Original Article
The Prevalence of Ulcerated Plaques in the Aortic Arch in Patients with Stroke
N Engl J Med 1992; 326:221-225January 23, 1992
- Abstract
- Abstract
Background and Methods.
The cause of cerebral infarction is obscure in up to 40 percent of patients with this disorder who are studied prospectively. In this investigation, we determined the frequency of ulcerated plaques in the aortic arch and explored the part they may play in the formation of cerebral emboli. Using an autopsy data bank, we studied the prevalence of ulcerated plaques in the aortic arch in 500 consecutive patients with cerebrovascular and other neurologic diseases who were studied at autopsy.
Results.
Ulcerated plaques were present in 26 percent of the 239 patients with cerebrovascular disease but in only 5 percent of the 261 patients with other neurologic diseases (P<0.001 ). After we controlled for age and heart weight, the adjusted rates were 16.9 percent and 5.1 percent, respectively (adjusted odds ratio, 4.0; 95 percent confidence interval, 2.1 to 7.8; P<0.001). Among the patients with cerebrovascular disease, the prevalence of ulcerated plaques in the aortic arch was 28 percent in the 183 patients with cerebral infarcts and 20 percent in the 56 patients with brain hemorrhage. The prevalence of ulcerated plaques was 61 percent among the 28 patients with no known cause of cerebral infarction, as compared with 22 percent among the 155 patients with a known cause of cerebral infarction (P<0.001). After adjustment for covariates, the prevalence was 57.8 percent among patients with no known cause of cerebral infarction and 20.2 percent among those with a known cause (adjusted odds ratio, 5.7; 95 percent confidence interval, 2.4 to 13.6; P<0.001). The presence of ulcerated plaques in the aortic arch was not correlated with the presence of extracranial internal-carotid-artery stenosis, suggesting that these were two independent risk factors for stroke.
Conclusions.
Ulcerated plaques in the aortic arch may play a part in causing cerebral infarction, especially in patients in whom cerebral infarction has no known cause. (N Engl J Med 1992;326:221–5.)
Media in This Article
Figure 1
Appearance of the Opened Aortic Arch.Figure 2
Appearance of the Opened Aortic Arch.Article Activity
- Article
IN as many as 40 percent of the cases of cerebral infarction reported in the stroke data bank of the National Institute of Neurological Disorders and Stroke,1 the cause is undetermined. Recent studies with transesophageal echocardiography have found atherosclerotic plaques protruding into the lumen of the aortic arch in patients with transient ischemic attacks2 or unexplained embolic strokes.3 Although the presence of ulcerated plaques in the aortic arch is acknowledged as a causal factor in strokes,4 5 6 7 8 9 10 11 12 13 cerebral emboli arising from such plaques are considered to be rare.4 , 8 , 13 Most reported cases are isolated and occur as complications of cardiac surgery,14 15 16 aortography,17 18 19 or anticoagulant therapy.20 21 22 23 Our study was designed to determine the prevalence of ulcerated plaques in the aortic arch and their role in the formation of cerebral emboli.
Methods
Using an autopsy data bank, we reviewed the records of 500 consecutive complete autopsies of patients with neurologic diseases performed at the Hôpital de la Salpêtrière in Paris from December 19, 1983, to August 30, 1987; extensive macroscopical examination of the brain, aortic arch, and heart had been performed in all cases. The 500 patients examined at autopsy represented 73 percent of the patients with neurologic diseases who died during the period covered by the study. Ulcerated plaque in the aortic arch was defined as one or more ulcerations of a plaque located in the ascending aorta (i.e., proximal to the ostium of the innominate artery) or the horizontal aorta (i.e., proximal to the ostium of the left subclavian artery) between the leaflets of the aortic valve and the ostium of the left subclavian artery. Ulcerated plaques in the descending aorta were not included in our analysis. Ulceration was defined as a disruption of the intimal surface visible on macroscopical examination.
The patients were divided into two groups according to the presence or absence of cerebrovascular disease. Those with cerebrovascular disease (239 patients) had pathologically confirmed ischemic stroke (183 patients) or hemorrhagic stroke (56 patients). Six patients with other neurologic diseases who were found to have stroke at autopsy were included in the group with cerebrovascular disease. The patients with other neurologic disorders and no cerebrovascular disease (261 patients), who had no history or pathological evidence of stroke, had a variety of neurologic conditions: degenerative and demyelinating disease, such as Alzheimer's disease, Parkinson's disease, progressive supranuclear palsy, amyotrophic lateral sclerosis, other degenerative diseases, and multiple sclerosis (n = 80), brain tumors (n = 101), infections (n = 30), trauma (n = 8), toxic reactions (n = 2), and myelopathy, polyneuropathy, and other neurologic disorders with normal brain function (n = 40).
In the group with cerebrovascular disease, extracranial and intracranial arteries were examined in all patients. With use of a technique described elsewhere,24 , 25 the aorta and its cervical branches were dissected and the cervical spine and base of the skull excised and decalcified. In each case, the arterial pattern and the site and nature of the arterial lesions were noted, as previously described.26 The degree of stenosis was recorded. The clinical and pathological evidence of the cause of cerebral infarction was assessed in each case. Causes were classified as atherosclerotic (as evidenced by ipsilateral atheroma with either ulcerated plaque, whatever the degree of stenosis, or a thrombotic occlusion superimposed on stenosis, or by ipsilateral arterial stenosis of more than 40 percent), cardioembolic (as defined by the presence of a cardiac source of emboli and no atherosclerosis of extracranial and intracranial arteries, with or without visible occlusive thrombus), mixed (that is, both atherosclerotic and cardioembolic), other (such as cancer-related disseminated intravascular coagulation, systemic vascular collapse, aspergillosis, inflammatory arteritis, or dissecting aneurysm), or undetermined (no identifiable cause, in the absence of any of the conditions mentioned above).
Statistical Analysis
We used two-tailed t-tests for comparisons of means and the chi-square test for proportions. Multiple logistic-regression analysis was performed to compare the prevalence of ulcerated plaques in patients with cerebrovascular disease with that in patients without cerebrovascular disease and to compare the prevalence in patients whose cerebral infarction had a known cause with that in patients whose cerebral infarction had no known cause; we controlled for covariates related to atherosclerosis (age, sex, and heart weight, which reflects the presence of hypertension). Data were analyzed with use of SAS statistical software.27
Results
The size of the ulcers in the plaques in the aortic arch varied from 3 by 2 mm to 35 by 50 mm. The mean (±SD) area of ulceration was 214±449 mm2 per patient (median, 50 mm2). Figures 1Figure 1
Appearance of the Opened Aortic Arch. and 2Figure 2Appearance of the Opened Aortic Arch. show the smallest and the largest ulcerations we saw. Ulcerations more frequently involved the horizontal aorta (81 percent) than the ascending aorta (44 percent), and the superior wall (94 percent) more frequently than the caudal wall (38 percent). All ulcerations were found to lie around the origin of the cerebral arteries. The degree of agreement between the two independent observers who identified ulcerations was 94.7 percent, with a kappa value of 0.94 (indicating a high degree of agreement).The group with cerebrovascular disease was older than the group with other neurologic diseases (mean age, 73±12 vs. 62±16 years; P<0.001) and had a higher heart weight (415±108 vs. 343±76 g, P<0.001). The sex ratio was similar in both groups (134 men and 105 women vs. 150 men and 111 women, P = 0.75). We found ulcerated plaques in the aortic arch in 26 percent of the patients with cerebrovascular disease and in 5 percent of the patients with other neurologic diseases and no pathological evidence of cerebrovascular disease (P<0.001) (Table 1Table 1
Prevalence of Ulcerated Plaques in the Aortic Arch in 500 Patients Examined at Autopsy.). After we controlled for confounding factors related to atherosclerosis (age and heart weight), the adjusted rates were 16.9 percent and 5.1 percent, respectively (adjusted odds ratio, 4.0; 95 percent confidence interval, 2.1 to 7.8; P<0.001).Among the 183 patients with cerebral infarcts, no definite cause was found in 28; the prevalence of ulcerated plaques in the aortic arch in this group was 61 percent. Among the 155 patients in whom a cause of cerebral infarction could be identified, the prevalence of ulcerated plaques was 22 percent (P<0.001) (Table 1). These two groups were not significantly different in terms of age, sex, and heart weight (Table 2Table 2
Clinical and Pathological Characteristics of 183 Patients with Cerebral Infarction.). After adjustment, the prevalence of ulcerated plaques was 57.8 percent among the patients with no known cause of cerebral infarction and 20.2 percent among those with a known cause; the difference between the groups remained significant after adjustment (adjusted odds ratio, 5.7; 95 percent confidence interval, 2.4 to 13.6; P<0.001). The frequency of ulcerated plaques in the aortic arch did not differ according to the presence or absence of extracranial internal-carotid-artery stenosis or according to the degree of stenosis (≥75 percent or <75 percent). In patients with ulcerated plaques in the aortic arch, the frequency of internal-carotid-artery stenosis of ≥75 percent was not significantly different from that in patients without ulcerated plaques in the aortic arch (7 of 51 [14 percent] vs. 14 of 132 [11 percent], P not significant), and internal-carotid-artery stenosis was absent as frequently in patients with ulcerated plaques in the aortic arch as in those without ulcerated plaques (26 of 51 [51 percent] vs. 86 of 132 [65 percent], P not significant). The frequency of ulcerated plaques in the aortic arch in various age groups is shown in Table 3Table 3
Prevalence of Ulcerated Plaques in the Aortic Arch According to Age Group and Diagnosis..Pathological study of the brains of the 17 patients who had ulcerated plaques in the aortic arch and cerebral infarction of unknown cause showed that there was more than one infarct in 14 patients. The infarcts were small (13 patients), large (2 patients), or both (2 patients). Small infarcts were cortical (two patients), deep (six patients), or both (seven patients). Three patients had border-zone infarcts, nine had lacunas, état criblé, or both, and two had Binswanger's disease.28 In five instances, the infarcts were hemorrhagic (and therefore likely to be embolic).
Discussion
In this autopsy study of 500 patients with neurologic disease, ulcerated plaques in the aortic arch were frequent (15 percent) and were linked to cerebrovascular disease. When they examined not only the arch but the entire aorta of 178 patients, Fisher et al. found only 37 aortas free of ulceration; they emphasized that the aorta was two to four times more likely to show evidence of severe atherosclerosis than the cervical arteries.29 In our study, we were unable to determine in each case whether there was a mural thrombus. Fisher et al. found 42 mural thrombi in their 178 patients; 21 thrombi were found on the aorta, but no details were given specifically about the arch.29 Despite the existence of several papers reporting atheromatous embolization from the aortic arch,4 5 6 7 8 9 10 11 12 13 we found no reports on large series dealing with this subject. We found strong correlations between the presence of ulcerated plaques in the aortic arch and increasing age and heart weight (the latter mainly reflects the presence of hypertension). Although autopsies were not performed blindly to identify stroke or other neurologic diseases, we believe the 5 percent prevalence of ulcerated plaques in the aortic arch in our control group (the patients without cerebrovascular disease) is not an underestimate, since the degree of agreement between the observers who studied the autopsy material for evidence of ulcerated plaques was good. In the present series, the multivariate analysis, in which we controlled for age and heart weight, showed that the prevalence of ulcerated plaques in the aortic arch was significantly higher among patients with cerebrovascular disease than among patients with other neurologic diseases. Only 2 patients under 60 years of age (1 percent) had ulcerated plaques in the aortic arch; among patients 60 or older who had ischemic stroke, 51 (31 percent) had such plaques. This figure is much higher than, for example, the 15 percent prevalence of lone atrial fibrillation reported by Wolf et al.30 in patients with cerebral infarction. The 36 percent prevalence of ulcerated plaques in the aortic arch in the oldest group of patients with cerebral infarction in our study (≥80 years of age) is equal to the prevalence of atrial fibrillation in the same group of patients in the study of Wolf et al.30
These results might indicate only that the presence of ulcerated plaques in the aortic arch is a marker of atherosclerotic disease. In an attempt to determine whether it is actually a risk factor for ischemic stroke, we further divided the 183 patients with ischemic strokes into two groups: 155 patients for whom a definite cause of stroke could be determined and 28 patients with no clinical or pathological evidence of a cause. These two groups were not significantly different in terms of age, sex, or heart weight. Interestingly, the prevalence of ulcerated plaques in the aortic arch in patients with a known cause of stroke was 22 percent, very close to the 20 percent prevalence in the 56 patients with brain hemorrhage; this similarity suggests that these two groups in fact make up one large group of patients with atherosclerotic disease. By contrast, among patients with no known cause of stroke, the prevalence of ulcerated plaques was 61 percent (P<0.001) (Table 1). This striking difference suggests that ulcerated plaques in the aortic arch should be considered and investigated as a risk factor for cerebral infarction, particularly in patients with no identifiable cause of stroke. Since only 15 percent of the patients with cerebral infarction in the present study had no identified cause of infarction, however, the 61 percent prevalence of ulcerated plaques in the aortic arch in this subgroup of our highly selected population cannot be generalized to the 40 percent of patients with ischemic stroke of unknown cause in prospective clinical series.1
Like atrial fibrillation31 and stenotic atheroma of the cerebral arteries, ulcerated plaques in the aortic arch may simply be a marker for the true cause of stroke. An important question is whether such plaques are risk factors for stroke that are independent of the presence of other atheromatous lesions, such as internal-carotid-artery stenosis. We found no correlation between the presence of ulcerated plaques in the aortic arch and extracranial internal-carotid-artery stenosis, whatever its degree, suggesting that these two risk factors may be independent.
Seventeen patients had no apparent cause of cerebral infarction other than ulcerated plaques in the aortic arch. Detailed study of these 17 patients showed that the cerebral infarcts were usually multiple, usually small, in various locations (deep, cortical, or both, or in a border-zone area), and sometimes hemorrhagic. Such lesions are suggestive of cerebral emboli. Lacunas and état criblé,28 also frequently noted in the present series, are lesions believed to be related to hypertension. The role of hypertension as a cause of lacunar stroke is still being debated,32 however, and cerebral emboli have been recognized as a possible cause of lacunar stroke.33 Thus, the cerebral ischemic lesions observed in these 17 patients are compatible with the existence of cerebral emboli and may have been caused by thrombotic or cholesterol emboli from ulcerated plaques in the aortic arch.
We conclude that ulcerated plaques in the aortic arch are common. Their frequency increases with age and heart weight, and they occur more frequently in patients with cerebrovascular disease, particularly those with cerebral infarction of no known cause. These findings suggest that ulcerated plaques in the aortic arch may be a source of cerebral emboli and could account for some cases of cerebral infarction of unknown cause. There is at present no satisfactory way to diagnose ulcerated plaques in the aortic arch in living patients. Transesophageal echocardiography may show atherosclerotic plaques protruding into the aortic arch or intraluminal thrombus,2 , 3 , 34 but this procedure is unable to identify ulcerations. Future technical refinements will undoubtedly improve our ability to detect such lesions.
We are indebted to Dr. Annick Alperovitch for her helpful criticism of this article.
Source Information
From the Laboratoire de Neuropathologie R. Escourolle, Hôpital de la Salpêtrière (P.A., CD., D.H., J.-J.H.), and the Service de Neurologie, Hôpital Saint-Antoine (P.A., M.-G.B.), Université Pierre et Marie Curie, Paris, and Institut National de la Santé et de la Recherche Médicale U169, Recherches en Epidémiologie, Villejuif, France (C.T.). Address reprint requests to Dr. Amarenco at the Service de Neurologie Hôpital Saint-Antoine, 184, rue du Faubourg Saint-Antoine, 75571 Paris, CEDEX 12, France.
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