Author + information
- Received September 22, 2016
- Revision received January 11, 2017
- Accepted February 22, 2017
- Published online September 18, 2017.
- Balaji Krishnan, MD, MS∗ (, )
- Caroline Cross, MD,
- Richard Dykoski, MS, PA,
- David G. Benditt, MD,
- Mackenzie Mbai, MD,
- Edward McFalls, MD, PhD, MS,
- Jian-Ming Li, MD, PhD,
- Stefan Bertog, MD and
- Venkatakrishna N. Tholakanahalli, MD
- Cardiac Arrhythmia Center, Cardiovascular Division and Department of Pathology, University of Minnesota and Minneapolis VA Health Care System, Minneapolis, Minnesota
- ↵∗Address for correspondence:
Dr. Balaji Krishnan, Cardiac Electrophysiology Fellow, Cardiology Division, University of Minnesota, 420 Delaware Street SE, MMC 508, Minneapolis, Minnesota 55455.
Objectives The study examined the frequency in which a right coronary artery (RCA) anomaly resulting in intra-atrialization of the vessel might increase risk of RCA damage during routine radiofrequency ablation in the right atrium even with low power or temperature.
Background Right coronary artery (RCA) injury with endocardial RF ablation of the right atrium is a rare complication.
Methods This prospective observational study comprised an analysis of coronary artery anatomies in 331 patients who underwent autopsies at our institution from 2005 to 2014. The presence of intra-atrial RCA including the number and length of intra-atrial RCA segments with accompanying atherosclerosis and coronary anomalies were evaluated.
Results The authors report a case series of 6 of 331 (1.8%) patients in whom autopsies showed evidence of an intra-atrial RCA. The patients were all men (average 69 ± 12 years of age). They observed 3 variations of the intra-atrial RCA course. In 2 similar variations, the RCA entered the anterolateral aspect of the right atrium, returning to its normal distribution to supply the distal RCA (case 4 of 6) and the atrioventricular nodal artery (case 1 of 6). In the sixth case, the atrialized artery was an anterior branch of the RCA, in which the artery similarly coursed across the pectinate muscles, extending to the region of the anterior crista terminalis, before diving into the muscle.
Conclusions The prevalence and variants of the intra-atrial RCA have not been reported before. In the presence of an intra-atrial artery, RCA damage may occur due to direct injury rather than collateral injury due to transmural extension of an ablation lesion.
Radiofrequency (RF) catheter ablation of accessory pathways requires the application of energy to the endocardial surface of the atrioventricular groove adjacent to the major epicardial coronary arteries. During this procedure, the coronary artery may be damaged.
Coronary artery injury occurring in association with catheter ablation procedures has primarily occurred during ablation of accessory atrioventricular pathways and has been almost exclusively confined to the left coronary artery (1). However, although rare, the right coronary artery (RCA) may also be injured. Similarly, RCA injury rarely occurs as a resultant of cavotricuspid isthmus (CTI) ablation (2,3). In particular, a few clinical case studies have shown that RCA occlusion during RF ablation of typical atrial flutter (4–7). Similarly RCA injury has also been shown during cryoablation of CTI atrial flutter (8). The risk of injury is thought to be due to transmural proximity to the coronary artery.
The purpose of this study was to evaluate the anatomic relationship of the RCA to the right atrium and ventricle, to determine the frequency with which anomalies exist that may increase risk of direct injury to the coronary vessel during ablation within the right atrium.
We conducted a prospective observational study comprising consecutive subjects who had an autopsy performed at the Minneapolis Veterans Administration (VA) Health Care System (Minneapolis, Minnesota) between January 2005 and December 2014.
The study protocol was reviewed and approved by the institutional review board. Informed consent from the family of the deceased patients for autopsy was obtained in all cases.
Since 2000, 945 patients underwent autopsy at the Minneapolis VA with detailed heart dissection as part of the standard assessment. The first case of an atrialized RCA was observed in 2005. Since 2005, for subsequent autopsies (n = 331) a special protocol has been adopted for all heart specimens to undergo careful dissection by stripping the epicardium to display the major coronary and the atrial arteries. Each of the major coronary epicardial vessels had a complete description of the course of the coronary arteries relevant to the clinical series. Then the coronary arteries were individually transected along their course at 2-mm slices to display the vascular wall, intima, and lumen.
Anatomic dissection protocol for coronary vessels
Following postmortem examination, the heart is routinely fixed in formalin for 24 h. Thereafter, the entire length of the coronary arteries is dissected out of the epicardium, leaving a generous amount of surrounding adipose tissue. Then they are placed in decalcifying solution for approximately 12 h. Following decalcification, the coronary arteries are transected at 2-mm intervals and sequentially positioned on a glass panel superimposed on a coronary artery anatomy drawing (Figure 1A). Under a magnifying glass, each segment is then grossly examined for pathology. Specifically, the percent luminal stenosis is estimated with detailed description of eccentric and circumferential lesions of the vessel walls. These lesions are subsequently depicted on a hand-drawn 2-dimensional coronary artery anatomy diagram, producing an overall representation of the coronary artery pathology (Figure 1B). Subsequently, gross digital photographs are taken for further mathematical computation and pathologic documentation. Representative sections of lesions and normal coronary artery segments are then submitted for histological examination. This technique was developed by Mr. Richard Dykoski, who is specialized in assessing coronary anatomy in cardiac dissections, which we have termed the Dykoski method.
The intra-atrial coronary artery is the segment of the RCA that is intracavitary in the right atrium without any myocardial interface between the blood pool and the vessel adventitia.
The atrialized coronary artery is a segment of the RCA that traverses the epicardial surface of the heart, displaced superiorly from the usual position within the atrioventricular groove to a more atrialized location on the atrial aspect of the atrioventricular groove. This is an uncommon position for the right coronary vessel.
Myocardial bridging is a band of myocardial fibers overlaying a segment of coronary artery along some part of their subepicardial; fibers of ventricular origin are known as myocardial bridges, whereas those of atrial origin are referred to as myocardial loops.
Intramyocardial vessels are vessels surrounded by myocardial fibers and usually considered deep myocardial bridged vessels, whereas myocardial fibers that cross the tunneled coronary artery perpendicularly or at an acute angle are considered superficial.
We report a case series of 6 patients with an intra-atrial course of the RCA within the right atrial chamber. These cases were identified among 331 autopsies in which a standard protocol for examination of the coronary arteries was followed (1.8%).
Index case report
A 68-year-old man with past medical history of diabetes mellitus, nonischemic cardiomyopathy with left ventricular ejection fraction of 45% to 50%, chronic obstructive pulmonary disease, and hypertension with atrial flutter. He underwent a CTI-dependent atrial flutter ablation. An 8-mm-tip catheter was used. Temperature was limited to 60°C, powered to 50 W. The procedure was successful, with no ischemic electrocardiographic signs or symptoms noted during ablation or afterward while monitored on cardiac telemetry. Twenty-four hours after the procedure, he expired due to pulseless electrical activity. Postmortem examination revealed extensive bilateral pleural effusions and diffuse alveolar damage. The heart showed cardiomegaly with biventricular hypertrophy, coronary atherosclerosis, and focal myocardial necrosis in the posterior wall of the left ventricle. The right atrium revealed several areas of recent hemorrhage on the lateral edge of the eustachian ridge, lateral pectinate muscles, and the tricuspid valve (Figure 2). The sectioned coronary artery showed severe atherosclerosis at the site of hemorrhagic necrosis due to the ablation and delayed thrombus in the distal RCA. According to the autopsy pathology, thrombus was not at the sites of ablation but rather distal to the sites of ablation. The pathologist deemed the cause of death as respiratory arrest secondary to acute respiratory distress syndrome with subsequent pulseless electrical activity. We noted that a portion of RCA appeared intra-atrial without any atrial myocardium separating the endocardium from the arterial adventitia (Figure 3).
In all of these scenarios (types I, II, and III), the coronaries start in the usual location within the aorta valve sinus. As well, the aforementioned exposed segment is often displaced superiorly from the usual position within the atrioventricular groove to a more atrialized location (3–5). In this new locality, the exposed segment may be positioned within the CTI, which is a common site of typical atrial flutter ablation. The RCA then travels along the atrioventricular groove in the epicardial fat along the atrial aspect of the atrioventricular groove, giving off normal marginal branches extending inferiorly to the ventricle.
In 4 cases, the RCA entered the anterolateral atrial chamber from the atrioventricular groove, at a distance of 3.4 to 4.0 cm from its origin, in the aortic sinus of Valsalva. The RCA deviated to the atrial aspect of the atrioventricular groove in the epicardial fat and penetrated the right atrial wall for a few centimeters running on or into the pectinate muscles. The artery than penetrated the right atrial wall a second time just proximal to the inferior vena cava, returning to its normal distribution within the posterior longitudinal sulcus. The length of the intra-atrial segment of the RCA in the 4 described cases ranged from 1.4 to 3.9 cm (mean 2.2 cm) (Figure 4).
In the fifth case, the RCA entered the anterolateral atrial chamber from the atrial aspect of the atrioventricular groove, at a distance of approximately 3.0 cm from its origin in the aortic sinus. It penetrated the right atrial wall, and then traversed the right atrial chamber along the endocardial surface of the annulus and into the pectinate muscles. The artery exited the right atrium just proximal to inferior vena cava, returning to supply the atrioventricular nodal artery and distal RCA. The length of the intra-atrial segment of the RCA in this case was 3.6 cm (Figure 5). The aforementioned exposed segment was displaced superiorly from the usual position within the atrioventricular groove to a more atrialized location.
In the sixth case, the intra-atrial artery was an anterior branch of the RCA, extending superiorly over the right atrial epicardium and penetrating the right atrial wall. This branch ran through and on the pectinate muscles where it supplied blood to the crista terminalis before diving into the muscle (Figure 6).
In our study, the intra-atrial vessel segments lacked significant atherosclerosis in all 6 cases. Cases 1 and 2 showed focal 20% to 40% luminal stenosis within the intra-atrial segment. All cases showed right coronary dominance. No accompanying alternative coronary artery anomalies were identified in any of the 6 cases, including myocardial bridging (Table 1).
The present study is the first to demonstrate 3 variants of the intra-atrial right coronary anomaly and shows that prevalence is higher than previously described in the literature. In our study, following a standardized protocol of coronary artery examination, a somewhat higher prevalence of 1.8% is demonstrated. This is a small case series in a VA hospital population of almost entirely male autopsy cases. However, this anomaly appears to be more common than previously described.
The intra-atrialized RCA (IARCA) has a prevalence of 0.09% to 0.10% by single coronary bypass surgery and autopsy series (9,10) and 0.15% by coronary computed tomography angiography (11). In the autopsy study of McAlpine et al. (10) on 1,000 dissected and nondiseased heart specimens, the authors found only 1 RCA to be in an intracavitary position (0.1%). Similar results were reported by Ochsner and Mills (9), who encountered 4 IARCAs among 4,414 patients (0.09%) operated for coronary bypass grafting. Since that time, there has been a single compiled study on the prevalence of the IARCA as studied by coronary computed tomography angiography (11).
In the absence of a planned intra-atrial procedure such as a cavotricuspid ablation, an aberrant intra-atrial course of the RCA is of little consequence and does not produce physiologic symptoms or result in abnormal pathology (12). However, as illustrated by the case described previously, atrialization of the RCA or 1 of its branches may result in arterial injury during ablation within the right atrial chamber. IARCA increases chances of patient complaining chest pain or direct damage in some cases of crystal atrial tachycardia while performing the ablation. Anatomic reports have focused on avoiding septal or lateral RF delivery during CTI ablation because the posterior descending artery and proximal posterior lateral RCA branches are located close to the septal portion of the CTI, most commonly reported with ablation near the coronary sinus (13). Further, the RCA may bifurcate before the crux, either as an aberrant acute marginal artery or as an early posterior descending artery, crossing the diaphragmatic surface of the right ventricle along the lateral edge of the eustachian ridge, lateral pectinate muscles, and the tricuspid valve.
Risk of injury to coronary arteries is typically thought to be due to collateral damage due to proximity and orientation of the ablation lesion to the coronary artery. Other factors including lesion size and properties of RF energy are also known parameters that may determine the impact of RF ablation on coronary arteries (14). However, the coronary arteries course mostly on the ventricular side of the atrioventricular groove; therefore, during ablation within the right atrium, there is little risk of injuring coronary arteries. A major protective factor to coronary artery injury is convective cooling. Initially described in the setting of anti–malignant hyperthermia treatment (15), convective cooling results from the flow of intracardiac and microvascular blood, which creates a heat sink. In general, the susceptibility of coronary arteries to thermal damage is inversely proportional to the electrode-to-artery distance (16). When RF ablation is delivered to a tissue through an electrode, temperature gradients are created as heat moves from the tip through the tissue. Because the temperature decreases through tissue in a hyperbolic fashion (15), the likelihood of thermal injury to coronary arteries also decreases as distance from the catheter tip increases.
Whether the application of RF in the vicinity of coronary arteries predisposes to late coronary stenoses is not known. Evidence of persistent injury without acute occlusion has been observed in animal models. After RF ablation near coronary arteries, minimal angiographic changes are observed in the short term. However, between 3 and 9 months after ablation, intimal hyperplasia may develop that is not detectable angiographically. Bertram et al. (17) described 2 children who developed coronary artery stenosis, identified over 1 year after the initial ablation procedure. In 1 of the cases, ST-segment elevation was observed shortly after the ablation, but angiography after intracoronary nitroglycerin showed no abnormality. Other angiographic studies in patients with accessory pathways with several months of follow-up have not shown any angiographic abnormalities (18).
The anatomist remains a vital part of cardiovascular training. Through hundreds of hours of practice, not to mention significant prior knowledge and expertise, these dissections have played a vital role in providing the first descriptions of basic cardiac anatomy and complex anomalies. It is through this precedent that further discoveries are being made with advanced imaging. It is certain that increased use of 3-dimensional imaging techniques such as magnetic resonance imaging, computed tomography, and echocardiography will elucidate with more precision the association of various cardiac structures in 3-dimensional space.
The observations in this report are subject to a number of important limitations. First, in this study a standardized approach to evaluate intra-atrial anomalies was only begun after the initial index case even though the coronary dissection technique during autopsy described in this manuscript existed since 2005. Consequently, subtle forms of atrialized RCA segments might have been missed in earlier cases. Second, to demonstrate the structures after death, the prosector must remove the heart from the body and then dissect the epicardial tissue to identify the arteries. These processes, of necessity, produce some disruption of the initial arrangement. However intra-atrial location of the artery would not be expected from such dissection artifacts. In determining if the vessel is on the atrial aspect or ventricular aspect of the annulus, the distinction is made by observing the atrioventricular sulcus on the epicardium and the valve leaflet insertions on the endocardium. Even though these appear to be reliable landmarks, sometimes during dissection, they may not so clear. This may be better distinguished by imaging modalities such as computed tomography. Finally, because RF ablation was not present in autopsy cases subsequent to the initial index case, it is not possible with our data to quantitate the risk of arterial damage due to direct vascular contact during CTI ablation. If such a case series were present, the best control group would have been CTI ablation patients who died of an unrelated cause. We recognize this potential injury in only the 1 case summarized previously.
Typically, right-sided supraventricular tachycardias have low risk of coronary artery injury. Nonetheless, extra care should be paid when a patient complains of severe chest pressure during ablation. Any evidence for ST-segment elevation change in the inferior-posterior region should raise concern of possibility of RCA injury and possibility of an RCA branch atrialization anomaly. Consequently, although septal- or atrial-side RF delivery has been known to increase arterial injury risk during CTI, the variable anatomy of atrialized RCA branches suggests that even lateral RF delivery may increase risk.
COMPETENCY IN MEDICAL KNOWLEDGE: In this report we describe anomalies of the RCA that result in an intra-atrial course that may explain the rare injury to the RCA during RF ablation. We demonstrate that injury to the RCA is likely a result of direct injury to the coronary vessel during ablation within the right atrium rather than collateral damage due to proximity and orientation of the ablation lesion to the coronary artery.
TRANSLATIONAL OUTLOOK: Noninvasive imaging modalities such as computed tomography and magnetic resonance imaging may shed further light on the prevalence of these anatomic coronary artery variants. However, anatomic dissection still plays a significant role in discovery and in the continuing medical education of physicians.
Dr. Benditt has received grant support from the Dr. Earl E. Bakken Family. Dr. Tholakanahalli has received research funding from St. Jude Medical and has served as a partner of PATVIA One LLC. All other authors have reported that they have no relationships relevant to the contents of this paper to disclose.
All authors attest they are in compliance with human studies committees and animal welfare regulations of the authors’ institutions and Food and Drug Administration guidelines, including patient consent where appropriate. For more information, visit the JACC: Clinical Electrophysiology author instructions page.
- Abbreviation and Acronyms
- cavotricuspid isthmus
- intra-atrialized right coronary artery
- right coronary artery
- Veterans Administration
- Received September 22, 2016.
- Revision received January 11, 2017.
- Accepted February 22, 2017.
- 2017 American College of Cardiology Foundation
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