CLINICAL STUDY: ATHEROSCLEROSIS
Transcutaneous detection of aortic arch atheromas by suprasternal harmonic imaging
Ehud Schwammenthal, MD*,
,
Yvonne Schwammenthal, MD
,*,
,
David Tanne, MD
,
,
Alexander Tenenbaum, MD*,
,
Alex Garniek, MD
,
,
Michael Motro, MD, FACC*,
,
Babeth Rabinowitz, MD, FACC*,
,
Michael Eldar, MD, FACC*,
and
Micha S. Feinberg, MD*,
* Heart Institute and Cardiac Rehabilitation Institute, Tel Hashomer, Israel
Department of Neurology, Chaim Sheba Medical Center, Tel Hashomer, Israel
Department of Radiology, Chaim Sheba Medical Center, Tel Hashomer, Israel
Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel
Manuscript received September 10, 2001;
revised manuscript received December 26, 2001,
accepted January 10, 2002.
* Reprint requests and correspondence: Dr. Ehud Schwammenthal, Heart Institute, Sheba Medical Center, Tel Hashomer, Israel
sehud{at}post.tau.ac.il
 |
Abstract
|
|---|
OBJECTIVES: The goal of the present study was to examine whether suprasternal harmonic imaging (SHI) (i.e., harmonic imaging from the suprasternal windows) can visualize protruding arch atheromas (PAAs) and reliably predict the presence or absence of significant lesions.
BACKGROUND: Protruding arch atheromas are a major source of cerebral and peripheral embolism and probably the most frequent cause of stroke during cardiac catheterization and open-heart surgery. Preprocedural screening by transesophageal echocardiography (TEE) would be desirable but is limited by the nature of the examination.
METHODS: Of 354 patients who underwent a TEE study in our laboratory during the study period, 106 were referred for detection of a source of embolism. Findings were classified based on the French Aortic Plaque study criteria as: 1) no or minimal atherosclerotic changes; 2) PAAs <4 mm; 3) PAAs
4 mm or presence of a mobile component.
RESULTS: Adequate transcutaneous image quality could be achieved in 89 patients (84%). Protruding arch atheromas were present in 42 patients (47%) and absent in 47 (53%). Positive and negative predictive values for large PAAs on TEE were 91% and 98%, respectively. In one case, SHI detected a complex PAA inaccessible for TEE due to interposition of the left bronchus as demonstrated by dual helical computed tomography. Inter-observer agreement for SHI was 91%.
CONCLUSIONS: Suprasternal harmonic imaging reliably predicted or excluded the presence of PAAs in a sizable, consecutive group of patients referred to TEE for detection of a source of embolism. It represents an excellent screening test and provides complimentary views of regions, which may be blind spots for TEE.
|
Abbreviations and Acronyms
| | DHCT | | dual helical computed tomography | | PAA | | protruding aortic arch atheroma | | SHI | | suprasternal harmonic imaging | | TEE | | transesophageal echocardiography |
|
Aortic arch atheromas are a major source of cerebral and peripheral embolism (16) and probably the most frequent cause of stroke during cardiac catheterization and open-heart surgery (715). Stroke that complicates surgery involving cardiopulmonary bypass occurs at least six times more frequently in patients with protruding arch atheromas (PAAs) (11,15), has an in-hospital mortality rate of almost 40%, and leaves many survivors severely disabled (15). Preprocedural screening by transesophageal echocardiography (TEE) would be desirable (1623) but is limited by the nature of the examination, involving the need to place an endoscopic device in the esophagus. The recently introduced technique of harmonic imaging combines good penetration with preserved resolution and an excellent signal-to-noise ratio (24). We therefore hypothesized that harmonic imaging can be used to directly visualize aortic arch atheromas from the jugulum or the supraclavicular fossae and reliably predict the presence or absence of significant lesions.
 |
Methods
|
|---|
Patients.
During the study period, 354 patients underwent a TEE in our laboratory; 106 of these patients were referred for detection of a source of embolism. Seventeen patients (16%) were excluded because of insufficient transthoracic image quality. The remaining 89 patients (84%) represent the study group. There were 29 women and 60 men ranging in age from 19 years to 84 years (61 ± 16 years). Sixty-three patients (71%) were referred after a transitory ischemic attack, and 15 (17%) after a cerebrovascular accident. Two patients (3%) were referred after peripheral embolization, and nine (10%) before planned cardiac surgery.
Suprasternal harmonic imaging (SHI).
Examinations were performed with a System Five ultrasound system (GE Vingmed, Horten, Norway) (1.6 to 1.7 MHz probe), a Sequoia C 256 Acuson (Mountain View, California) (1.75 MHz) or a Hewlett Packard Sonos 5500 (Andover, Massachusetts) (1.8 MHz). Individual patients, in whom a fundamental frequency of 1.8 MHz did not allow sufficient penetration, were restudied with a system that provided lower frequency transmission. The transducer was placed at the jugulum or the supraclavicular fossae and angulated to obtain a long-axis view of the complete aortic arch (Fig. 1). Views of the ascending aorta and proximal arch were obtained by anterior tilting of the transducer; views of the distal arch and descending thoracic aorta were obtained by posterior tilting of the transducer. Special care was taken to identify the origin of the three major branches of the aorta. The aortic arch was systematically scanned using acoustic zoom intermittently to facilitate detail recognition and adjusting gain to optimize signal-to-noise ratio (Fig. 2 to 5). Based on the classification of the French Study of Aortic Plaques in Stroke group (4,5), findings of the examination were classified as follows: 1) absence of significant atherosclerotic lesions (normal arch or only intimal thickening); 2) presence of aortic arch atheromas protruding not more than 3.9 mm into the lumen; 3) presence of aortic arch atheromas protruding 4 mm or more into the lumen or presence of a mobile component regardless of atheroma size.

View larger version (119K):
[in this window]
[in a new window]
|
Figure 1 Long-axis view of the proximal thoracic aorta. (Left) Views of the ascending aorta with origin of the inominate artery (IA) obtained by anterior tilting of the transducer. (Right) Views of the distal arch and descending thoracic aorta (dAo) obtained by posterior tilting of the transducer. The origin of the left common carotid artery and the left subclavian artery are visualized in the same plane; the IA can be recognized, but its origin cannot be appropriately delineated in this plane.
|
|

View larger version (70K):
[in this window]
[in a new window]
|
Figure 2 (Left) Large protruding aortic atheroma (arrows) vis-à-vis the origin of the left common carotid and subclavian artery detected by suprasternal harmonic imaging (HI) (zoomed frame, the overview image is shown as an inlay picture in the right upper corner). (Right) Same atheroma visualized by transesophageal echocardiography (TEE).
|
|

View larger version (77K):
[in this window]
[in a new window]
|
Figure 3 (Left) Large protruding aortic atheroma at the minor curvature of the aortic arch (zoomed frame), with features compatible with ulceration (arrows). Long and continuous segments of the aortic wall appear as thick hypoechoic plaques (arrowheads). (Right) The same features can be identified by transesophageal echocardiography.
|
|

View larger version (175K):
[in this window]
[in a new window]
|
Figure 4 Examination of the aortic arch by suprasternal harmonic imaging. (Top) Overview images of the proximal thoracic aorta (long axis). (Bottom) Zoomed image sections after adjusting gain facilitate detail recognition. (Left) Calcifications without protruding atheromas at the minor curvature of the aorta (three arrowheads pointing down) and at the origin of the inominate artery (two arrowheads pointing up). (Right) Large noncalcified atheroma (arrowheads) protruding into the proximal descending thoracic aorta vis-à-vis the origin of the left subclavian artery. Note that the hypoechoic ("soft") atheroma is clearly delineated only after zoom and gain adjustments.
|
|

View larger version (147K):
[in this window]
[in a new window]
|
Figure 5 (Left) Visualization of the complete descending thoracic aorta in a long-axis view by suprasternal harmonic imaging (SHI). The posterior aortic wall is covered by aortic plaques over a segment of several centimeters. (Right) Transesophageal echocardiography (TEE) confirms the findings. Appropriate visualization of the latter half of the descending thoracic aorta was possible only in the minority of cases.
|
|
TEE.
All TEE examinations were performed using a multiplane probe (5 to 7 MHz). The ascending aorta was visualized in a long-axis view and also in a short-axis view above the coronary sinuses. After imaging the descending aorta, the probe was gradually pulled back until the curve of the distal arch was visible. The probe was then rotated clockwise to study the proximal arch, and if possible, the distal portion of the ascending aorta using multiple imaging planes.
Data analysis.
Classification of aortic arch findings by SHI and TEE were compared using contingency tables (chi-square test). If the studies were grossly discrepant (more than one grade), dual helical computed tomography (DHCT) was performed in an attempt to clarify the cause of the discrepancy (25). Positive and negative predictive values of SHI were calculated for the diagnosis of atheromas of any size as well as only large (
4 mm) or mobile ones. The SHI studies were read blinded to the findings on TEE. Inter-observer agreement was determined as the ratio of concordant classifications to all comparisons performed. A p value of <0.05 was considered significant.
 |
Results
|
|---|
Forty-seven patients (53%) had a normal aortic arch or only intimal thickening by TEE; 42 patients (47%) had PAAs. In 21 patients (24%), PAAs protruded <4 mm into the lumen, in 21 patients (24%), 4 mm or more. Classification of the aortic arch findings by SHI and TEE/DHCT agreed well (p < 0.0001, chi-square = 122) (Fig. 6). In four of 45 patients classified as having no PAA by SHI, an atheroma of 1 to 2 mm was detected by TEE. In two patients classified as having PAAs of <4 mm by SHI, only intimal thickening (at the most) was found on TEE. In one case, a PAA
4 mm was underestimated by SHI. A major discrepancy was present in two cases, and consequently, these patients underwent DHCT. In the first patient, a moderately sized plaque was found by both ultrasound techniques, but SHI suggested the presence of an additional large PAA (in retrospect a misinterpreted artifact) not seen on TEE and DHCT. In the second patient, a freely mobile component compatible with a thrombus superimposed on a plaque was detected by SHI (Fig. 7) but could not be visualized by TEE. Dual helical computed tomography demonstrated that the protruding component of the complex atheroma was obscured by interposition of the left bronchus between aortic arch and esophagus (Fig. 8). In one of four cases, a mobile component on a correctly identified large PAA was missed by SHI. All 12 cases of hypoechoic components and three of four cases of ulcerative components were correctly appreciated by SHI.

View larger version (23K):
[in this window]
[in a new window]
|
Figure 6 (Left) Agreement between harmonic imaging (SHI) and transesophageal echocardiography (TEE) or dual helical computed tomography (DHCT) in the classification of aortic arch findings. (Right) Agreement between two observers in the classification of aortic arch findings using harmonic imaging. PAA = protruding atheroma of the aortic arch.
|
|

View larger version (159K):
[in this window]
[in a new window]
|
Figure 7 Mobile thrombus superimposed on an atherosclerotic plaque of the aortic arch; the curved arrow indicates systolic motion of the thrombus). LCA = left common carotid artery; LSA = left subclavian artery.
|
|

View larger version (95K):
[in this window]
[in a new window]
|
Figure 8 Dual helical computed tomography in a patients with a protruding atheroma of the aortic arch with a mobile thrombus, visualized by suprasternal harmonic imaging (Fig. 4), but not by transesophageal echocardiography. (Left) The dashed line demonstrates that the posterior view of the complex plaque from the esophagus (E) (arrow) is obstructed by the origin of the left bronchus (LB) from the trachea (T). The solid line depicts the view from the esophagus after maximum anterior rotation of the transducer before interference with the left bronchus. The angle of freedom limited by the left bronchus does not allow visualization of the aorta at all at the level of the complex plaque. (Right) The sagittal view shows that the complex plaque is readily accessible anteriorly from the suprasternal window.
|
|
Positive and negative predictive values of SHI for the diagnosis of PAA were 95% and 92%, respectively, and for diagnosis of only large or mobile PAAs, 91% and 98%, respectively. Sensitivity and specificity for diagnosing large PAAs were 95% and 97%, respectively. When inadequate studies were counted as transthoracic misses of the TEE findings, sensitivity and specificity were 77% and 83%, respectively (negative predictive value was still 85%). The two independent observers agreed in 81 of the 89 cases (91%, p < 0.0001, chi-square = 123); there were no major discrepancies (Fig. 6).
 |
Discussion
|
|---|
The present study demonstrates that PAAs can be well visualized transcutaneously using SHI (i.e., harmonic imaging from suprasternal windows). This technique reliably predicted the presence or absence of PAAs in a sizable, consecutive group of patients referred to TEE for detection of a source of embolism. It represents not only an excellent screening test but provides complementary views of regions, which may be blind spots for TEE (Fig. 7). Both the anatomical orientation and the localization of detected atheromas with respect to the origin of the major aortic branches are more readily achieved with SHI than TEE, because SHI is facilitated by the long-axis view of the complete aortic arch (Fig. 1).
Weinberger et al. (26) first demonstrated the feasibility of the transcutaneous approach for imaging atherosclerotic plaques in the aortic arch of stroke patients compared with TEE, as well as for correlating plaque morphology to cerebrovascular symptoms (27). However, because of the small sample size, no attempts were made to assess the diagnostic accuracy of the method (26). Although the high-frequency probe the authors used may provide excellent resolution, it does so at the expense of ultrasound penetration. It may therefore be difficult to obtain a complete study of the proximal thoracic aorta in adult patients, especially in the elderly. In contrast, harmonic imaging provides good penetration, preserved resolution, and reduced signal-to-noise ratio, particularly in the near field (24), which is important given the relatively small distance between jugulum and aortic arch.
Clinical implications.
Screening noninvasively
Stroke prevention is of paramount importance in an era characterized by an increasing number of cardiovascular procedures performed in an aging population. Suprasternal harmonic imaging may facilitate preprocedural screening of patients at risk for stroke during cardiac interventions, particularly cardiac surgery involving cardiopulmonary bypass or port-access using an intra-aortic endoclamp. In patients in whom a significant PAA can be clearly demonstrated by SHI, or no evidence of atheroma can be detected despite good imaging quality, TEE would probably not alter the management strategy. In cases in which image quality is inadequate to reliably rule out atheromas, or in which there are inconclusive findings or evidence of plaque with insufficient image quality to evaluate plaque characteristics, TEE should be performed. In addition, transcutaneous screening of unselected asymptomatic patients within a primary prevention program could provide data about the natural risk of asymptomatic patients with PAAs unrelated to cardiac interventions.
Complementing TEE
When imaging is performed from the posteriorly located esophagus, the left bronchus (at its origin from the trachea) may obscure a portion of varying size of the aortic arch. The size of this blind segment depends on the diameter of the bronchus, its take-off angle and the curvature of the aortic arch. The segment is readily accessible from the anteriorly positioned suprasternal window (Fig. 8). In the present study a mobile thrombus superimposed on an aortic arch atheroma was clearly demonstrated by SHI (Fig. 7), but missed by TEE, in a patient without prior embolic event who was scheduled for cardiac catheterization and open-heart surgery. Intervention was deferred, coumadine therapy was instituted, and the thrombus gradually and uneventfully dissolved. Every TEE examination should be complemented by careful imaging from the suprasternal window to close the blind gap and perform a truly comprehensive ultrasound examination of the proximal thoracic aorta.
Learning curve.
Achieving a high degree of versatility and accuracy in SHI requires a learning process. Comparison of the ultrasound studies with findings on DHCT in the sagittal plane in patients with known PAAs (not included in the study) was extremely useful (25). Adjustment of gain and contrast settings is mandatory in order to avoid missing "soft," hypoechoic, noncalcified plaques (Figs. 3 and 4), morphologic features, which are associated with high embolic risk and may represent lipid-rich atheromas with or without thrombus formation (19,20).
Study limitations.
Adequate image quality for evaluating the aortic arch transcutaneously cannot be obtained in 16% of the patients using current state-of-the-art equipment, which seems acceptable for screening purposes. Frequently, a positive diagnosis can be made even when imaging quality is less than perfect, because in patients who are difficult to scan, image quality is usually at its worst in areas proximal to the inominate artery (where significant plaques are rare) (28) and distal to the left subclavian artery (irrelevant for stroke) but is relatively preserved in the arch. Because the descending thoracic aorta cannot usually be visualized completely, TEE is recommended in patients referred for detection of a source of peripheral (and not cerebral) embolism, if suprasternal imaging does not detect significant findings.
 |
Acknowledgments
|
|---|
The authors thank Lili Ezer, RCDS, and Ziva Dror, RCDS, for their dedication to this project, and Meirav Moreno for her expert secretarial assistance.
 |
Footnotes
|
|---|
Supported by a grant from the Israel Science Foundation.
 |
References
|
|---|
- Tunick PA, Kronzon I. Protruding atherosclerotic plaque in the aortic arch of patients with systemic embolization: a new finding seen by transesophageal echocardiography. Am Heart J. 1990;25:382390
- Dávila-Román VG, Barzilai B, Wareing TH, Murphy SF, Schechtman KB, Kouchoukos NT. Atherosclerosis of the ascending aorta: prevalence and role as an independent predictor of cerebrovascular events in cardiac patients. Stroke. 1994;25:20102016[Abstract]
- Amarenco P, Cohen A, Tzourio C, et al. Atherosclerotic disease of the aortic arch and the risk of ischemic stroke. N Engl Med. 1994;331:14741479[Abstract/Free Full Text]
- The French Study of Aortic Plaques in Stroke Group. Aortic disease of the aortic arch as a risk factor for recurrent ischemic stroke. N Engl J Med. 1996;334:12161221[Abstract/Free Full Text]
- Tunick PA, Perez JL, Kromzon I. Protruding atheromas in the thoracic aorta and systemic embolization. Ann Intern Med. 1991;115:423427[Medline]
- Tunick PA, Rosenzweig BP, Katz ES, Freedberg RS, Perez JL, Kronzon I. High risk for vascular events in patients with protruding aortic atheromas. J Am Coll Cardiol. 1994;23:10851090[Abstract]
- Keeley EC, Grines CL. Scraping of aortic debris by coronary guiding catheters: a prospective evaluation of 1,000 cases. J Am Coll Cardiol. 1998;32:18611865[Abstract/Free Full Text]
- Karalis DG, Quinn V, Victor MF, et al. Risk of catheter-related emboli in patients with atherosclerotic debris in the thoracic aorta. Am Heart J. 1996;131:11491155[CrossRef][Medline]
- Katz ES, Tunick PA, Kronzon I. Observations of coronary flow augmentation and balloon function during intraaortic balloon counterpulsation using transesophageal echocardiography. Am J Cardiol. 1992;69:16351639[CrossRef][Medline]
- Multicenter Study of Perioperative Ischemia Research Group and the Ischemia Research and Education Foundation Investigators. Adverse cerebral outcomes after coronary bypass surgery. N Engl J Med. 1996;335:18571863[Abstract/Free Full Text]
- Katz ES, Tunick PA, Rusinek H, et al. Protruding aortic atheromas predict stroke in elderly patients undergoing cardiopulmonary bypass: a review of our experience with transesophageal echocardiography. J Am Coll Cardiol. 1992;20:7077[Abstract]
- Barzilai B, Marshall WG Jr., Saffitz JE, Kouchoukos N. Avoidance of embolic complications by ultrasonic characterization of the ascending aorta. Circulation. 1989;80(Suppl I):I275279
- Marshall WG, Barzilai B, Kouchoukos NT, Saffitz J. Intraoperative ultrasound imaging of the ascending aorta. Ann Thorac Surg. 1989;48:339344[Abstract]
- Wareing TH, Dávila-Román BG, Barzilai B, et al. Management of the severely atherosclerotic ascending aorta during cardiac operations: a strategy for detection and treatment. J Thorac Cardiovasc Surg. 1992;103:40534062
- Stern A, Tunick PA, Culliford AT. Protruding aortic arch atheromas. Risk of stroke during heart surgery with and without aortic arch endarterectomyAm Heart J. 1990;138:746752[CrossRef]
- Pop G, Sutherland GR, Koudstaal PJ, Sit TW, de Jong G, Roelandt JRTC. Transesophageal echocardiography in the detection of intracardiac embolic sources in patients with transient ischemic attacks. Stroke. 1990;21:560565[Abstract/Free Full Text]
- Horowitz DR, Tuhrim S, Budd J, Goldman ME. Aortic plaque in patients with brain ischemia: diagnosis by transesophageal echocardiography. Neurology. 1992;42:16021604[Abstract/Free Full Text]
- Montgomery DH, Ververis JJ, McGorisk G, Frohwein S, Martin RP. Natural history of severe atheromatous disease of the thoracic aorta: a transesophageal echocardiographic study. J Am Coll Cardiol. 1996;27:95101[Abstract]
- Tunick PA, Kronzon I. Atheromas of the thoracic aorta: clinical and therapeutic update. J Am Coll Cardiol. 2000;35:545554[Abstract/Free Full Text]
- the FAPS InvestigatorsCohen A, Tzourio C, Bertrand B, et al. Aortic plaque morphology and vascular events: a follow-up study in patients with ischemic stroke. Circulation. 1997;96:38373841
- Vaduganathan P, Newton A, Nagueh SF, et al. Pathologic correlates of aortic plaques, thrombi and mobile "aortic debris" imaged in vivo with transesophageal echocardiography. J Am Coll Cardiol. 1997;30:357363[Abstract]
- Stone DA, Hawke MW, LaMonte M, et al. Ulcerated atherosclerotic plaques in the thoracic aorta are associated with cryptogenic stroke: a multiplane transesophageal study. Am Heart J. 1995;130:105108[CrossRef][Medline]
- Tenenbaum A, Fisman EZ, Schneiderman J, et al. Disrupted mobile aortic plaques are a major risk factor for systemic embolism in the elderly. Cardiology. 1998;89:246251[CrossRef][Medline]
- Thomas JD, Rubin DN. Tissue harmonic imaging: why does it work? J Am Soc Echocardiogr. 1998;11:803808[CrossRef][Medline]
- Tenenbaum A, Garniek A, Shemesh J, et al. Dual-helical CT for detecting aortic atheromas as a source of stroke: comparison with transesophageal echocardiography. Radiology. 1998;208:153157[Abstract/Free Full Text]
- Weinberger J, Azhar S, Danisi F, et al. A new noninvasive technique for imaging atherosclerotic plaque in the aortic arch of stroke patients by real-time-B-mode ultrasonography: an initial report. Stroke. 1998;29:673676[Abstract/Free Full Text]
- Weinberger J, Papamitsakis N, Newfield A, Godbold J, Goldman M. Plaque morphology correlates with cerebrovascular symptoms in patients with complex aortic arch plaque. Arch Neurol. 2000;57:8184[Abstract/Free Full Text]
- Katibzadeh M, Mitusch R, Stierle U, Gromoll B, Sheikhzade A. Aortic atherosclerotic plaques as a source of systemic embolism. J Am Coll Cardiol. 1996;27:664669[Abstract]
This article has been cited by other articles:

|
 |

|
 |
 
K. Nasir, A. Roguin, A. Sarwar, J. A. Rumberger, and R. S. Blumenthal
Letter to the Editor: Gender Differences in Coronary Arteries and Thoracic Aorta Calcification
Arterioscler. Thromb. Vasc. Biol.,
May 1, 2007;
27(5):
1220 - 1222.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y.-L. Li, D. T. Wong, W. Wei, and J. Liu
A novel acoustic window for trans-oesophageal echocardiography by using a saline-filled endotracheal balloon
Br. J. Anaesth.,
November 1, 2006;
97(5):
624 - 629.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Kronzon and P. A. Tunick
Aortic Atherosclerotic Disease and Stroke
Circulation,
July 4, 2006;
114(1):
63 - 75.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F Chirillo, A Pedrocco, A De Leo, A Bruni, O Totis, P Meneghetti, and P Stritoni
Impact of harmonic imaging on transthoracic echocardiographic identification of infective endocarditis and its complications
Heart,
March 1, 2005;
91(3):
329 - 333.
[Abstract]
[Full Text]
[PDF]
|
 |
|