doi: 10.1161/hs1201.099797
(Stroke. 2001;32:2782.)
© 2001 American Heart Association, Inc.
Original Contributions |
Carotid Stenosis
Factors Affecting Symptomatology
From the Second Department of Propedeutic Surgery, Athens University Medical School, Laiko Hospital, Athens, Greece.
Correspondence to Dr Christos Liapis, 131 Vas. Sofias Ave, 11521 Athens, Greece. E-mail liapis{at}hol.gr
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Abstract |
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Background and Purpose— The ability to predict future strokes in asymptomatic patients with carotid stenosis is currently limited. The management of symptomatic patients with <50% stenosis is also debatable. In this context, we performed the following open prospective study to identify factors affecting symptomatology in patients with carotid stenosis.
Methods— During 1988–1997, 442 arteries with various degrees of stenosis were followed with the use of color Duplex ultrasonography every 6 months. The main outcome measures were development of symptoms related to the carotid territory and progression in the degree of stenosis. Results of follow-up were analyzed in relation to the traditional risk factors for atherosclerosis as well as the ultrasonographic characteristics of the plaques. Statistical analysis was performed by multiple linear and Cox regression analysis.
Results— Mean duration of follow-up was 44 months (range, 12 to 120 months). Significant progression of stenosis occurred in 18.5% of the cases and was more frequent in younger patients (P=0.09), in patients with coronary artery disease (P=0.02), and in patients with echolucent plaques (P=0.02). In regard to clinical presentation, men (P=0.07), hypertensives (P=0.07), and patients with echolucent plaques (P=0.09) showed a trend toward higher frequency of stroke in their history. During the follow-up period, neurological events developed in 12.4% of the cases and were associated with the severity of carotid disease (P<0.001), history of neurological events (P=0.02), progression of stenosis (P=0.002), echolucent plaques (P=0.01), and hypertension (P=0.02).
Conclusions— Factors other than degree of stenosis and history of neurological events are also important in determining high-risk carotid plaque. In our study hypertension, echolucent plaques, and progressive lesions were associated with an increased risk of neurological events. These factors should be taken into consideration in determining treatment strategies for carotid stenosis.
Key Words: atherosclerosis • carotid stenosis • cerebrovascular disorders • risk factors • ultrasonography
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Introduction |
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Stroke is one of the most common causes of disability and the third leading cause of death in the developed world. The identification and treatment of factors associated with increased risk of stroke have therefore become of great interest over the past decade. The most well-known risk factor for the development of cerebrovascular events is high-degree internal carotid artery (ICA) stenosis. However, only a minority of patients with carotid stenosis will develop symptoms. It is obvious that factors other than the degree of stenosis are also important in determining high-risk carotid plaque.
To identify factors affecting symptomatology in patients with ICA stenosis, we conducted the following open prospective study. Special emphasis was placed on the ultrasonographic characteristics of the plaques, which were studied in relation to traditional risk factors for atherosclerosis, presenting symptoms, and the natural history of carotid stenosis.
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Subjects and Methods |
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Over a 10-year period during 1988–1997, 332 patients with ICA stenosis were followed with the use of color duplex ultrasonography every 6 months. Indications for the initial carotid duplex scan, by which the carotid stenosis was identified, included presence of a cervical bruit, focal neurological symptoms, coronary artery disease (CAD), or peripheral arterial occlusive disease. Eligibility for entering this study required asymptomatic carotid stenosis of any degree or symptomatic stenosis <50% at the time of entry. Cerebrovascular symptoms were attributed to a carotid stenosis of <50% when no other cause (cardiac valvular or rhythm disorder, recent myocardial infarction, intracerebral or subarachnoid hemorrhage, lacunar infarct) could be identified. Arteries without stenosis or with total occlusion as well as arteries that had been operated on were excluded, leading to a total of 442 carotid arteries included in our study.
At the time of the initial scan a complete medical history was taken, and the following risk factors were recorded: age, sex, CAD (angina pectoris, myocardial infarction, coronary artery bypass grafting procedure, or percutaneous transluminal coronary angioplasty), DM (patients on diet, oral hypoglycemic agents, or insulin or with fasting glucose levels >7 mmol/L), hypertension (blood pressure >160 mm Hg systolic and/or 95 mm Hg diastolic), hypercholesterolemia (total cholesterol >5.2 mmol/L), and smoking status (1, never smoked; 2, quit >3 years; 3, current smoker). All patients with 1 or more risk factors were aggressively treated. The adequacy of treatment was ensured by the regular follow-up.
Among the arteries studied, 290 (65.6%) were asymptomatic, 62 (14%) had caused transient ischemic attack (TIA) or amaurosis fugax, and 90 (20.4%) had caused stroke. Of these arteries, 320 belonged to men (72.4%) and 122 to women (27.6%). At the time of the initial scan, mean age of the patients was 66.8 years (range, 40 to 85 years), and mean stenosis was 45% (range, 30% to 95%). Initial stenosis was >50% in 136 arteries (30.8%) and <50% in 306 (69.2%). Diabetes mellitus (DM) was present in 134 cases (30.3%), hypertension in 248 (56.1%), CAD in 145 (32.8%), hypercholesterolemia in 139 (31.4%), and history of smoking in 370 (83.7%).
The ultrasonographic characteristics of the plaques were also recorded, with the plaques being divided into 5 categories: 44 (10%) were uniformly echolucent (type I), 19 (4.3%) hemorrhagic, 136 (30.7%) predominantly echolucent (type II), 146 (33%) predominantly echogenic (type III), and 97 (22%) echogenic (type IV). The presence of intraplaque hemorrhage was suggested by a hypo-anechogenic stria separating the intimal plaque from the media-adventitia complex. Only plaques that definitely fulfilled this criterion were characterized as hemorrhagic.
All patients were followed with a color duplex scan every 6 months. An ATL Interspec Apogee scanner with a 7.5-MHz probe was used (Advanced Technologies Laboratories). Eight categories of carotid stenosis (expressed as the percent decrease in artery diameter) were defined on the basis of the B-mode image and on velocity criteria: ICA peak systolic velocity (PSV), end-diastolic velocity (EDV), and ICA/common carotid artery PSV ratio1 (Table 1). Patients were classified according to the highest degree of stenosis identified (maximum stenosis).
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The main outcome measures were the progression in the degree of ICA stenosis, as defined by any change to a higher category of carotid stenosis, as well as the development of symptoms related to the carotid stenosis, ie, TIA, amaurosis fugax, or ischemic stroke. Follow-up was terminated at the date of death, stroke, total occlusion, or carotid endarterectomy.
Statistical analysis was performed by multiple linear regression analysis and Cox proportional hazards regression analysis. Results were considered statistically significant when the P value was <0.05.
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Results |
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The ultrasonographic characteristics of the carotid plaques were evaluated with respect to the traditional risk factors for atherosclerosis. Multiple linear regression analysis was performed with the ultrasonographic characteristics as the dependent variable, while independent variables were sex; age; presence of CAD, hypertension, or hypercholesterolemia; and history of smoking. The results of the analysis showed that echogenic plaques (Table 2) were more often found in men (P=0.014), in patients with CAD (P=0.017), and in smokers (P=0.025). Sixty-five percent of male patients had echogenic plaques compared with only 49% of women. Similarly, 70% of patients with CAD had echogenic plaques, while in patients without CAD echogenic plaques were found in 54%. Smoking was also significantly associated with echogenic plaques, with 69% of smokers having this type of plaque. The respective value in nonsmokers was 48% and in quitters 57%.
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Echolucent plaques (Table 3) were more often found in women (P=0.005) and in patients with DM (P=0.022). Thirteen percent of female patients had echolucent plaques compared with only 6% of men. Similarly, 11% of diabetics had echolucent plaques, while in patients without DM echolucent plaques were found in 6%.
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No statistically significant association was found between hemorrhagic or predominantly echolucent plaques and any of the recorded risk factors.
To identify factors affecting symptomatology, a multiple linear regression analysis was performed with history of stroke at the time of entry in the study as the dependent variable, while independent variables were the traditional risk factors of atherosclerosis as well as the ultrasonographic characteristics of the plaques. Analysis (Table 4) revealed a trend toward higher frequency of strokes in men (P=0.076; odds ratio, 2.5; 95% CI, 1.3 to 5.0), patients with hypertension (P=0.072; odds ratio, 1.9; 95% CI, 1.1 to 3.2), and patients with echolucent plaques (P=0.086; odds ratio, 1.9; 95% CI, 1.1 to 3.4). History of stroke was present in 24% of men compared with 11% of women, in 24% of hypertensives compared with 15% of patients with normal blood pressure, and in 32% of patients with echolucent plaques, while the respective value in patients with other types of carotid plaques was 19%. No statistically significant association was found between history of TIAs or amaurosis fugax and any of the recorded risk factors.
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All of our patients were prospectively observed for a mean of 44 months (range, 12 to 120 months), leading to a total of 1620 artery-years of follow-up. The average number of follow-up duplex scans was 7.3±5.2 per patient (range, 2 to 20), while the total number of duplex scans that were performed was 3240. Significant progression of stenosis, resulting in a change of 1 or more spectral categories of carotid stenosis, occurred in 82 cases (18.5%). The mean annual frequency of stenosis progression was 5%. Two carotids progressed to total occlusion, both in male patients, 1 with uniformly echolucent and 1 with uniformly echogenic plaque. The first one progressed from 20% stenosis to total occlusion in 4 years and the second from 70% stenosis to total occlusion in 2 years. Both of them remained asymptomatic at the time of occlusion.
Multiple linear regression analysis (Table 5) revealed that the frequency of stenosis progression was higher in patients with CAD (25% versus 15%; P=0.021), as well as in patients with echolucent plaques (25% versus 18%; P=0.020). Younger patients also showed a trend toward higher frequency of stenosis progression (P=0.092).
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During the follow-up period, 387 (87.6%) of the cases remained asymptomatic, 39 (8.8%) experienced a TIA, and 16 (3.6%) experienced a stroke. All of the patients who developed neurological symptomatology during the follow-up period were submitted to CT of the brain. Among the patients with TIAs, 4 infarcts (10.3%) (2 cortical and 2 subcortical) were revealed at the territory of the middle cerebral artery at the symptomatic hemisphere, while 2 subcortical infarcts (5.1%) were found at the contralateral (asymptomatic) hemisphere. Among the patients with stroke, 6 cortical (37.5%) and 10 subcortical (62.5%) infarcts were recognized at the territory of the middle cerebral artery of the symptomatic hemisphere, while 2 subcortical infarcts (12.5%) were observed at the contralateral (asymptomatic) hemisphere.
Cox proportional hazards regression analysis showed that severity of carotid stenosis, history of neurological events, progression of stenosis, echolucent plaques, and hypertension were independent predictors of future neurological events (Table 6). The annual risk of stroke in the initially symptomatic patients with <50% carotid stenosis was 1.4% (8 patients overall), while the annual risk of TIA was 3.4% (19 patients). However, 7 of the 8 patients who experienced a stroke and 16 of the 19 patients who experienced a TIA had progressed to 
50% stenosis at the time of the neurological event. The annual risk of stroke and TIA in the asymptomatic patients with <50% stenosis was 0.2% (1 patient) and 0.4% (2 patients), respectively. In the asymptomatic patients with 50% to 69% stenosis, the annual stroke rate was 0.9% (3 patients) and the annual TIA rate 2.3% (8 patients), while in the asymptomatic patients with 70% stenosis, the respective values were 2.5% (4 patients) and 6.3% (10 patients).
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In regard to progression of stenosis, the annual risk of stroke in patients with progressive lesions was 3% versus 0.5% in patients whose lesions did not progress, while the annual risk of TIA was 5.6% versus 1.7%, respectively. The ultrasonographic characteristics of the plaques were also associated with the development of neurological events. The annual risk of stroke in patients with echolucent plaques was 2.4% versus 0.8% in patients with the other types of plaques, while the annual risk of TIA was 4.3% versus 2.2%, respectively. None of the other types of plaques was significantly correlated with the occurrence of neurological events.
Among the various traditional risk factors, the only one that proved to be an independent predictor of future cerebrovascular events was hypertension. Yearly risk of stroke and TIA in patients with hypertension was 1.5% and 3.6%, respectively, versus 0.7% and 1.8% in patients with normal blood pressure.
Ninety-two carotid arteries were submitted to endarterectomy, and 33 patients died of various causes during the 10-year follow-up. Indications for surgery were the development of neurological symptomatology in 45 patients and the asymptomatic progression to stenosis >70% in 47 patients. In patients with progressive lesions, endarterectomy was performed in 47 of the 56 patients who remained asymptomatic (since the other 9 did not progress to >70% stenosis), in 5 of the 9 patients who experienced stroke (since the other 4 had disabling or fatal strokes), and in all of the 17 patients who had TIAs. Among the patients with stable lesions, endarterectomy was performed in 19 of the 22 patients who had TIAs (since the other 3 had stenosis <50%) and in 4 of the 7 patients who presented with stroke (since the other 2 had disabling injuries and 1 patient had low-degree stenosis).
CAD was the leading cause of death in our patients, accounting for 25 deaths (75.8%). Three patients (9.1%) died of cancer, 2 patients (6.1%) had fatal strokes, and 3 patients (9.1%) died of miscellaneous causes.
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Discussion |
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Extensive research over the past decade has identified several factors associated with carotid stenosis as powerful predictors of subsequent stroke. While there is some variation in the findings of different studies, at least 2 factors are universally accepted as being associated with an increased risk of future stroke: severity of stenosis and history of neurological events. On the basis of these factors, 3 large-scale, multicenter, randomized trials2–4 have recommended carotid endarterectomy in symptomatic patients with >70% stenosis of the ICA and in asymptomatic patients with >60% stenosis. However, even in these high-risk groups, the majority of carotid lesions remained clinically silent during the study period (in the North American Symptomatic Carotid Endarterectomy Trial [NASCET], 2 risk of any ipsilateral stroke at 2 years was 26%), indicating that our ability to predict future strokes needs further improvement. In this context, factors other than the degree of stenosis are being studied.
Several investigators have compared carotid plaques removed from symptomatic and asymptomatic patients to define the histopathologic characteristics of the unstable plaque. However, the results of these studies are inconsistent. Some authors report that intraplaque hemorrhage is more common in symptomatic patients, 5–7 while others have failed to verify these findings.8–13 Similarly, plaque rupture or ulceration5,13 and lumen thrombus13 have been implicated by some investigators, while others have not found them to be of prognostic significance.8,9 Inflammation, as demonstrated by increased numbers of macrophages and T lymphocytes, may also play a key role in the development of symptoms by causing thinning of the fibrous cap and, eventually, plaque rupture.9,14,15 In regard to the core of the plaques, the volume of the necrotic core does not seem to differ significantly between symptomatic and asymptomatic patients.16 The same is true of the volume of the lipid core, with the exception of 1 study12 in which it was found that plaques removed from symptomatic patients contained more extracted lipid and cholesterol than those from asymptomatic patients. To summarize the existing data, Golledge et al17 reviewed the results of previous histology studies comparing symptomatic and asymptomatic plaques. They conclude that surface ulceration and plaque rupture as well as thinning of the fibrous cap and infiltration of the cap by greater numbers of macrophages and T cells are characteristic features of unstable plaques.
Histopathologic examination of the carotid plaques has undoubtedly provided useful information on the pathogenesis of neurological events. However, patients are in greater need of a method of preoperative identification of high-risk carotid plaque. High-resolution B-mode ultrasonography has been widely used for this purpose, and its ability to characterize carotid plaques is currently considered a major advantage over arteriography. Almost all authors agree that echolucent plaques or plaques with gray scale median <32 are associated with a higher frequency of cerebrovascular symptoms.18–24 These findings are in accordance with the results of our study, in which patients with echolucent plaques showed a trend toward higher frequency of neurological events in their history and a significantly higher risk of future neurological events.
Histological studies performed in specimens removed during carotid endarterectomy have been able to correlate the ultrasonographic characteristics of the plaque with its composition. It has been shown that echolucent plaques are associated with an increased lipid content, rendering them more vulnerable to rupture and future cerebrovascular events. On the contrary, echogenic plaques consist mainly of fibrin and collagen, which makes them more stable.22,25–28
Our study also revealed that neurological events occurred more frequently in patients with progression of stenosis than in patients with stable lesions. Several risk factors have been studied to identify groups of patients at higher risk for progression of stenosis. Young29 or old30,31 age, degree of initial stenosis,29,30 smoking,31 CAD,32 low levels of HDL cholesterol,29 high levels of lipoprotein(a)29 and LDL cholesterol,31 high blood pressure,33 low ankle-brachial index,33 and high PSV33 have been implicated in progression of ICA stenosis. Nevertheless, other studies have failed to document any association between progression of stenosis and age,33 sex,30,33,34 DM,30,33,34 smoking,30,33,34 CAD,30,33,34 hypercholesterolemia,33 or initial clinical presentation.33,34 In accordance with these studies, no statistically significant correlation was found between the aforementioned factors and progression of stenosis in our series, except for CAD, which was found to be associated with a higher frequency of progression of stenosis. Progression of stenosis was also significantly associated with the ultrasonographic characteristics of the plaques. Uniformly echolucent plaques (type I) showed a higher frequency of progression of stenosis (31.8%) than other types of plaques. These results are in contrast with the findings of Iafrati et al,30 who did not find plaque morphology to play a significant role in progression of stenosis.
In conclusion, factors other than the degree of stenosis are also important in determining high-risk carotid plaque. In our study hypertension, echolucent plaques, and progressive lesions were associated with an increased risk of neurological events. Taking these factors into account when dealing with patients with carotid stenosis would help us identify more accurately the patients at greater risk for the development of cerebrovascular symptoms.
Received March 27, 2001; revision received September 11, 2001; accepted September 12, 2001.
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