Carotid Artery Restenosis: Ultrasonographic Characteristics

Scientific Articles The Journal for Vascular Ultrasound 35(1):7–10, 2011 Carotid Artery Restenosis: Ultrasonographic Characteristics Miguel Maia, MD, RVT; Joana Ferreira, MD; Sandrina Braga, MD; João Vasconcelos, MD; Pedro Brandão, MD; Guedes Vaz, MD ABSTRACT Introduction.—The purpose of our study was to evaluate the ultrasonographic characteristics of recurrent carotid stenosis in patients submitted to carotid endarterectomy with patch angioplasty. Methods.—We performed carotid ultrasound examinations on patients who had undergone unilateral carotid endarterectomy between 2002 and 2009. Patients with bilateral and/or endovascular procedures were excluded. All ultrasound examinations were performed by the same registered vascular technologist. Results.—One hundred male and 25 female patients were studied. The average time between surgery and the ultrasound examination was 38.8 months (range, 3–99.2 months). Twenty-nine (23.2%) patients had recurrent carotid artery stenosis after unilateral endarterectomy. Of these, 17 patients were found to have recurrent carotid artery stenosis classified as <50%; 7 patients had recurrent stenosis in the range of 50% and 69%, and 5 patients had >70% diameter-reducing lesions. Plaques associated with recurrent carotid stenosis were significantly less echogenic, more acoustically homogenous, and had a smoother surface contour. Compared with the primary carotid stenosis (nonintervened side), plaques associated with recurrent carotid stenosis were more often hypoechoic (58.6% versus 8.1%), acoustically homogenous (69% versus 44.6%) and smoothsurfaced (93.1% versus 74.3%). Also, the longer the interval between surgery and the carotid sonographic examination, the more similar the ultrasonographic characteristics were between the two groups. Conclusions.—The different sonographic characteristics of primary carotid stenosis and recurrent stenosis after carotid endarterectomy in the same patients, are associated with different outcomes for the two conditions. There is a current clinical consensus that patients presenting with recurrent symptoms after carotid endarterectomy should be treated, but the best management for asymptomatic patients with recurrent carotid artery stenosis remains uncertain. Introduction Carotid restenosis is a different entity than the initial atherosclerotic disease. Although relatively common after carotid endarterectomy, recurrent carotid artery stenosis is seldom symptomatic.1–3 The lesion associated with carotid restenosis is most often histologically different than the typical atherosclerotic carotid lesion.1 Lesions recurring within the first 2 years after carotid endarterectomy are commonly fibrotic and less prone to embolization. Beyond 2 years, recurrent carotid artery lesions may be associated with thromboembolic ischemia.4,5 The purpose of our study was to evaluate recurrent carotid stenosis by assessing sonographic characteristics of recurrent lesions and to correlate the From Servico de Angiologia e Cirurgia Vascular, Rua Conceicao Fernandes, Vila Nova de Gaia, Portugal. Presented at the 2010 Society for Vascular Ultrasound Annual Conference, June 2010, Boston, MA, as poster. Address correspondence to: Miguel Maia, MD, RVT, Servico de Angiologia e Cirurgia Vascular, Rua Conceicao Fernandes, 4434-502 Vila Nova de Gaia, Portugal. E-mail: [email protected] findings with the presence of neurological symptoms and time after surgery. Methods All patients submitted to unilateral carotid endarterectomy with patch angioplasty at our institution between 2002 and 2009 were asked to present for a carotid ultrasound examination and a clinical interview. Patients with bilateral and/or endovascular procedures were excluded from our study. All ultrasound examinations were performed by the same physician, who is a registered vascular technologist. In all cases, bilateral (intervened and nonintervened sides) carotid duplex examinations were performed. The criteria used for classification of carotid artery restenosis on the intervened side were those published in the Journal of Vascular Surgery by AbuRahma et al.6 A peak systolic velocity ≥213 cm/sec was predictive of ≥50% restenosis, and a peak systolic velocity ≥274 was suggestive of ≥70% restenosis. For the evaluation of nonintervened sides, the classification of carotid artery 8 JVU 35(1) MAIA ET AL. stenosis was determined by criteria established by the Society of Radiologists in Ultrasound Carotid Consensus Conference.7 We used different criteria for each side because intervened carotid arteries are known to have distinct wall properties and therefore different standard normal velocities.6 The following sonographic characteristics for both recurrent lesions and stenotic atherosclerotic plaques were assessed: echogenic features (hypoechoic, medium echogenic or hyperechoic); acoustic uniformity (homogeneous or heterogeneous); and plaque surface characteristics (smooth or irregular). The clinical interview focused on the recognition of new cerebrovascular events and management of atherosclerotic risk factors. All data were recorded by the use of Excel 2003 (Microsoft, Redmond, WA), and the Statistical Package for Social Sciences (SPSS, Chicago, IL) was used for data analysis. A p value of less than 0.05 was considered to be significant. Table 1 Sonographic Characteristics of Primary Carotid Plaques and Restenosis Lesions Nonintervened Side N (%) Intervened Side N (%) p Value 52 (70.3) 16 (21.6) 3 (10.3) 9 (31) <0.001 6 (8.1) 17 (58.6) Echogenicity Hyperechoic Medium echogenic Hypoechoic Acoustic uniformity Heterogeneous Homogeneous Plaque surface Irregular Smooth 41 (55.4) 33 (44.6) 9 (31) 20 (69) 0.030 19 (25.7) 55 (74.3) 2 (6.9) 27 (93.1) 0.054 Results One hundred male and 25 female patients were studied. The average time between surgery and the ultrasound examination was 38.8 months (range, 3–99 months; SD, 25.6 months; median, 36 months). Our protocol includes postoperative carotid duplex examinations at discharge, 1, 3, 6, and 12 months after surgery and annually thereafter; however, less than one-half of these patients attended all examinations. Therefore, for the purposes of this study, we did not use data from previous carotid ultrasound examinations. Of the 125 patients evaluated, recurrent carotid stenosis was identified in 29 patients. Seventeen patients had recurrent carotid artery stenosis classified as <50% diameter-reducing, 7 patients had recurrent stenosis between 50% and 69% on the operated side, and 5 patients were found to have recurrent stenosis that exceeded >70%. One internal carotid artery was occluded. Review of these data indicates that 12 (9.6%) patients had restenosis that narrowed the carotid artery by more than 50%. Seventy-four patients exhibited carotid plaques on the nonintervened side. Forty-nine of these patients presented stenosis <50% diameter-reducing whereas 22 patients exhibited lesions that were classified as 50% to 69% diameter-reducing, and 3 patients had lesions that narrowed the carotid artery >70%. Four internal carotid arteries were found to be occluded. In summary, 20% (n = 25) of patients were found to have carotid artery plaques exceeding >50% diameter-reduction on the nonintervened side. As illustrated in Table 1, compared with primary atherosclerotic plaques, recurrent carotid artery lesions were more often hypoechoic (58.6% versus 8.1%; p < 0.001), more acoustically homogenous (69% versus 44.6%; p = 0.03), and had a smoother surface contour (93.1% versus 74.3%; p = 0.054). Primary stenosis plaques (nonintervened side) were more often hyperechoic (70.3% of the total plaques identified), slightly more acoustically heterogeneous (55.4%), and had a smoother surface contour (74.3%; Table 1). Furthermore, the sonographic characteristics of recurrent lesions correlated with time after surgery. All of the early recurrent carotid lesions (less than 2 years after carotid endarterectomy) demonstrated hypoechoic characteristics. However, 9 recurrent lesions (42.9%) that were at least 2 years postintervention demonstrated hypoechoic features, 9 (42. 9%) were medium echogenic, and, surprisingly, 3 (14.3%) had characteristics that were consistent with hyperechogenicity. This difference was statistically significant (p = 0.021). There was no statistically significant difference in acoustic uniformity and plaque surface contour between patients who were studied less than 2 years after endarterectomy and patients who had undergone carotid endarterectomy more than 2 years before their carotid sonographic examination (Table 2). Since their surgery, none of the patients with restenosis had ipsilateral (intervened side) cerebrovascular symptoms. During this period, 2 patients had symptoms in the contralateral hemisphere (nonintervened side), one patient experienced a transient ischemic attack and one patient had a completed stroke, Table 2 Sonographic Characteristics of Restenosis Lesions Correlated with Time after Surgery Echogenicity Hyperechoic Medium echogenic Hypoechoic Acoustic uniformity Heterogeneous Homogeneous Plaque surface Irregular Smooth <2 Years N (%) ≥2 Years N (%) 0 (0) 0 (0) 8 (100) 3 (14.3) 9 (42.9) 9 (42.9) 4 (50) 4 (50) 5 (23.8) 16 (76.2) 0.209 0 (0) 8 (100) 2 (9.5) 19 (90.5) 1.000 p Value 0.021 2011 CAROTID ARTERY RESTENOSIS attributed to concomitant cardiac disease. None of these symptomatic patients had carotid stenosis. Discussion Recurrent carotid stenosis, defined as a >50% diameter reduction, is relatively common after carotid endarterectomy, but few patients develop symptoms. Most authors report an incidence of restenosis from 1% to 37%, but fewer than 8% of patients become symptomatic.1,8 Some investigators indicate that the risk of restenosis is approximately 10% in the first year, 3% in the second year, and 2% in the third year, with a long-term rate of restenosis approximating 1% per year.4 The pathology of early carotid restenosis after endarterectomy is different than the pathology of lesions associated with late restenosis. In the first 2 years, recurrent carotid stenosis is mainly caused by intimal hyperplasia and may quickly regress.2,9 This type of lesion is considered benign and less prone to embolization.4,5,9 Late carotid restenosis originates mainly from atherosclerotic development, and thus, may induce thromboembolic ischemia.4 Therefore, this late restenosis is clinically threatening and more important to detect. Carotid occlusion, in patients without carotid interventions, has been considered to be a benign event and usually not associated with neurological symptoms, but some publications have shown a 10% risk of ipsilateral stroke.5 We detected 29 lesions associated with recurrent carotid artery stenosis after endarterectomy, with 12 (9.6% of total patients evaluated) lesions corresponding to stenosis greater than or equal to 50%. One (0.8%) internal carotid artery was occluded. None of these patients had ipsilateral neurological symptoms. There is confounding data about the risk of stroke or transient ischemic attack in patients with restenosis after carotid endarterectomy. Most authors report that fewer than 8% of patients with carotid restenosis become symptomatic.1 Some emphasize that the incidence of stroke or transient ischemic attack is not statistically different in patients with and without restenosis.9 Bernstein et al.2 showed that there was a significantly greater life expectancy among patients with restenosis after carotid endarterectomy and that stroke was less likely to occur in those patients. Their conclusion was that patients with carotid restenosis were less likely to have late symptoms, stroke, or early death compared with patients with normal postoperative examinations. Recurrent lesions tend to be hypoechoic, acoustically homogenous, and smooth-surfaced. These findings suggest a more stable and fibrous plaque than the lesions associated with most primary carotid artery atherosclerotic plaques.1 In our series, more than one-half of the recurrent lesions were hypoechogenic, acoustically homogeneous, and almost all had a smooth surface. Interestingly, all recurrent lesions occurring less than 2 years after surgery had hypoechoic features. In 9 contrast, stenotic lesions occurring later than 2 years after endarterectomy exhibited both hypoechogenic and medium echogenic features, and some had hyperechogenic characteristics. These data suggest a variation in the composition of recurrent lesions, changing from a stable and relatively benign condition to a potentially more dangerous and emboligenic one. Nevertheless, our data does not support an increased risk for patients with restenosis occurring more than 2 years after carotid endarterectomy because all patients were asymptomatic. In the available literature, no specific sonographic characteristics were predictive for the development of ipsilateral neurological symptoms in patients with carotid restenosis after endarterectomy.5 These ultrasound characteristics, especially if easily and economically identifiable, should be determined because they may yield valuable clues about which patients would benefit most from a reintervention. Carotid duplex sonography is the preferred method for follow-up after carotid endarterectomy. The reported sensitivity and specificity of this modality in identifying a 50% restenosis of the carotid artery is 91% and 87%, respectively.4 The follow-up protocol is still nonconsensual. Some investigators believe that frequent testing results in large number of false-positive reports of recurrent carotid stenosis. These authors recommend that ultrasound examinations should be performed with large intervals between examinations.4 Other investigators believe that ultrasound studies after carotid endarterectomy are unnecessary and cannot be justified as a mean of preventing late strokes related to recurrent stenosis.2,10 Still others believe that frequent follow-up is beneficial and advocate postoperative ultrasound examinations at 3 days, 1, 3, 6, and 12 months and annually thereafter.2 Our follow-up protocol includes ultrasound examinations at discharge, 1, 3, 6, and 12 months after surgery and annually thereafter. However, motivate patients to follow our protocol is difficult and only less than one-half of our patients attend all examinations. Regardless of frequency of follow-up, there is a consensus that patients presenting with symptomatic restenosis after carotid endarterectomy should be treated.1 The best management for asymptomatic patients, however, remains uncertain. Sadideen and colleagues1 defend an aggressive approach in the treatment of most asymptomatic restenosis. They argue that there is the possibility of a high-grade restenosis progressing to carotid occlusion, and simultaneous stroke, and therefore, almost all asymptomatic patients should be treated.1,5 Others advocate that asymptomatic carotid restenosis is a benign condition and should not be treated.2,9 On the basis of our experience, we believe that treatment should be reserved for symptomatic patients and for asymptomatic patients with high-grade recurrent stenosis (at least 70% diameter reduction) after endarterectomy. Currently, we only treat asymptomatic patients with high-grade restenosis that has persisted at least 2 years after surgery or patients who have demonstrated progression in severity of restenosis, hence 10 JVU 35(1) MAIA ET AL. at risk of carotid occlusion. Endovascular carotid angioplasty and stenting is our preferred method for treatment of restenosis after carotid endarterectomy. Conclusion The different sonographic characteristics between primary carotid stenosis and restenosis after carotid endarterectomy, in the same patients, indicate a different outcome for the two conditions, and thus, the need for different treatment strategies. Even more, there is a difference in sonographic characteristics between lesions that occur less than 2 years after carotid endarterectomy and lesions that occur more than 2 years after surgery. This difference may preclude a different risk concerning thromboembolic complications. There is still a lack of a consensus regarding the management of recurrent carotid stenosis. Most studies have few patients enrolled and do not offer clear conclusions about treatment. We endorse reintervention in symptomatic patients with carotid restenosis. We also advocate reintervention of high-grade carotid restenosis in asymptomatic patients, whose lesions have recurred or persisted more than 2 years after surgery. References 1. Sadideen H, Taylor PR, Padavachee TS. Restenosis after carotid endarterectomy. Int J Clin Pract 2006;60:1625–1630. 2. Bernstein EF, Torem S, Dilley RB. Does carotid restenosis predict an increased risk of late symptoms, stroke, or death? Ann Surg 1990;212:629–636. 3. Mattos MA, Shamma AR, Rossi N, et al. Is duplex follow-up cost-effective in the first year after carotid endarterectomy? Am J Surg 1998;156:91–95. 4. Frericks H, Kievit J, van Baalen JM, van Bockel JH. Carotid recurrent stenosis and risk of ipsilateral stroke: A systematic review of the literature. Stroke 1998;29:244–250. 5. O’Donnell TF, Rodrigues AA, Fortunato JE, Welch HJ, Mackey WC. Management of recurrent carotid stenosis: Should asymptomatic lesions be treated surgically? J Vasc Surg 1996;24:207–212. 6. AbuRahma AF, Stone P, Deem S, Dean LS, Keiffer T, Deem E. Proposed duplex velocity criteria for carotid restenosis following carotid endarterectomy with patch closure. J Vasc Surg 2009;50:286– 291. 7. Grant EG, Benson CB, Moneta GL, et al. Carotid artery stenosis: Gray-scale and Doppler US diagnosis—Society of Radiologist in Ultrasound Consensus Conference. Radiology 2003;229:340–346. 8. Lattimer CR, Burnand KG. Recurrent carotid stenosis after carotid endarterectomy. Br J Surg 1997;84:1206–1219. 9. Healy DA, Zierler RE, Nicholls SC, et al. Long-term follow up and clinical outcome of carotid restenosis. J Vasc Surg 1989;10:662– 669. 10. Mackey WC, Blekin M, Sindhi R, Welch H, O’Donnell TF Jr. Routine postendarterectomy duplex surveillance: Does it prevent late stroke? J Vasc Surg 1992;16:934–939.