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AJR 2000; 174:1119-1125
© American Roentgen Ray Society


Review

Diagnostic Imaging of Thoracic Aortic Atherosclerosis

Paul A. Tunick1, Glenn A. Krinsky2, Vivian S. Lee2 and Itzhak Kronzon1

1 Department of Medicine, New York University School of Medicine, 560 First Ave., New York, NY 10016.
2 Department of Radiology, New York University School of Medicine, New York, NY 10016.

Received August 3, 1999; accepted after revision September 17, 1999.

 
Address correspondence to G. Krinsky


Introduction
Top
Introduction
Transesophageal Echocardiography
The Importance of a...
CT
MR Imaging
Therapy
Conclusion
References
 
As recently as 1989, large stroke databanks listed up to 40% of strokes as cryptogenic [1]. More recently, the thoracic aorta has been implicated as a source of cryptogenic strokes and peripheral organ damage because imaging techniques, including transesophageal echocardiography, CT, MR imaging, and MR angiography, have allowed the visualization, characterization, and quantification of atherosclerotic lesions in the thoracic aorta. We reviewed the imaging findings of thoracic aortic atherosclerosis and their clinical significance, the understanding of which has previously been derived from transesophageal echocardiography. We also reviewed the related developments in CT and MR imaging of atheromatous disease, including the characterization of plaque components on MR imaging.


Transesophageal Echocardiography
Top
Introduction
Transesophageal Echocardiography
The Importance of a...
CT
MR Imaging
Therapy
Conclusion
References
 
First developed in the 1970s [2], transesophageal echocardiography provides high-resolution images of the entire thoracic aorta except for a small part of the ascending aorta, which is blocked by the air column in the trachea.

Currently, transesophageal echocardiography is the procedure of choice for the detection, measurement, and characterization of thoracic aortic atheromas. Direct sonography has been used in the operating room to view atheromas in the ascending aorta [3], and transthoracic echocardiography has been used to view plaque in the ascending aorta and the aortic arch. In one study, 20 patients were examined with transthoracic and transesophageal techniques [4]. However, the resolution of images obtained with the transthoracic approach is worse than that of those obtained with the transesophageal approach. Higher resolution images can be obtained with intravascular sonography using high frequency transducers, and intravascular sonography has been successfully used in conjunction with thoracic aortic interventional procedures [5]. However, it is too invasive to be used as a diagnostic test for atheromatous disease and could result in iatrogenic embolization.

Transesophageal echocardiography is a safe minimally invasive procedure with a low risk of complications. It can be performed in various settings, from the operating room to the bedside. Moreover, it may be performed in conscious patients with local anesthesia, and a thorough examination of the thoracic aorta and the heart can be performed in 10 min or less. In 1990, researchers reported viewing atheromas in the thoracic aorta on transesophageal echocardiography in patients with embolic disease [6].

Plaque Thickness on Transesophageal Echocardiography
The normal aorta has a smooth intimal surface (<=1 mm thick) and can be seen on transesophageal echocardiography (Fig. 1). Atherosclerosis causes intimal thickening with the accumulation of lipid-laden foam cells and smooth muscle cells, which migrate from the media. Other features of atherosclerosis include ulceration (Fig. 2), calcification (Fig. 3), and a fibrous cap. The thickness of an intimal plaque, ulcerations, calcifications, and super-imposed mobile thrombi can be measured on transesophageal echocardiography. One study graded aortic plaque thickness in patients undergoing cardiac surgery with cannulation of the aorta for cardiopulmonary bypass [7]. The study included a five-grade ranking system: grade 1 = normal aorta, grade 2 = flat intimal thickening, grade 3 = protruding atheroma in the aortic lumen (< 5 mm) (Fig. 4), grade 4 = protruding atheroma (>= 5 mm) (Fig. 5), and grade 5 = atheroma with a mobile thrombus (Fig. 6). Patients with grade 5 disease had the highest risk of intraoperative stroke during cardiac surgery, which probably resulted from the dislodgment of atheroma and thrombus by the bypass cannula [7].



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Fig. 1. —72-year-old woman with mitral regurgitation. Transesophageal echocardiogram shows normal segment of thoracic aorta. Note smooth thin intimal layer (arrow).

 


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Fig. 2. —59-year-old man with left main coronary artery stenosis and transient ischemic attack. Transesophageal echocardiogram shows severe atherosclerosis of thoracic aorta with large ulcerated plaque (U).

 


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Fig. 3. —55-year-old woman with endocarditis. Transesophageal echocardiogram shows severe atherosclerosis of thoracic aorta with shadowing (S) of calcified plaque (arrow).

 


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Fig. 4. —75-year-old woman with stroke. Transesophageal echocardiogram shows moderate atherosclerosis of thoracic aorta with 3-mm intimal plaque (arrow).

 


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Fig. 5. —75-year-old woman with stroke. Transesophageal echocardiogram shows severe atherosclerosis of thoracic aorta with 7-mm protruding plaque (arrow).

 


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Fig. 6. —76-year-old woman with congestive heart failure and stroke. Transesophageal echocardiogram shows severe atherosclerosis and large protruding mobile thrombus (arrow).

 

The French Aortic Plaque in Stroke investigators used transesophageal echocardiography to characterize aortic arch plaque thickness in a group of patients with stroke [8]. They found that increasing plaque thickness imparted increasing risk, and patients with a plaque thickness of 4 mm or more had a significantly greater odds ratio. The odds ratio for aortic arch plaques (<1 mm) and stroke was 1.0 (no increased risk). The odds ratio was 3.9 for arch plaques between 1- and 3.9-mm thick and 13.8 for plaques greater than or equal to 4-mm thick.

Plaque Morphology and Plaque Thrombosis
Ulceration.—In 1992, a landmark autopsy study examined the thoracic aorta of 500 patients with stroke and other neurologic diseases [9]. Ulcerated plaques were present in the aortic arch of 26% of patients with cerebrovascular disease and in 5% of patients with other neurologic diseases. Of patients with cryptogenic stroke, 61% had aortic arch disease, the highest prevalence among all disease groups. Ulcerations (>=2 mm) diagnosed with transesophageal echocardiography are associated with a higher risk of stroke (Fig. 2). Such ulcerations were noted in 39% of patients with cryptogenic stroke, 8% with stroke of known cause, and 7% without stroke [10].

Calcification.—Although calcification represents one manifestation of the atherosclerotic process (Fig. 3), large high-risk plaques are often uncalcified; therefore, palpation of the aorta by a cardiac surgeon does not necessarily help to identify high-risk plaques [7]. The French Aortic Plaque in Stroke investigators examined plaque morphology on transesophageal echocardiography in 334 stroke patients over the age of 60 years [11]. Plaques greater than or equal to 4-mm thick had the highest risk for and an increased prevalence of ulceration, calcification, and hypoechoic areas. Hypoechoic areas are possibly indicative of a lipid core. Interestingly, it was the absence of calcification that imparted the greatest risk of stroke (odds ratio 10.3). Using an analogy with unstable coronary artery plaques, it is possible that the lipid-laden vulnerable plaques may be uncalcified. Support for this argument comes from a histologic examination of human aortic plaques that were intact as compared with those that had superimposed thrombi [12]. Furthermore, researchers noted the presence of plaque thrombosis as a characteristic of plaques with a high proportion of extracellular lipid content [12].

Superimposed thrombi.—Many protruding atheromas have mobile components such as thrombi. (Fig. 6) [13,14,15,16]. These mobile lesions may disappear after heparin or warfarin therapy [17, 18] or thrombolysis [19].

The unstable nature of plaques with thrombi.—A longitudinal study reported the results of repeat transesophageal echocardiography in patients with aortic atheromas [20]. In 11 (61%) of 18 patients, repeat imaging revealed new mobile lesions on plaques that were previously lesion free. Additionally, seven of 10 mobile lesions present during the first examination disappeared before follow-up. Research shows that these mobile lesions are responsible for high embolic risk and that embolization of thrombus from aortic atheromas has been documented with specimens removed from the femoral arteries of patients with acute limb ischemia [13, 14]. Furthermore, it is likely that cerebral embolization of thrombus from aortic atheromas causes stroke. Another embolic syndrome, atheroemboli syndrome with blue toes (which may occur in patients with aortic atherosclerosis), often accompanies renal failure or intestinal infarction. This syndrome is relatively uncommon, and was reported in 0.7% of patients treated with warfarin during the Stroke Prevention in Atrial Fibrillation-III trial [21].

One advantage of transesophageal echocardiography over other imaging techniques is its ability to reveal high-risk mobile thrombi in the thoracic aorta with real-time imaging.

Imaging the great vessels with transesophageal echocardiography.—Transesophageal echocardiography does not show the innominate artery because the tracheal air column obscures its origin. The ability to image the innominate artery is a significant advantage of CT and MR imaging, especially in patients with right brain events who have transesophageal echocardiograms with negative results. However, innominate atheromas are relatively uncommon [22].

Transesophageal echocardiography reveals the proximal portions of the left common carotid artery and the left subclavian artery [23]. Usually, the two arteries are not revealed in the same plane but each can be identified by distinct flow patterns on Doppler sonography. The subclavian artery has a high-resistance flow velocity pattern with relatively little or no diastolic flow. The common carotid artery has a pattern of low-resistance flow provided that the internal carotid artery is unoccluded.

Clinical Usefulness of Transesophageal Echocardiography in Patients with Thoracic Aortic Plaque
As mentioned previously, aortic atheromas may be responsible for stroke and peripheral emboli. These embolic events may be spontaneous or may result from aortic manipulation during cardiac surgery [24], balloon pump placement, or cardiac catheterization [25]. After the first report of strokes and peripheral emboli caused by atheromas appeared in 1990 [6], other case series [26,27,28] were followed by retrospective (case-control) [29,30,31] and prospective studies [32,33,34]. These studies reported the prevalence of significant thoracic aortic plaques (approximately 25% in stroke patients) and the future risk of stroke in patients with plaques (12% per year). An additional prospective study followed patients with ascending aortic plaques seen with epiaortic sonography during surgery [35]. The study reported a significant increase in future events and a higher mortality rate in patients with significant plaques. The mortality rate was 43% over 7 years in those with the severe-grade plaques (>5 mm, ulcerated, or mobile).

Although most clinicians think of carotid artery disease and atrial fibrillation as the most important causes of stroke, two recent studies report the prevalence of aortic atheromas on transesophageal echocardiography (21-27%) similar to that of carotid disease (10-13%) and atrial fibrillation (18-30%) [8, 30]. Therefore, transesophageal echocardiography may identify an atherosclerotic embolic source for cryptogenic strokes.

Transesophageal Echocardiography During Heart Surgery
Intraoperative transesophageal echocardiography is used to examine left ventricular wall motion and filling [36] and the success of valve reconstruction [37]. The amount of atherosclerotic plaque in the thoracic aorta has a major impact on the outcome of cardiac surgery. Patients with significant aortic arch atheromas have an intraoperative stroke rate that is approximately 12% [24]—five times higher than the general intraoperative stroke rate. It is possible that the identification of arch atheromas may allow surgeons to avoid cannulating directly in the lesions, thereby avoiding embolic complications.

Patients with aortic arch atheromas should avoid the newly developed minimally invasive technique using a port-access system. With this Heartport technique, surgeons pass a cannula with a balloon occluder (endoclamp) through the aorta from the femoral artery [38]. However, high-risk patients with significant aortic arch plaque may undergo coronary artery bypass on the beating heart (minimally invasive direct coronary artery bypass). During this procedure, while the heart is beating, internal mammary grafts are placed on the epicardial coronary arteries distal to obstructions. This procedure may avoid intraoperative strokes that can be caused by aortic cannulation in patients with arch atheromas [39].


The Importance of a Combined Sonographic Examination of the Carotid Arteries and the Thoracic Aorta in Stroke Patients
Top
Introduction
Transesophageal Echocardiography
The Importance of a...
CT
MR Imaging
Therapy
Conclusion
References
 
High resolution real-time sonography of the carotid arteries has been used for over 20 years [40], although originally, some concluded that the development of venous digital subtraction angiography would make further vascular sonography studies useless [41]. Currently, duplex scanning (real-time sonography combined with Doppler interrogation of carotid flow velocity) is the standard for the diagnosis of carotid stenosis and is often the first test performed to determine the cause of stroke in patients with normal sinus rhythms.

Researchers have found the association of thoracic aortic atheromas with stroke independent of carotid disease and atrial fibrillation [29,30,31]. All patients with carotid stenosis or atrial fibrillation were excluded from the first study, and in the other two studies thoracic aortic atheromas were independent predictors of stroke even when carotid disease and atrial fibrillation were controlled for multivariate analysis. However, it is not surprising that patients with symptomatic severe carotid artery atherosclerosis may also have severe atherosclerosis in the thoracic aorta. This association was reported in a retrospective study that found that stroke patients with severe carotid stenosis had a significantly higher prevalence of severe aortic arch atheromas (38%) than stroke patients without carotid stenosis (17%) [42]. That study also showed that patients with high-risk aortic arch plaques (with superimposed mobile thrombi) also had a high risk for carotid disease (>80% diameter stenosis on duplex scanning). In fact, the presence of mobile thrombi in the aortic arch was limited to patients with the most severe carotid stenosis. Therefore, it is reasonable to consider transesophageal echocardiography to examine the aortic arch in patients with carotid disease, especially if neurologic events are contralateral to carotid stenosis, if peripheral emboli are present, or if neurologic events occur in spite of technically successful carotid endarterectomy because there may be more than one source of emboli in these patients.


CT
Top
Introduction
Transesophageal Echocardiography
The Importance of a...
CT
MR Imaging
Therapy
Conclusion
References
 
The development of electron-beam CT to quantify coronary artery calcification and coronary atherosclerotic plaque burden [43,44,45,46] has paralleled similar developments using conventional CT to quantify calcifications of the aortic wall [47]. Unlike coronary artery imaging, the larger-sized aorta lends itself to easier quantification of noncalcified plaque, particularly with contrast-enhanced CT. This approach has been proposed as a valuable noninvasive method for following the progression and regression of atherosclerotic disease [48, 49].

Tenenbaum et al. [50] used unenhanced dualhelical CT to assess calcium deposits and areas of hypoattenuation adjacent to the aortic wall in 32 patients with recent stroke or embolic events. The authors found that defining a threshold of 4-mm thickness for protruding atheromatous plaques resulted in the best sensitivity (13/15; 87%) and specificity (14/17; 82%) for CT when compared with transesophageal echocardiography. This corresponds well to the threshold of 4 mm that was found in the French Aortic Plaque in Stroke study [8] to predict a significantly increased risk of stroke. Tenenbaum et al. also found that although unenhanced CT is suitable for screening studies, unenhanced dual-helical CT with positive results should be followed with contrast-enhanced CT (Figs. 7A,7B and 8) or transesophageal echocardiography. Notably, the authors also reported six protruding atheromas in the upper ascending aorta and proximal arch that were overlooked on transesophageal echocardiography. These cases highlight one advantage of CT over transesophageal echocardiography: CT provides complete imaging of the thoracic aorta, whereas transesophageal echocardiography does not.



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Fig. 7A. —82-year-old man with severe atherosclerotic disease. Contrast-enhanced helical CT scan at level of right main pulmonary artery reveals ulcerated plaque in ascending aorta (straight arrow) and descending thoracic aorta (curved arrow).

 


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Fig. 7B. —82-year-old man with severe atherosclerotic disease. Contrast-enhanced helical CT scan at level of bifurcation of main pulmonary artery shows protruding atheromas of ascending (solid arrow) and descending (open arrow) thoracic aortas.

 


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Fig. 8. —56-year-old man with history of peripheral embolic disease. Contrast-enhanced helical CT scan shows large presumably mobile thrombus in aortic arch (arrow).

 

New multidetector CT scanners with image acquisition times less than 1 sec are promising because, similar to electron beam CT, they may allow synchronous imaging with the cardiac cycle, thereby reducing artifacts (associated with cardiac motion) in the ascending aorta and the aortic root. Additionally, the temporal resolution of CT fluoroscopy may provide the ability to detect the mobile component of atheromas. However, such improvements in the detection and characterization of atheromatous plaque remain to be revealed.


MR Imaging
Top
Introduction
Transesophageal Echocardiography
The Importance of a...
CT
MR Imaging
Therapy
Conclusion
References
 
As early as 1983, Herfkens et al. [51] reported that MR imaging could be used to view aortic atherosclerosis. Using spin-echo imaging at 0.35 T, researchers were able to view aortic wall thickening and protruding atheromas in the abdominal aorta and pelvic vessels of patients in vivo. More recently, one group compared transesophageal echocardiography with MR angiography for examining protruding atheromas [52]. They found that MR angiography underestimated plaque thickness, probably because of difficulties in defining the aortic wall on the contrast-enhanced MR angiograms. Without ECG-gated cine gradient-echo images, MR imaging also provides static views of disease without assessing clinically significant mobile thrombus. However, similar to CT, MR imaging can reveal the complete aorta (including the blind spots of transesophageal echocardiography) and assess great vessel disease.

In addition to identifying morphologic features of atheromas, MR imaging reveals contrast between different tissue types that can be used to define the histologic components of atherosclerotic plaque. Using a range of techniques including T1-weighted, proton density—weighted, T2-weighted, and diffusion-weighted MR imaging, several groups describe the accuracy of MR imaging to reveal calcification, fibrocellular tissue, lipid, and thrombus both ex vivo and in vivo [53,54,55,56] (Fig. 9A,9B). Although requiring more invasive measures, intravascular MR imaging techniques with MR catheter coils are also under investigation for the high-resolution imaging of the aorta [57]. For example, Zimmermann-Paul et al. [58] developed intravascular MR coils that allow monitoring of plaque formation in rabbit models with hyperlipidemia. These coils allow high-resolution imaging during intervention under MR guidance.



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Fig. 9A. —31-year-old woman with history of peripheral embolic disease and severe atherosclerosis of descending thoracic aorta. Representative plaques are different in appearance and can be characterized on the basis of T1-, proton density—, and T2-weighted MR images. Inserts represent magnified views of descending thoracic aorta. (Courtesy of Fayad ZA, New York, NY) Axial T2-weighted MR image shows 7-mm fibrocellular stable plaque (arrows). Note origin of right coronary artery (RCA) from aortic root (Ao).

 


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Fig. 9B. —31-year-old woman with history of peripheral embolic disease and severe atherosclerosis of descending thoracic aorta. Representative plaques are different in appearance and can be characterized on the basis of T1-, proton density—, and T2-weighted MR images. Inserts represent magnified views of descending thoracic aorta. (Courtesy of Fayad ZA, New York, NY) Axial T2-weighted MR image at different level than A shows 7-mm fibrocellular unstable lipid-rich plaque. Hypointense area in plaque (arrow) corresponds to lipid-rich core.

 

By characterizing the components of atheromatous plaque, MR imaging can potentially make significant distinctions between stable plaques and unstable plaques that may be vulnerable to thrombosis or embolization, thereby warranting intervention. As a noninvasive tool for assessing the progression and regression of plaque components, such as the fatty core, MR imaging is promising for the examination of antiatherosclerotic therapeutic regimens. When combined with other MR imaging techniques to examine the cardiac chambers, valves, morphology, and functions, and the entire thoracic aorta and its branch vessels, MR imaging has the potential to provide a comprehensive study of cerebrovascular atheroembolic disease. Currently, MR imaging is useful to view atheromas in the innominate artery (Fig. 10) and contiguous ascending aorta (Fig. 11).



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Fig. 10. —56-year-old man with right brain transient ischemic attacks. Coronal reformatted image from breath-hold gadolinium-enhanced three-dimensional MR angiogram shows complex protruding atheroma originating from innominate artery (arrow). Plaque was overlooked on transesophageal echocardiogram because of tracheal interposition between esophagus and innominate artery.

 


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Fig. 11. —62-year-old man with history of stroke. Coronal reformatted image from breath-hold gadolinium-enhanced three-dimensional MR angiogram shows protruding atheroma of ascending aorta (solid arrow) with filiform morphology suggesting mobility. Note innominate artery (open arrow).

 


Therapy
Top
Introduction
Transesophageal Echocardiography
The Importance of a...
CT
MR Imaging
Therapy
Conclusion
References
 
Researchers have not determined the correct therapeutic approach to patients with aortic atheromas. However, anticoagulation with warfarin may be a reasonable treatment [21] because thrombi have been documented on aortic plaques and represent mobile components seen on transesophageal echocardiography. Another therapeutic approach may be the use of drugs known as statins. These cholesterol-lowering drugs were recently found to reduce the stroke rate of patients observed in the Cholesterol And Recurrent Events (CARE) study [59]. By reducing plaque lipid in patients with aortic atheromas, statins could theoretically make aortic plaques stable or nonthrombogenic. However, this result remains to be proven. Clearly, a large prospective study is required to determine the efficacy and risks of various anticoagulant, antithrombotic, and lipid-lowering strategies.


Conclusion
Top
Introduction
Transesophageal Echocardiography
The Importance of a...
CT
MR Imaging
Therapy
Conclusion
References
 
Thoracic aortic atherosclerosis is an important cause of severe morbidity and mortality. Its presence in patients undergoing surgery requiring cardiopulmonary bypass dramatically increases the risk of complications such as stroke. Currently, the ease of performance, the detailed information obtainable, and the cost and availability of the equipment for transesophageal echocardiography make it the procedure of choice for examining thoracic aortic atherosclerosis. However, technical advances in MR imaging and CT, particularly in the characterization of plaque on MR imaging, may allow a less invasive and more complete examination of thoracic aortic atherosclerosis in the near future.


References
Top
Introduction
Transesophageal Echocardiography
The Importance of a...
CT
MR Imaging
Therapy
Conclusion
References
 

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