary Arterial Fistulae

PT

Termination in the Right and Left Atria. Chest 65: 76-81. 17. Neufeld HN, Lester R, Adams P, Anderson R, Lillehei W, Edwards J. 1961. Congenital

CE

communication of a coronary artery with a cardiac chamber or the pulmonary trunk.

AC

Circulation 24:171-179.

18. Valdiva E, Rowe G, Angevine DM. 1957. Large congenital aneurysm of the right coronary artery. Arch Pathol 63:168-171. 19. Edwards JE, Gladding TC, Weir AB. 1958. Congenital communication between the right coronary artery and right atrium. J Thorac Surg 35: 662-673. 20. Rose AG. 1978. Multiple Coronary Arterioventricular Fistulae. Circulation 58:178-180. 21. Rittenhouse EA, Doty DB, Ehrenhaft JL. 1975. Congenital coronary artery-cardiac chamber fistula: review of operative management. Ann Thorac Surg 20: 468–85.

23

ACCEPTED MANUSCRIPT 22. Liberthson RR, Saga K, Berkohen JP,Weintraub RM, Levine FH . 1979. Congenital coronary arteriovenous fistula. Report of 13 patients, review of the literature and

T

delineation of management. Circulation 59: 849–854.

RI P

23. Heidenreich F, Leon D, Shaver J. 1969. A Case of Anomalous Right Coronary Artery to Right Atria1 Fistula Presenting as Atypical Aortic Insufficiency. Am J Cardiol 23: 453-

SC

457.

NU

24. Sherwood MC, Rockenmacher S, Colan SD, Geva D. 1999. Prognostic significance of clinically silent coronary artery fistulas. Am J Cardiol 83: 407–411.

MA

25. Cheung DLC, Au WK, Cheung HHC, Chiu CS, Lee WT. 2001. Coronary artery fistulas: long-term results of surgical correction. Ann Thorac Surg 71: 190–195.

ED

26. Mangukia CV. Coronary Artery Fistula. Ann Thorac Surg. 2012 Jun;93(6):2084-92.

PT

27. Baim D, Kline H, Silverman J. 1982. Bilateral coronary artery to pulmonary artery fistulas: report of 5 cases and review of literature. Circulation 65:810–815.

CE

28. Mehta D, Redwood D, Ward DE. 1987. Multiple bilateral coronary arterial to pulmonary

AC

artery fistulae in an asymptomatic patient. Int J Cardiol16: 96–98. 29. McLellan BA, Pelikan PCD. 1989. Myocardial infarction due to multiple coronaryventricular fistulas. Cathe Cardiovasc Daign 16:247–9. 30. Jacobs GJ, Calvert CA, Hall DG, Kraus M. 1996. Diagnosis of right coronary artery to right atrial fistula in a dog using two- dimensional echocardiography. J Small Anim Pract 37: 387-390. 31. Piciche M, De Paulis R, Chiariello L. 1999. A review of aorto- pulmonary fistulas in aortic dissection. Ann Thorac Surg 68: 1833-1836. 32. Endara A, Corekeron MA, Diger AM, Neal AJ, Kang D. 2001. Pneumococcal aortic

24

ACCEPTED MANUSCRIPT valve endocarditis causing aortopulmonary artery fistula. Ann Thorac Surg 72: 17371738.

T

33. Ata Y., Turk T., Bicer M., Yalcin M., Ata F., and Yavuz S. 2009. Cononary

RI P

arteriovenous fistulas in the adults: Natural history and management strategies. J of Cardiothoracic Surg, 2009; 4:62.

SC

34. Taleb MM, Sheikh MA, Cooper CJ, Tinkel JL.Multiple coronary to pulmonary artery

NU

fistulas: a case report and review of the literature.Cardiovasc Interv Ther. 2012 May;27(2):127-30

MA

35. Angelini P., Velasco J.A., Flamm S., 2002. Coronary Anomalies: Incidence, Pathophysiology and Clinical Relevance. Circulation: J of the AHA 2002; 105:2449-

ED

2454

PT

36. Mechleb W., Abboud L., Mattar C., Haddadin T., 2013. Case Report and review of literature: Coronary Artery Fistulae. Tenn Med 2013 106(7): 39-41

CE

37. Mavroudis C, Backer L, Rocchini A, Muster A, Gevitz M. 1997. Coronary Artery

AC

Fistulas in Infants and Children: A Surgical Review and Discussion of Coil Embolization. Ann Thorac Surg 63:1235-1242. 38. Stierle U, Giannitsis E, Sheikhzadeh A, Potratz J. 1998. Myocardial ischemia in generalized coronary artery–left ventricular microfistulae. Int J Cardiol 63:47–52. 39. Roubille F, Micheau A, Vernhet-Kovacsik H. 2011. Multiple coronary-left ventricular fistulae associated with apical hypertrophic cardiomyopathy: Coronary angiogram compared to coronary scan and cardiac magnetic resonance scan. Cardiol J 18: 702–703. 40. Urcelay G, Ludomirsky A, Vermilion R, Serwer G, Mosca R, Bove E. 1995. Acquired Coronary Artery Fistulae After Right Ventricular Myotomy and/or Myomectomy for

25

ACCEPTED MANUSCRIPT Congenital Heart Disease. Am J Cardiol 75: 408-411. 41. Schumacher G, Roithmaier A, Lorenz HP, Meisner H, Sauer U, Müller KD, Sebening F,

T

Bühlmeyer K. 1997.Congenital coronary artery fistula in infancy and childhood:

RI P

diagnostic and therapeutic aspects. Thorac Cardiovasc Surg 45: 287–94. 42. Fukudo K, Handa S, Ogawa S, Ohnishi S, Nakamura Y. 1988. Noninvasive Evaluation of

SC

Right Coronary Artery-Right Atrial Fistula Using Two-Dimensional Echocardiography,

NU

Pulsed Doppler Echocardiography and Color Flow Mapping. Cardiology 75: 375-380. 43. Tsubata S, Ichida F, Miyawaki T. 1998. Noninvasive diagnosis of coronary arterial

MA

fistulas using multiplanar cine magnetic resonance imaging. Cardiol Young 8: 250–252. 44. McElhinney DB, Burch GH, Kung GC, Villegas MD, Silverman NH, Moore P. 2000.

ED

Echocardiographic Guidance for Transcatheter Coil Embolization of Congenital

PT

Coronary Arterial Fistulas in Children. Pediatr Cardiol. 21: 253–258. 45. Aydinlar A, Cicek D, Enturk T, Gemici K, Serdar O, Kazazoglu A, Kumbay E, Corda J.

CE

2005. Primary Congenital Anomalies of the Coronary Arteries: A Coronary

AC

Arteriographic Study in Western Turkey. Int Heart J 46: 97-103. 46. Giannoccaro PJ, Sochowski RA, Morton B C, Chan KL. 1993. Complementary role of transoesophageal echocardiography to coronary angiography in the assessment of coronary artery anomalies. Br Heart J 70:70-74. 47. Dawn B, Talley J, Prince C, Hoque A, Morris G, Xenopoulos N, Stoddard M. 2003. Two-dimensional and Doppler Transesophageal Echocardiographic Delineation and Flow Characterization of Anomalous Coronary Arteries in Adults. J Am Soc Echocardiogr 16: 1274-1286. 48. Woo J, Koh Y, Ha S, Chang K, Hong S. 2011. Non-invasive recognition of generalized

26

ACCEPTED MANUSCRIPT coronary arteriosystemic fistulae by contrast echocardiography and multidetector CT. Int J Cardiovasc Imaging 27:749–753.

T

49. Agatston A, Chapman E, Hildner F, Samet P. 1984. Diagnosis of a Right Coronary

RI P

Artery- Right Atrial Fistula Using Two- Dimensional and Doppler Echocardiograph. Am J Cardiol 54: 238-239.

SC

50. Lessick J, Kumar G, Bevar R, Lorber A, Engel A. 2004. Anomalous origin of a posterior

NU

descending artery from the right pulmonary artery: report of a rare case diagnosed by multidetector computed tomography angiography. J Comput Assist Tomogr 28: 857-9.

MA

51. Parga JR, Ikari NM, Bustamante LNP, Rochitte CE, A’Vila L, Oliveira A. 2004. MRI evaluation of congenital coronary artery fistulae. Br J Radiol 77:508–511.

ED

52. Ankersmit HJ, Loewe C, Hacker S, Hoetzenecker K, Grimm M. 2008. Gigantic Coronary

PT

Fistula. Wien Klin Wochenschr 120:152. 53. Schmitt R, Froehner S, Brunn J, Wagner M, Brunner, H; Cherevatyy, O. 2005.

CE

Congenital anomalies of the coronary arteries: imaging with contrast-enhanced,

AC

multidetector computed tomography. Eur Radiol 15: 1110–1121. 54. Funabashi N, Komuro I. 2006. Aberrant fistula arteries from the left main branch and right coronary artery to the left pulmonary arterial sinus demonstrated by multislice computed tomography. Int J Cardiol 106: 428–430. 55. Kate GJR, Weustink AC, de Feyter PJ. 2008. Coronary artery anomalies detected by MSCT-coronary angiography in the adult. Neth Heart J 16: 369-375. 56. Yiginer O, Bas S, Feray H. 2009. Demonstration of coronary-to-pulmonary fistula with MDCT and conventional angiography. Int J Cardiol 134: 126–128. 57. Gillebert C, van Hoof R, Van der Werf F, Peissens J, de Geest H. 1986. Coronary artery

27

ACCEPTED MANUSCRIPT fistulas in an adult population. Eur Heart J 7: 437–43. 58. Boxer RA, LaCorte MA, Singh S, Ishmael R, Cooper R, Stein H. 1989. Noninvasive

RI P

resonance imaging. Pediatr Cardiol 10: 45–47.

T

diagnosis of congenital left coronary artery to right ventricle fistula by nuclear magnetic

59. Velvis H, Schmidt KG, Silverman NH, Turley K. 1989. Diagnosis of coronary artery

NU

imaging. J Am Coll Cardiol 14: 968–976.

SC

fistula by two-dimensional echocardiography pulsed Doppler ultrasound and color flow

60. Fernandes ED, Kadivar H, Hallman GL, Reul GJ, Ott DA, Cooley DA. 1992. Congenital

MA

malformations of the coronary arteries: the Texas Heart Institute experience. Ann Thorac Surgery 54: 732.

ED

61. Kubota S, Suzuki T, Murata K. 1991. Cine magnetic resonance imaging for diagnosis of

PT

right coronary arterial-ventricular fistula. Chest 100: 735–737. 62. Said S, el Gamal M, Van der Werf T. 1997. Coronary arteriovenous fistulas: collective

CE

review and management of six new cases-changing etiology, presentation, and treatment.

AC

Clin Cardiol 20:748–52. 63. Duerinckx AJ, Shaaban A, Lewis A, Perloff J, Laks H. 2000. 3D MR imaging of coronary arteriovenous fistulas. Eur Radiol 10: 1459–1463. 64. Lida R, Yamamoto T, Suzuki T, Saeki S, Ogawa S. 2005. The usefulness of intraoperative transesophageal echocardiography to identify the site of drainage of coronary artery fistula. Anesth Analg 101: 330–331. 65. Bjoerk VO, Bjoerk L. 1965. Coronary artery fistula. J Thorac Cardiovasc Surg 49:921930. 66. Armsby LR, Keane JF, Sherwood MC, Forbess JM, Perry SB, Lock JE. 2002.

28

ACCEPTED MANUSCRIPT Management of coronary artery fistulae: patient selection and results of transcatheter closure. J Am Coll Cardiol 39:1026–32.

T

67. Mielke G, Sieverding L, Borth-Bruns T, Eichhorn K, Wallwiener D, Gembruch U. 2002.

fistula. Ultrasound Obstet Gynecol 19: 612-615.

RI P

Prenatal diagnosis and perinatal management of left coronary artery to right atrium

SC

68. Sharland GK, Tynan M, Qureshi SA. 1996. Prenatal detection and progression of right

NU

coronary artery to right ventricle fistula. Heart 76: 79–81. 69. Chaoui R, Tennstedt C, Göldner B, Bollmann R. 1997. Prenatal diagnosis of ventriculo-

MA

coronary communications in a second-trimester fetus using transvaginal and transabdominal color Doppler sonography. Ultrasound Obstet Gynecol 9:194 –7.

ED

70. Chaoui R, Machlitt A, Tennstedt C. 2000. Prenatal diagnosis of ventriculo-coronary

PT

fistula in a late first-trimester fetus presenting with increased nuchal translucency. Ultrasound Obstet Gynecol 15: 160-162.

CE

71. Jiang Z, Chen H, Wang J.Right coronary artery fistula to left ventricle treated by

AC

transcatheter coil embolization: a case report and literature review.Intern Med. 2012;51(11):1351-3. 72. Schanzenbächer P, Bauersachs J. 2003. Acquired right coronary artery fistula draining to the right ventricle: angiographic documentation of first appearance following reperfusion after acute myocardial infarction, with subsequent spontaneous closure. Heart 89:22-23. 73. Lipiec P, Peruga M, Kr emin ska-Pakula M, Forys’ J, Dro d J, Kaspr ak J. 2004. Right Coronary Artery–to-Right Ventricle Fistula Complicating Percutaneous Transluminal Angioplasty: Case Report and Review of the Literature. J Am Soc Echocardiogr 17: 280283.

29

ACCEPTED MANUSCRIPT 74. Hirzallaha M, Horlick E, Zelovitzky L. 2010. Coronary artery to main pulmonary artery fistulae via a Vieussens’ arterial ring. J Cardiovasc Comput Tomogr 4:339–341.

coronary artery fistulas. Heart 85: 1–4.

RI P

T

75. Schleich JM, Rey C, Gewillig M, Bozio A. 2001. Spontaneous closure of congenital

76. Lowe JE, Oldham HN Jr, Sabiston DC Jr. 1981. Surgical management of congenital

SC

coronary artery fistulas. Ann Surg 194:373–380.

NU

77. Wang S, Wu Q, Hu S, Xu J, Sun L, Song Y, Lu F. 2001. Surgical treatment of 52 patients with congenital coronary artery fistulas. Chin Med J 114:752–755.

MA

78. Kamiya H, Yasuda T, Nagamine H, Sakakibara N, Nishida S, Kawasuiji M, Watanabe G. 2002. Surgical treatment of congenital coronary artery fistulas: 27 years' experience and a

ED

review of the literature. J Card Surg 17: 173-177.

PT

79. Harikrishnan S, Bimal F, Ajithkumar V, Bhat A, Krishnamoorthy KM, Sivasubramonian S, Titus T, Tharakan J. 2011. Percutaneous treatment of congenital coronary

CE

arteriovenous fistulas. J Interv Cardiol 24: 208-215.

AC

80. Jama A, Barsoum M, Bjarnason H, Holmes D, Rihal C. 2011. Percutaneous Closure of Congenital Coronary Artery Fistulae Results and Angiographic Follow-Up. Jacc Cardiovasc Interv 4: 814-821. 81. Bjork G, Crafoord C. 1947. Arteriovenous aneurysm on the pulmonary artery simulating patent ductus arteriosus Botalli. Thorax 2: 65-74. 82. Reul R, Cooley D, Hallman G, Reul G. 2002. Surgical Treatment of Coronary Artery Anomalies: Report of a 371⁄2-Year Experience at the Texas Heart Institute. Tex Heart Inst J 29: 299-307. 83. Kassaian SE, Mahmoodian M, Salarifar M, Alidoosti M, Abbasi SH, Rasekh A. 2007.

30

ACCEPTED MANUSCRIPT Stent-graft exclusion of multiple symptomatic coronary artery fistulae. Tex Heart Inst J 34: 199-202.

T

84. Oto A, Aytemir K, Çil B, Peynircioğlu B, Yorgun H, Canpolat U, Kaya EB. 2011.

RI P

Percutaneous closure of coronary artery fistulae in adults with intermediate term followup results. J Interv Cardiol 24: 216-22.

SC

85. Kabbani Z, Garcia-Nielsen L, Lozano M, Febles T, Febles-Bethencourt T, Castro A.

Cardiovasc Revasc Med 9:14–17.

NU

2008. Coil embolization of coronary artery fistulas. A single-centre experience.

MA

86. Kassaiain S, Alidoosti M, Sadeghian H, Dehkordi M. 2008. Transcatheter Closure of a Coronary Fistula with an Amplatzer® Vascular Plug Should a Retrograde Approach Be

ED

Standard? Tex Heart Inst J 35:58-61.

PT

87. Bialkowski J; Szkutnik M; Fiszer R; Zembala M. 2011. Transcatheter cocclusion of a

1318–1319.

CE

large coronary artery fistula using a patent ductus arteriosus. Kardiologia Polska 12:

AC

88. Said S; Nijhuis R; op den Akker J; Kimman G, Van Houwelingen K; Gerrits D; Huisman A; Slart R; Nicastia D; Koomen E; Trans A; Al-Windy N; Sonker U; Slagboom T; Pronk A. 2011. Diagnostic and therapeutic approach of congenital solitary coronary artery fistulas in adults: Dutch case series and review of literature. Neth Heart J 19:183–191. 89. Yim D; Murray C; Bullock A. 2011. Computed tomography and occlusion of a right coronary artery to the left atrial fistula. Cardiol Young 21: 585–586. 90. Mesko ZG, Damus PS. 1998. Myocardial infarction in a 14-year-old girl, ten years after surgical correction of congenital coronary artery fistula. Pediatr Cardiol 19: 366-368.

31

ACCEPTED MANUSCRIPT 91. Wang NK, Hsieh LY, Shen CT. 2002. Coronary arteriovenous fistula in pediatric

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MA

NU

SC

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patients: a 17-year institutional experience. J Formos Med Assoc 101: 177–82.

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