- Email: [email protected]
Open surgery remains a valid option for the treatment of recurrent carotid stenosis
Open surgery remains a valid option for the treatment of recurrent carotid stenosis Raphaël Coscas, MD, Badre Rhissassi, MD, Noémie Gruet-Coquet, MD, Thibault Couture, MD, Christian de Tymowski, MD, Laurent Chiche, MD, Edouard Kieffer, MD, and Fabien Koskas, MD, Paris, France Objective: The choice between open surgery (OS) and transluminal carotid angioplasty with stenting (CAS) for the treatment of primary carotid stenosis remains controversial. However, CAS is considered a valid option for selected cases, such as recurrent carotid stenosis (RCS). Tertiary RCS seems to be a concerning issue after CAS but few large reports focused on the durability of CAS and OS. We report our early and long-term results with OS for RCS. Methods: From 1989 to 2006, perioperative data regarding 4245 consecutive surgical carotid reconstructions was prospectively collected. Patients whose indication was RCS were subjected to further analysis. Indications for surgery were symptomatic RCS >50% or asymptomatic RCS >80%. Freedom from neurologic event was defined as the absence of any ipsilateral symptom at any time after the procedure. Kaplan-Meier analysis was used to estimate freedom from reintervention, freedom from restenosis >50% and occlusion, freedom from neurologic event and survival. Results: A total of 119 patients (2.8%) with RCS underwent OS. The average time from the primary OS was 59.4 ⴞ 54.5 months (range, 2-204). Forty-nine patients (41%) were symptomatic. In 103 patients (87%), the technique did not differ from a primary approach. Postoperative (<30 days) combined stroke and death rate was 3.3%. Cranial nerve injury occurred in 5 cases (4.2%). With a mean follow-up of 53 ⴞ 48 months (range, 1-204), 3 patients had an ipsilateral stroke (including one hemorrhagic stroke) and 7 were diagnosed with a tertiary RCS >50%. At 5 years, Kaplan-Meier estimates of freedom from reintervention, freedom from restenosis and occlusion, freedom from neurologic event, and survival were 99%, 91%, 89%, and 91%, respectively. Conclusion: OS for RCS is not a high-risk procedure and provides excellent long-term results, with low rates of tertiary RCS and reinterventions. The comparison between OS and CAS in this indication suffers from the absence of standardized follow-up paradigms after primary OS and the lack of prospective randomized trial comparing the two techniques. Despite these limitations in the available data, we conclude that OS should remain the first line therapy when treatment of RCS is indicated. ( J Vasc Surg 2010;51:1124-32.)
Carotid artery endarterectomy (CAE) has been demonstrated to be the best option to prevent stroke for patients with high-grade symptomatic1,2 or asymptomatic3,4 carotid stenosis. Despite excellent immediate results, recurrent carotid stenosis (RCS) remains a concern whose incidence is dependent upon the surgical technique, the method of imaging utilized for surveillance, the definition of RCS, and the length of follow-up.5 A controversy remains regarding the choice between open surgery (OS) and transluminal carotid angioplasty with stenting (CAS) for the treatment of primary carotid stenosis. Although early results of the stent-protected angioplasty vs carotid endarterectomy (SPACE) trial and the Endarterectomy versus Angioplasty in Patients with Symptomatic Severe Carotid Stenosis (EVA-3S) trial were in favor of OS for the treatment of symptomatic cases,6,7 intermediate-term results of these two prospective randomized trials demonstrated similar clinical outcomes for both techniques.8,9 In the EVA-3S trial, one main reason for the From the Department of Vascular Surgery, Hôpital Pitié-Salpêtrière. Reprint requests: Raphaël Coscas, MD, 106, rue de la glacière, 75013 Paris, France (e-mail: [email protected]). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a competition of interest. 0741-5214/$36.00 Copyright © 2010 by the Society for Vascular Surgery. doi:10.1016/j.jvs.2009.12.020
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difference observed during the early postoperative period was a low rate of complications after primary CAE in specialized centers.6 Therefore, it has been suggested that CAS could provide a significant advantage in situations where OS provides its worst results. The treatment of RCS has been considered to be a high-risk procedure. The dissection of the carotid artery in a previously operated field would be expected to carry a higher risk of local complications such as cranial nerve injury (CNI) and wound hematoma. Difficulties in controlling the carotid artery could increase the risk of cerebral emboli. Using a puncture distant from the site of the RCS, CAS has been suggested to be an interesting alternative in these situations. Despite the lack of prospective comparative trials, its early results seemed to compare favorably with OS in the management of RCS.10,11 However, several authors emphasize that the surgical approach to RCS may not be technically demanding and historic series reporting on OS to treat RCS have concluded that this procedure provides early results comparable to those reported with primary CAE.12,13 Long-term results of both techniques have not been well studied. The durability of CAS for RCS is poorly known, whereas only two recent large series (⬎100 patients) reported on late results of OS.12,13 These considerations are paramount because patients with RCS are often in their seventh or eighth decades and may be expected to
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live for 5 years or more after reintervention. Recommendations of public authorities and vascular societies regarding management of RCS could not conclude whether CAS or OS was the most appropriate treatment for menacing RCS because of the absence of comparative trials and the lack of long-term follow-up data.14,15 The aim of this study is to report our results with OS in the management of RCS, focusing on long-term outcomes. MATERIALS AND METHODS Data collection and patient selection. From January 1989 to December 2006, perioperative data of 4245 consecutive carotid reconstructions performed in our department were prospectively collected in a database. Patients whose intervention was a redo procedure were identified and only cases whose indication was RCS were selected and subjected to further analysis. Patients who underwent another concomitant vascular repair at the time of the RCS repair were excluded. Repairs of intrathoracic supra-aortic trunks were excluded, as were aneurysmal degenerations of previous endarterectomy patches. Surgical management. All patients referred for the management of RCS underwent confirmation of the recurrence using two different imaging methods including a duplex ultrasound scan in all cases associated with a non-operatordependent method (CT scan, MRI, and/or carotid angiography). Surgery was indicated for patients with symptomatic stenosis ⬎50% and high-grade asymptomatic stenosis ⬎80% (North American Symptomatic Carotid Endarterectomy Trial [NASCET] criteria). Patients presenting with intracranial stenosis that exceeded the severity of the extracranial stenosis, severe disability from stroke, short life expectancy, or inability to give informed consent were not offered surgery. Interventions for RCS were performed under general anesthesia by a senior surgeon (L.C., E.K., F.K.). The surgical approach always consisted of a redo anterior cervicotomy along the sternocleidomastoid muscle, as for a primary intervention. Technically, we usually preferred to first control the common carotid artery (CCA) and the internal carotid artery (ICA) in nondissected portions, and then to dissect the carotid bulb after clamping. After identification and control of the main carotid vessels, a systemic bolus of 0.5 mg/kg of unfractioned heparin was administered intravenously before clamping. Occlusion of the external carotid artery was frequently obtained through the inflation of a 5F intravascular Fogarty catheter (Edwards Lifesciences Corporation, Irvine, Calif). Selective shunting was used in the presence of preoperative severe stenosis and/or occlusion of other major cerebral vessels (contralateral carotid artery, vertebral arteries) or intraoperative finding of nonpulsatile reflux from the distal ICA. Carotid artery reconstruction depended on the severity and extent of the lesion and was adapted to each case at the discretion of the vascular surgeon. Preference was given to the simplest procedure. Dacron patch (Hemacarotid Patch; Intervascular Datascope, La Ciotat, France) angioplasty with or without intimectomy was used whenever it was possible. In
Coscas et al 1125
cases of obvious smooth plaque suggesting myointimal hyperplasia, intimectomy was not performed and a simple patch angioplasty was performed. When the extent of the lesion rendered the use of a bypass mandatory, a prosthetic polytetrafluoroethylene graft (Thin-walled tubular graft; GoreTex, Flagstaff, Ariz) was used, except in the presence of a distal ICA with reduced diameter (⬍3.5 mm) where a saphenous vein graft was used. At the end of the procedure, selective angiography was performed to assess the patency of the repair. Postoperatively, all patients returned to a conventional hospital ward and were generally discharged at day 3-4 in the absence of any complication. Unless contraindicated, an oral antiplatelet agent (aspirin 75-250 mg daily or clopidogrel 75 mg daily) was administered to all patients before surgery and life-long. Follow-up. Duplex ultrasound scan was performed at 1 month, 6 months, 12 months, and yearly in the absence of a neurologic event and/or duplex scan anomaly. Data regarding long-term survival, neurologic state, and anatomic lesions of the ipsilateral carotid were retrospectively collected using medical charts and/or direct contact with the patient (or his relatives in case of death) by phone call. Freedom from neurologic event was defined as the absence of any ipsilateral neurologic event (transient ischemic attack and minor stroke included) after the procedure. Freedom from restenosis was defined as the absence of tertiary stenosis ⬎50% (NASCET criteria) or occlusion of the ipsilateral carotid artery on duplex ultrasound scan examination during follow-up. Statistical analysis. Demographic and periprocedural characteristics are shown as number (%) or mean ⫾ SD. Kaplan-Meier (KM) analysis was conducted to estimate survival, freedom from restenosis, neurologic event, and reintervention. The Statistical Package for the Social Sciences (SPSS) software version 13.0 (SPSS Inc, Chicago, Ill) was used for the statistical analysis. RESULTS One hundred nineteen consecutive patients operated on for RCS were subjected to further analysis. This subset represents 2.8% of the 4245 carotid reconstructions performed in our department during the same period. All were managed using OS and we never used CAS for RCS during this period. Demographics. Ninety-two patients (77%) were male and the mean age at reintervention was 69.6 ⫾ 8.9 years (range, 45-86). Cardiovascular risk factors were mainly a history of tobacco use in 69% and hypertension in 68% (Table I). Several patients presented with multifocal atherosclerosis including coronary artery disease (any symptom of heart ischemia, antecedent of coronary revascularization, and/or positive stress test) in 33%, and peripheral arterial disease (any peripheral arterial symptoms resulting from occlusive disease and/or antecedent of limb revascularization) in 22%. Thirty-four patients (29%) had a history of vascular surgery including aortoiliac repair in 18 (12 for aneurysm and 6 for occlusive disease), lower limb revascu-
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Table I. Preoperative clinical data of 119 patients who underwent an open surgery for recurrent carotid stenosis in our department (1989-2006)
Table III. Early postoperative complications (⬍30 days) in 119 patients who underwent an open surgery for recurrent carotid stenosis in our department (1989-2006)
Preoperative clinical data
Early postoperative complications (⬍30 days)
No. (%)
Deaths Including: Stroke Nonfatal neurologic complications Including: Stroke Transient ischemic attack Extra neurologic systemic complications Including: Myocardial infarction Local complications Including: Hematoma evacuation Cranial nerve injury
1 (0.8)
General Total population Age (years) Time from primary CAE (months) Male Left side Indication Symptomatic Including: TIA Stroke Asymptomatic Cardiovascular risk factors Tobacco use Hypertension Dyslipidemia Diabetes Chronic renal insufficiency Cardiovascular diseases Coronaropathy artery disease Including: myocardial infarction Peripheral arterial disease Previous arterial repair Aortoiliac* Lower limb CABG Renal artery Superior mesenteric artery
No. (%) 119 (100) 69.6 ⫾ 8.9 59.4 ⫾ 54.5 92 (77) 67 (56) 49 (41) 29 (24) 20 (17) 70 (59) 82 (69) 81 (68) 70 (59) 19 (16) 12 (10) 39 (33) 15 (13) 26 (22) 18 (15) 16 (13) 15 (13) 3 (3) 2 (2)
CAE, Carotid artery endarterectomy; TIA, transient ischemic attack; CABG, aorto-coronary bypass graft. *Including, 12 aneurysms and 6 occlusive disease.
Table II. Intraoperative technical adaptations used in our series Intraoperative technical adaptations Division of the occipital artery Division of the posterior belly of the digastric muscle Mobilization of the hypoglossal nerve Division of the stylohyoid muscles No technical adaptation
1 (0.8) 5 (4.2) 2 (1.7) 3 (2.5) 1 (0.8) 1 (0.8) 6 (5.0) 1 (0.8) 5 (4.2)
Table IV. Late complications (⬎30 days after the procedure) in 118 patients who survived the intervention after a mean follow-up of 53 ⫾ 48 months Late complications (⬎30 days)
No. (%)
Ipsilateral stroke Including: Ischemic Hemorrhagic Transient ischemic attack Recurrent occlusive disease Including: 50% to 80% stenosis 80% to 99% stenosis Ipsilateral carotid occlusion Tertiary intervention
3 (2.5) 2 (1.7) 1 (0.8) 1 (0.8) 7 (5.9) 5 (4.2) 1 (0.8) 2 (1.7)* 2 (1.7)
*Including one asymptomatic occlusion discovered during the immediate post-operative period.
N (%) 9 (8) 5 (4) 3 (3) 2 (2) 103 (87)
larization in 16, coronary bypass in 15, renal revascularization in 3, and superior mesenteric artery revascularization in 2 cases. The primary carotid intervention was an endarterectomy with patch suture in 56 patients (47%), an endarterectomy with direct suture in 41 patients (34%), a carotid bypass in 12 patients (10%), and an eversion in 10 patients (8%). The RCS was located on the left carotid in 67 cases (56%). The average time from the primary CAE to the intervention for RCS was 59.4 ⫾ 54.5 months (range, 2-204). Forty-nine patients (41%) were symptomatic. The main symptom was a transient ischemic attack (TIA) in 29 cases (including 8 amaurosis fugax) and a recent (⬍3 months) cerebral infarction with or without superimposed TIA in 20 cases. The remaining 70 asymptomatic patients
presented with high-grade RCS ⬎80% and/or rapidly progressive RCS on duplex ultrasound scan study. All patients underwent preoperative duplex ultrasound scan, and the second imaging method was a CT scan in 24 cases (20%), an MRI in 20 cases (17%), and an angiography in 75 cases (63%). Of note, no complication of carotid angiography was noted in this series. Surgical management. We always used an anterior approach along the sternocleidomastoid muscle and never used a retrojugular approach. In 103 patients (87%), the approach was defined as “simple” by the senior surgeon and did not necessitate any technical adaptation when compared to a primary approach. In the remaining 16 cases (13%), several technical modifications were used and are summarized in Table II. Intimectomy with patch angioplasty was used in 63 patients (53%) whereas prosthetic bypass graft was used in 31 patients (26%), isolated patch angioplasty in 13 patients (11%), and others (saphenous bypass, carotid eversion, resection-anastomosis) in 12 patients (11%). Macroscopic examination of the plaque revealed myointimal hyperplasia in 45 patients (38%) and atherosclerosis in the other cases.
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Fig. (a) Actuarial plots of freedom from restenosis, (b) freedom from reintervention, (c) freedom from neurologic events and (d) survival after open surgery for carotid restenosis.
Postoperative complications. One patient (0.8%) died during the 30-day perioperative period (Table III). This death was secondary to an immediate severe postoperative ipsilateral ischemic stroke in an 85-year-old female who underwent a prosthetic bypass graft for a symptomatic RCS. The mechanism of this event remains poorly understood because good reflux was noted intraoperatively (clamping time ⬍30 minutes) and postoperative angiography did not demonstrate any clear anomaly of brain perfusion. Nonfatal stroke occurred in 3 cases (2.5%). All were ischemic and ipsilateral to the operated carotid artery (Rankin score: 3, 3 and 4, respectively). Three patients (2.5%) experienced a TIA. One additional patient suffered a nonfatal postoperative myocardial infarction. Consequently, the rate of combined perioperative mortality and stroke morbidity (CMSM) is 3.3% for our series. Local operative morbidity consisted in 5 cases (4.2%) of CNI including recurrent laryngeal nerve palsy in 2 cases, hypoglossal nerve injury in 2 cases, and facial nerve injury in 1 case. All but 1 had completely recovered 1 year after the intervention. One patient (0.8%) with wound hematoma
necessitated an emergent surgical drainage. All but one (0.8%) repaired ICA were patent on the predischarge duplex ultrasound scan. Two external carotids were occluded (1.7%). These 3 last patients did not suffer any neurologic symptoms. Follow-up. With a mean follow-up of 53 ⫾ 48 months (range, 1-204), 39 patients were lost and 25 patients expired (Table IV and Fig). Two patients experienced ipsilateral ischemic stroke at 14 and 24 months. The first one was related to an ipsilateral carotid occlusion and the second presented with a 40% tertiary RCS. Other complications were one ipsilateral hemorrhagic stroke at 2 months, and one contralateral ischemic stroke at 70 months. Recurrent occlusive disease was found in 7 patients: 5 patients were noted to have a 50% to 80% tertiary RCS at 6, 39, 41, 49, and 73 months, 1 patient was discovered to have a 90% tertiary RCS at 78 months, and 1 patient was found to have an asymptomatic total occlusion of the ICA at 132 months. From those, 2 patients were given tertiary open surgery for RCS. One was for a severe asymptomatic 90% RCS and the second was indicated for
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Table V. Early and long-term results of consequent series (⬎30 vessels) reporting on open surgery for recurrent carotid stenosis Early results (⬍30 days)
Author
Period 16
Long-term results
No. Nonfatal patients stroke Death CMSM CNI (carotids) % % % %
Stoney et al Das et al17 Piepgras et al18 Bartlett et al19 Treiman et al20
1957-1975 29 (32) 1979-1983 61 (65) 1972-1984 51 (57) 1957-1985 94 (103) 1974-1991 162 (162)
0 1.5 10.5 1.9 2.5
3.1 3.1 0 1.9 1.2
3.1 4.6 10.5 3.8 3.7
Gagne et al21 Meyer et al22 AbuRahma et al23 Coyle et al24 Raithel25 O’Donnell et al26 Ballinger et al27 Mansour et al28 Rockman et al29 Hill et al30 Gorlitzer et al31 Archie Jr32 O’Hara et al12 AbuRahma et al33 Abou-Zamzam et al34 Cho et al35 Rockman et al36 Stoner et al13
1970-1991 1972-1992
42 (47) 82 (92)
0 5.4
0 4.3
0 9.7
1988-1993 1983-1992 NS
42 (46) 69 (69) 64 (66)
7 1.4 3.1
0 2.9 0
7 4.3 3.1
6.5 0 4.7
1983-1994 44 (48) 1984-1995 67 (74) 1976-1996 69 (82) 1980-1996 74 (82) 1993-1998 40 (40) 1992-1998 41 (42) 1981-1999 66 (69) 1989-1999 199 (206)
2.1 1.4 4.8 3.7 0 2.4 2.9 3.4
2.1 1.4 0 0 0 0 0 1
4.2 2.8 4.8 3.7 0 2.4 2.9 4.4
1996-2000
3.4
0
3.4
1990-2000 56 (56) 1990-2000 64 (66) 1992-2002 89 (89) 1989-2000 145 (153)
3.6 3 5.6 1.9
1.8 0 0 0
5.4 3 5.6 1.9
1.8 6 7.9 1.3
Mehta et al37 Jain et al38 De Borst et al39 Attigah et al40 Present series
1981-2002 59 (59) 1988-2005 80 (83) 1985-2006 72 (73) 1989-2007 NS (41) 1989-2006 119 (119)
1.7 0 0 4.9 2.5
0 1.2 0 0 0.8
1.7 1.2 0 4.9 3.3
3.4 7.2 1.4 0 4.2
58 (58)
Follow-up (months)
NS NS 10.8 23 NS NS 19.4 NS 2.4 35 (bypass) 64 (redo CAE) 4.5 54 NS NS
Neurologic Tertiary Carotid Tertiary event RCS occlusion CAE % % % % 3.6 5.1 NS NS 3.7 26 9.8 NS
3.6 NS NS NS 9.3 21.9 4.5 NS
0 NS NS NS 5.6 1 9 NS
3.6 NS NS NS 0 19 7 NS
30.9 57 NS
2.5 1.8 NS
11 NS NS
0 NS NS
2.5 NS NS
18.9 15.7 7.3 1.2 7.2 14.3 4.3 1
NS 48.2 NS 35 14 NS 50 51.6
NS 10.9 NS 5.4 0 NS 6.1 8.7
NS NS 6.1 4.9 10 NS 13 5/7/3*
NS NS NS 6.1 2.5 NS 0 6
NS NS NS 5.4 2.6 NS 4.5 NS
17
22.1
NS
0
0
0
29 51.6 34.6 52.8 45 (redo CAE) 19 (eversion) 50.9 52 70.3 53
1.8 8 NS NS
3.7 8 6.3 9.1
1.9 1.6 1 1.3
3.6 0 8 NS
0 4.6 4.3 0 8.5
3.4 NS 13.7 NS 5.0
0 1.2 0 NS 2.5
1.7 9.6 7.1 9.7 1.7
CMSM, Combined operative mortality and stroke morbidity; CNI, cranial nerve injury; RCS, recurrent carotid stenosis ⬎50%; CAE, carotid artery endarterectomy; NS, not stated. Neurologic events includes both transient ischemic attack and stroke. *Percentage of patients presenting with a 40% to 59%, a 60% to 79% and an 80% to 99% tertiary RCS, respectively.
a symptomatic (ipsilateral TIA) 50% tertiary RCS. This last patient was the only one to experience a TIA during follow-up. The main late complications are summarized in Table IV. At 5 years, estimated rates of freedom from tertiary RCS ⬎50%, freedom from reintervention, freedom from any neurologic event, and survival were 91%, 99%, 89%, and 91%, respectively. KM curves are presented in Fig, a-d. DISCUSSION The long-term results observed in this large series assess the durability of OS in the treatment of RCS, and contrast with the absence of long-term data regarding CAS for RCS. For the last 30 years, CAE has become a widely used procedure in preventing stroke. At the same time, improvement of noninvasive imaging techniques (duplex ultrasound scan, CT, and MRI) has allowed a better detection of
RCS after primary CAE. Studies regarding primary CAE found a wide range in RCS incidence, depending on the surgical technique (use of patch angioplasty or primary closure), the method used for detection, the definition of RCS, and the length of follow-up.5 Although the incidence of RCS is not clearly known, the proportion of procedures performed for RCS is between 1% and 10% (2.8% in our department) of open carotid procedures.12,13,16-40 However, RCS seems to become a more common indication for CAS, as demonstrated in the recent publication of the Society for Vascular Surgery (SVS) vascular registry data: the treatment of an RCS accounted for 1.2% of 3259 open surgical carotid procedures vs 22.3% of 2763 CAS procedures between 2005 and 2007.41 This finding suggests the acceptance of CAS as first-line therapy for RCS by many surgeons despite the lack of supporting evidence.
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Coscas et al 1129
Table VI. Early and long-term results of consequent series (⬎30 vessels) reporting on transluminal angioplasty with or without stenting for recurrent carotid stenosis Early results (⬍30 days)
Author
Period 10
New et al Vitek et al49 Bowser et al50 Mc Donnell et al51 De Borst et al52 Bettendorf et al53 Kadhkhodayan et al54 Cuadra et al55 Mehta et al11 Aburahma et al56 Attigah et al40 Vos et al57
No. patients (carotids)
Long-term results
Nonfatal Neurologic Tertiary Carotid Tertiary stroke Deaths CMSM CNI Follow-up events RCS occlusion intervention % % % % (months) % % % %
1998-NS 338 (358) NS 99 (110) 1997-2002 50 (52)
2.5 3 2
1.2 1 2
3.7 4 4
0 0 0
14 20 22
0 0 2
6.0 NS 16
0 NS 0
2.6 NS 8
1994-2001
25 (30)
0
3
3
0
20
0
10**
0
10
1998-2004
55 (57)
0
0
0
0
36
3.6
19
1.7
11.4
2002-2006
33 (45)
3
0
3
0
10
0
6.1*
0
NS
1996-2005 75 (83) 1996-2006 NS (118) 1996-2006 223 (NS)
3.6 2.5 1.4
0 2.5 0
3.6 5.1 1.4
0 0 0
22.4 NS NS
6 NS NS
4.8 NS NS
0 NS NS
0 NS NS
2001-2008 112 (112) 1989-2007 NS (45) 1997-2006 72 (72)
0.9 0 0
0 0 0
0.9 0 0
0 0 0
25 24.8 NS
1.8 0 NS
15 NS NS
0 NS NS
3.6 2.2 NS
CMSM, Combined operative mortality and stoke morbidity; CNI, cranial nerve injury; RCS, recurrent carotid stenosis ⬎50%; CAE, carotid artery endarterectomy; Neurologic events includes both transient ischemic attack and stroke. NS, not stated. *RCS ⬎80%. **RCS ⬎90%.
The reasons why some patients develop RCS whereas most do not remains poorly understood. Although tobacco use,42 female gender43 and hyperlipidemia44 were considered to be associated with RCS, these findings are controversial45 and the natural history of RCS remains poorly known. Some controversies exist about the risk of ipsilateral stroke in the setting of an RCS.46,47 However, most authors recommend treatment of lesions at high risk for stroke, such as ⬎50% stenosis for symptomatic RCS and ⬎80% stenosis for asymptomatic RCS, and this was our approach to the patients reported in this study. Although these recommendations are similar to those for primary CAE, the upper limit of acceptable stroke/death rate for OS in the management of RCS has been defined to be lower than 10%.48 In fact, all published series since 1995 have reported rates of CMSM between 0% and 5.6% and our early results are consistent with those previously reported (Table V).12,13,16-40 The surgical approach to RCS is reputed to be challenging. However, in our series, 103 (87%) of the 119 cases were defined as “simple” by the senior surgeon and did not require any technical adaptation in comparison to a primary approach. In our practice, the surgical approach to an RCS was not as technically demanding as surgeons supporting CAS argue. Should care be taken to first control the carotid in nonpreviously dissected areas, the rest of the procedure does not carry any major technical difficulty. Moreover, primary CAE is a commonly performed procedure with which all vascular surgeons are familiar. Our rate of CNI after OS for RCS is 4.2%, which is consistent with other reports (Table V).12,13,16-40 Al-
though CAS eliminates the risk of CNI, it must be emphasized that CNI are usually temporary as were all but one in this study. Regarding the rate of immediate neurologic and/or fatal complications, our results seem to be similar to those reported in previous series (Table V)12,13,16-40 but also to those published with CAS (Table VI).10,11,49-57 Indeed, apart from two series of OS with a CMSM of 10.5, and 9.7%, respectively, all reported rates of CMSM were between 0% and 6.3% regardless of the technique used (Tables V and VI). Few studies have focused on long-term durability of both techniques. However, this consideration is of particular importance because of the age and expected longevity of patients with RCS. To our knowledge, only two large recent studies (⬎100 cases) have reported long-term results for OS in RCS. O’Hara et al12 reported on a late neurologic event rate of 8.7% in 196 patients undergoing OS for RCS and followed for a mean of 4.3 years. More than half of the late neurologic events were TIAs. At last follow-up, 6% of the ipsilateral carotid arteries were found to be occluded, 3% had an 80% to 99% stenosis, 7% had a 60% to 79% stenosis, 5% had a 40% to 59% stenosis, 16% had a 20% to 39% stenosis, and 63% had a 0% to 19% stenosis. Reporting on their results of secondary CAE over 153 RCS (145 patients), Stoner et al13 found similar results with rates of stroke and ⬎50% tertiary RCS of 4% and 9.2%, respectively, at 4.4 years. However, in a study published in 1992, Treiman et al20 reported 23 tertiary RCS of ⬎50% in a series of 105 redo CAEs with 64-month follow-up. Our rate of tertiary RCS is 5.0% with a mean follow-up of 53
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months. A longer follow-up period could result in a higher rate of tertiary RCS. In contrast, the long-term results of CAS remain in question. No large series describing the long-term results of CAS has been published to date. At intermediate followup, rates of RCS seem relatively high, perhaps leading to even more challenging tertiary procedures. In the most important published series of CAS for RCS (358 cases), the rate of significant tertiary RCS ⬎50% was 6% at 6 months, which is similar to the rate observed in this series after 53 months of follow-up.10 Although the rate of tertiary RCS after CAS is acceptable at 6-month follow-up, it can be expected to increase with longer follow-up. Studies by AbuRahma33 and de Borst52 have shown tertiary RCS rates after CAS of 24% and 19% with mean follow-up periods of 18 and 36 months, respectively.32,52 In this single center report on OS for RCS, we were limited by the retrospective nature of the analysis and incomplete follow-up in an important proportion of patients. Moreover, although early results demonstrated stroke and mortality rates in the range of those usually reported for the treatment of primary carotid stenosis, it should be emphasized that our patients were not routinely examined by a neurologist during the postoperative period. Also, our team has extensive experience with open carotid procedures (⬎350/year). Our results may not be generalizable to lower volume centers. The lack of prospective randomized trial, the heterogeneity of reported data through the literature (Table V and VI) and the absence of standardized criteria for long-term success can only allow for tentative conclusions regarding the management of RCS. Clearly, late tertiary RCS is a concerning problem, more common after CAS, and follow-up paradigms should be defined as a function of the technique used to treat RCS. In perspective medical therapy, OS and CAS will improve their results in the following years. The generalization of the prescriptions of antiplatelet medications and statins,58 the refinement of perioperative protocols after OS, and the use of new CAS technical adjuncts like cerebral protection devices and drug-eluting stents59 will lead the vascular surgical community to undertake new evaluations in the future. CONCLUSION The results of this series support OS as a durable treatment for RCS. The low rates of both perioperative and long-term neurologic and anatomic complications observed after OS compare favorably with those reported for CAS and suggest that OS remains the preferred option for the treatment of severe RCS. The comparison between OS and CAS for RCS suffers from the absence of standardized follow-up paradigms after primary OS and the lack of a prospective randomized trial comparing the two techniques. Considering these findings and the age and expected longevity of patients presenting with RCS, OS remains the first line treatment for RCS in our center.
AUTHOR CONTRIBUTIONS Conception and design: RC, LC, FK Analysis and interpretation: RC, LC, FK Data collection: RC, BR, NG-C, TC, CdT Writing the article: RC, FK Critical revision of the article: RC, LC, FK Final approval of the article: RC, BR, NG-C, TC, CdT, LC, EK, FK Statistical analysis: RC, FK Obtained funding: Not applicable Overall responsibility: RC, FK REFERENCES 1. [No authors listed.] Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med 1991;325:445-53. 2. Barnett HJ, Taylor DW, Eliasziw M, Fox AJ, Ferguson GG, Haynes RB, et al. Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med 1998; 339:1415-25. 3. [No authors listed.] Endarterectomy for asymptomatic carotid artery stenosis. Executive Committee for the Asymptomatic Carotid Atherosclerosis Study. JAMA 1995;273:1421-8. 4. Halliday A, Mansfield A, Marro J, Peto C, Peto R, Potter J, et al. Prevention of disabling and fatal strokes by successful carotid endarterectomy in patients without recent neurological symptoms: randomised controlled trial. Lancet 2004;363:1491-502. 5. Lattimer CR, Burnand KG. Recurrent carotid stenosis after carotid endarterectomy. Br J Surg 1997;84:1206-19. 6. Mas JL, Chatellier G, Beyssen B, Branchereau A, Moulin T, Becquemin JP, et al. Endarterectomy versus stenting in patients with symptomatic severe carotid stenosis. N Engl J Med 2006;355:1660-71. 7. SPACE Collaborative Group, Ringleb PA, Allenberg J, Brückmann H, Eckstein HH, Fraedrich G, et al. 30 day results from the SPACE trial of stent-protected angioplasty versus carotid endarterectomy in symptomatic patients: a randomised non-inferiority trial. Lancet 2006;368:1239-47. 8. Mas JL, Trinquart L, Leys D, Albucher JF, Rousseau H, Viguier A, et al. Endarterectomy versus angioplasty in patients with symptomatic severe carotid stenosis (EVA-3S) trial: results up to 4 years from a randomised, multicentre trial. Lancet Neurol 2008;7:885-92. 9. Eckstein HH, Ringleb P, Allenberg JR, Berger J, Fraedrich G, Hacke W, et al. Results of the stent-protected angioplasty versus carotid endarterectomy (SPACE) study to treat symptomatic stenoses at 2 years: a multinational, prospective, randomised trial. Lancet Neurol 2008;7:893-902. 10. New G, Roubin GS, Iyer SS, Vitek JJ, Wholey MH, Diethrich EB, et al. Safety, efficacy, and durability of carotid artery stenting for restenosis following carotid endarterectomy: a multicenter study. J Endovasc Ther 2000;7:345-52. 11. Mehta RH, Zahn R, Hochadel M, Ischinger T, Jung J, Hauptmann KE, et al. Comparison of in-hospital outcomes of patients with versus without previous carotid endarterectomy undergoing carotid stenting (from the German ALKK CAS Registry). Am J Cardiol 2007;99:1288-93. 12. O’Hara PJ, Hertzer NR, Karafa MT, Mascha EJ, Krajewski LP, Beven EG. Reoperation for recurrent carotid stenosis: early results and late outcome in 199 patients. J Vasc Surg 2001;34:5-12. 13. Stoner MC, Cambria RP, Brewster DC, Juhola KL, Watkins MT, Kwolek CJ, et al. Safety and efficacy of reoperative carotid endarterectomy: a 14-year experience. J Vasc Surg 2005;41:942-9. 14. Autorité de Santé H. [Vascular prevention after cerebral infarct or transient ischemic attack. Recommendations. March 2008] [Article in French] Rev Neurol (Paris) 2008;164 Spec No 3:F229-34.
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15. Hobson RW 2nd, Mackey WC, Ascher E, Murad MH, Calligaro KD, Comerota AJ, et al. Management of atherosclerotic carotid artery disease: clinical practice guidelines of the Society for Vascular Surgery. J Vasc Surg 2008;48:480-6. 16. Stoney RJ, String ST. Recurrent carotid stenosis. Surgery 1976;80: 705-10. 17. Das MB, Hertzer NR, Ratliff NB, O’Hara PJ, Beven EG. Recurrent carotid stenosis. A five-year series of 65 reoperations. Ann Surg 1985; 202:28-35. 18. Piepgras DG, Sundt TM Jr, Marsh WR, Mussman LA, Fode NC. Recurrent carotid stenosis. Results and complications of 57 operations. Ann Surg 1986;203:205-13. 19. Bartlett FF, Rapp JH, Goldstone J, Ehrenfeld WK, Stoney RJ. Recurrent carotid stenosis: operative strategy and late results. J Vasc Surg 1987;5:452-6. 20. Treiman GS, Jenkins JM, Edwards WH Sr, Barlow W, Edwards WH Jr, Martin RS 3rd, Mulherin JK Jr. The evolving surgical management of recurrent carotid stenosis. J Vasc Surg 1992;16:354-62; discussion 362-3. 21. Gagne PJ, Riles TS, Jacobowitz GR, Lamparello PJ, Giangola G, Adelman MA, et al. Long-term follow-up of patients undergoing reoperation for recurrent carotid artery disease. J Vasc Surg 1993;18: 991-8; discussion 999-1001. 22. Meyer FB, Piepgras DG, Fode NC. Surgical treatment of recurrent carotid artery stenosis. J Neurosurg 1994;80:781-7. 23. AbuRahma AF, Snodgrass KR, Robinson PA, Wood DJ, Meek RB, Patton DJ. Safety and durability of redo carotid endarterectomy for recurrent carotid artery stenosis. Am J Surg 1994;168:175-8. 24. Coyle KA, Smith RB 3rd, Gray BC, Salam AA, Dodson TF, Chaikof EL, Lumsden AB. Treatment of recurrent cerebrovascular disease. Review of a 10-year experience. Ann Surg 1995;221:517-21; discussion 521-4. 25. Raithel D. Recurrent carotid disease: optimum technique for redo surgery. J Endovasc Surg 1996;3:69-75. 26. O’Donnell TF Jr, Rodriguez AA, Fortunato JE, Welch HJ, Mackey WC. Management of recurrent carotid stenosis: should asymptomatic lesions be treated surgically? J Vasc Surg 1996;24:207-12. 27. Ballinger BA, Money SR, Chatman DM, Bowen JC, Ochsner JL. Sites of recurrence and long-term results of redo surgery. Ann Surg 1997; 225:512-5; discussion 516-7. 28. Mansour MA, Kang SS, Baker WH, Watson WC, Littooy FN, Labropoulos N, Greisler HP. Carotid endarterectomy for recurrent stenosis. J Vasc Surg 1997;25:877-83. 29. Rockman CB, Riles TS, Landis R, Lamparello PJ, Giangola G, Adelman MA, Jacobowitz GR. Redo carotid surgery: an analysis of materials and configurations used in carotid reoperations and their influence on perioperative stroke and subsequent recurrent stenosis. J Vasc Surg 1999;29:72-80; discussion 80-1. 30. Hill BB, Olcott C 4th, Dalman RL, Harris EJ Jr, Zarins CK. Reoperation for carotid stenosis is as safe as primary carotid endarterectomy. J Vasc Surg 1999;30:26-35. 31. Gorlitzer M, Heine B, Mendel H, Günen E, Meinhart J, Sisel A, Deutsch M. Redo surgery for carotid artery stenosis: when and how? Cardiovasc Surg 2000;8:366-71. 32. Archie JP Jr. Reoperations for carotid artery stenosis: role of primary and secondary reconstructions. J Vasc Surg 2001;33:495-503. 33. AbuRahma AF, Bates MC, Stone PA, Wulu JT. Comparative study of operative treatment and percutaneous transluminal angioplasty/stenting for recurrent carotid disease. J Vasc Surg 2001;34:831-8. 34. Abou-Zamzam AM Jr, Moneta GL, Landry GJ, Yeager RA, Edwards JM, McConnell DB, et al. Carotid surgery following previous carotid endarterectomy is safe and effective. Vasc Endovascular Surg 2002;36: 263-70. 35. Cho JS, Pandurangi K, Conrad MF, Shepard AS, Carr JA, Nypaver TJ, Reddy DJ. Safety and durability of redo carotid operation: an 11-year experience. J Vasc Surg 2004;39:155-61. 36. Rockman CB, Bajakian D, Jacobowitz GR, Maldonado T, Greenwald U, Nalbandian MM, et al. Impact of carotid artery angioplasty and stenting on management of recurrent carotid artery stenosis. Ann Vasc Surg 2004;18:151-7.
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37. Mehta M, Roddy SP, Darling RC 3rd, Paty PS, Kreienberg PB, Ozsvath KJ, et al. Safety and efficacy of eversion carotid endarterectomy for the treatment of recurrent stenosis: 20-year experience. Ann Vasc Surg 2005;19:492-8. 38. Jain S, Jain KM, Kumar SD, Munn JS, Rummel MC. Operative intervention for carotid restenosis is safe and effective. Eur J Vasc Endovasc Surg 2007;34:561-8. 39. de Borst GJ, Zanen P, de Vries JP, van de Pavoordt ED, Ackerstaff RG, Moll FL. Durability of surgery for restenosis after carotid endarterectomy. J Vasc Surg 2008;47:363-71. 40. Attigah N, Külkens S, Deyle C, Ringleb P, Hartmann M, Geisbüsch P, Böckler D. Redo surgery or carotid stenting for restenosis after carotid endarterectomy: results of two different treatment strategies. Ann Vasc Surg 2009 [Epub ahead of print]. 41. Sidawy AN, Zwolak RM, White RA, Siami FS, Schermerhorn ML, Sicard GA; Outcomes Committee for the Society for Vascular Surgery. Risk-adjusted 30-day outcomes of carotid stenting and endarterectomy: results from the SVS Vascular Registry. J Vasc Surg 2009;49:71-9. 42. Clagett GP, Rich NM, McDonald PT, Salander JM, Youkey JR, Olson DW, Hutton JE Jr. Etiologic factors for recurrent carotid artery stenosis. Surgery 1983;93:313-8. 43. Ouriel K, Green RM. Clinical and technical factors influencing recurrent carotid stenosis and occlusion after endarterectomy. J Vasc Surg 1987;5:702-6. 44. Rapp JH, Qvarfordt P, Krupski WC, Ehrenfeld WK, Stoney RJ. Hypercholesterolemia and early restenosis after carotid endarterectomy. Surgery 1987;101:277-82. 45. Atnip RG, Wengrovitz M, Gifford RR, Neumyer MM, Thiele BL. A rational approach to recurrent carotid stenosis. J Vasc Surg 1990;11: 511-6. 46. 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;29:244-50. 47. Ricotta JJ, O’Brien-Irr MS. Conservative management of residual and recurrent lesions after carotid endarterectomy: long-term results. J Vasc Surg 1997;26:963-70; discussion 970-2. 48. Beebe HG, Clagett GP, DeWeese JA, Moore WS, Robertson JT, Sandok B, Wolf PA. Assessing risk associated with carotid endarterectomy. A statement for health professionals by an Ad Hoc Committee on Carotid Surgery Standards of the Stroke Council, American Heart Association. Circulation 1989;79:472-3. 49. Vitek JJ, Roubin GS, New G, Al-Mubarek N, Iyer SS. Carotid angioplasty with stenting in post-carotid endarterectomy restenosis. J Invasive Cardiol 2001;13:123-5; discussion 158-70. 50. Bowser AN, Bandyk DF, Evans A, Novotney M, Leo F, Back MR, et al. Outcome of carotid stent-assisted angioplasty versus open surgical repair of recurrent carotid stenosis. J Vasc Surg 2003;38:432-8. 51. McDonnell CO, Legge D, Twomey E, Kavanagh EG, Dundon S, O’Donohoe MK, et al. Carotid artery angioplasty for restenosis following endarterectomy. Eur J Vasc Endovasc Surg 2004;27:163-6. 52. de Borst GJ, Ackerstaff RG, de Vries JP, vd Pavoordt ED, Vos JA, Overtoom TT, Moll FL. Carotid angioplasty and stenting for postendarterectomy stenosis: long-term follow-up. J Vasc Surg 2007;45: 118-23. 53. Bettendorf MJ, Mansour MA, Davis AT, Sugiyama GT, Cali RF, Gorsuch JM, Cuff RF. Carotid angioplasty and stenting versus redo endarterectomy for recurrent stenosis. Am J Surg 2007;193:356-9; discussion 359. 54. Kadkhodayan Y, Moran CJ, Derdeyn CP, Cross DT 3rd. Carotid angioplasty and stent placement for restenosis after endarterectomy. Neuroradiology 2007;49:357-64. 55. Cuadra S, Hobson RW, Lal BK, Goldstein J, Chakhtoura E, Jamil Z. Outcome of carotid artery stenting for primary versus restenotic lesions. Ann Vasc Surg 2009;23:330-4. 56. AbuRahma AF, Abu-Halimah S, Bensenhaver J, Nanjundappa A, Stone PA, Dean LS, et al. Primary carotid artery stenting versus carotid artery stenting for postcarotid endarterectomy stenosis. J Vasc Surg 2009;50: 1031-9. 57. Vos JA, de Borst GJ, Overtoom TT, de Vries JP, van de Pavoordt ED, Zanen P, et al. Carotid angioplasty and stenting: treatment of postca-
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rotid endarterectomy restenosis is at least as safe as primary stenosis treatment. J Vasc Surg 2009;50:755-61.e1. 58. LaMuraglia GM, Stoner MC, Brewster DC, Watkins MT, Juhola KL, Kwolek C, et al. Determinants of carotid endarterectomy anatomic durability: effects of serum lipids and lipid-lowering drugs. J Vasc Surg 2005;41:762-8.
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59. Gupta R, Al-Ali F, Thomas AJ, Horowitz MB, Barrow T, Vora NA, et al. Safety, feasibility, and short-term follow-up of drug-eluting stent placement in the intracranial and extracranial circulation. Stroke 2006; 37:2562-6. Submitted Jul 17, 2009; accepted Dec 4, 2009.
Carotid artery endarterectomy (CAE) has been demonstrated to be the best option to prevent stroke for patients with high-grade symptomatic1,2 or asymptomatic3,4 carotid stenosis. Despite excellent immediate results, recurrent carotid stenosis (RCS) remains a concern whose incidence is dependent upon the surgical technique, the method of imaging utilized for surveillance, the definition of RCS, and the length of follow-up.5 A controversy remains regarding the choice between open surgery (OS) and transluminal carotid angioplasty with stenting (CAS) for the treatment of primary carotid stenosis. Although early results of the stent-protected angioplasty vs carotid endarterectomy (SPACE) trial and the Endarterectomy versus Angioplasty in Patients with Symptomatic Severe Carotid Stenosis (EVA-3S) trial were in favor of OS for the treatment of symptomatic cases,6,7 intermediate-term results of these two prospective randomized trials demonstrated similar clinical outcomes for both techniques.8,9 In the EVA-3S trial, one main reason for the From the Department of Vascular Surgery, Hôpital Pitié-Salpêtrière. Reprint requests: Raphaël Coscas, MD, 106, rue de la glacière, 75013 Paris, France (e-mail: [email protected]). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a competition of interest. 0741-5214/$36.00 Copyright © 2010 by the Society for Vascular Surgery. doi:10.1016/j.jvs.2009.12.020
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difference observed during the early postoperative period was a low rate of complications after primary CAE in specialized centers.6 Therefore, it has been suggested that CAS could provide a significant advantage in situations where OS provides its worst results. The treatment of RCS has been considered to be a high-risk procedure. The dissection of the carotid artery in a previously operated field would be expected to carry a higher risk of local complications such as cranial nerve injury (CNI) and wound hematoma. Difficulties in controlling the carotid artery could increase the risk of cerebral emboli. Using a puncture distant from the site of the RCS, CAS has been suggested to be an interesting alternative in these situations. Despite the lack of prospective comparative trials, its early results seemed to compare favorably with OS in the management of RCS.10,11 However, several authors emphasize that the surgical approach to RCS may not be technically demanding and historic series reporting on OS to treat RCS have concluded that this procedure provides early results comparable to those reported with primary CAE.12,13 Long-term results of both techniques have not been well studied. The durability of CAS for RCS is poorly known, whereas only two recent large series (⬎100 patients) reported on late results of OS.12,13 These considerations are paramount because patients with RCS are often in their seventh or eighth decades and may be expected to
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live for 5 years or more after reintervention. Recommendations of public authorities and vascular societies regarding management of RCS could not conclude whether CAS or OS was the most appropriate treatment for menacing RCS because of the absence of comparative trials and the lack of long-term follow-up data.14,15 The aim of this study is to report our results with OS in the management of RCS, focusing on long-term outcomes. MATERIALS AND METHODS Data collection and patient selection. From January 1989 to December 2006, perioperative data of 4245 consecutive carotid reconstructions performed in our department were prospectively collected in a database. Patients whose intervention was a redo procedure were identified and only cases whose indication was RCS were selected and subjected to further analysis. Patients who underwent another concomitant vascular repair at the time of the RCS repair were excluded. Repairs of intrathoracic supra-aortic trunks were excluded, as were aneurysmal degenerations of previous endarterectomy patches. Surgical management. All patients referred for the management of RCS underwent confirmation of the recurrence using two different imaging methods including a duplex ultrasound scan in all cases associated with a non-operatordependent method (CT scan, MRI, and/or carotid angiography). Surgery was indicated for patients with symptomatic stenosis ⬎50% and high-grade asymptomatic stenosis ⬎80% (North American Symptomatic Carotid Endarterectomy Trial [NASCET] criteria). Patients presenting with intracranial stenosis that exceeded the severity of the extracranial stenosis, severe disability from stroke, short life expectancy, or inability to give informed consent were not offered surgery. Interventions for RCS were performed under general anesthesia by a senior surgeon (L.C., E.K., F.K.). The surgical approach always consisted of a redo anterior cervicotomy along the sternocleidomastoid muscle, as for a primary intervention. Technically, we usually preferred to first control the common carotid artery (CCA) and the internal carotid artery (ICA) in nondissected portions, and then to dissect the carotid bulb after clamping. After identification and control of the main carotid vessels, a systemic bolus of 0.5 mg/kg of unfractioned heparin was administered intravenously before clamping. Occlusion of the external carotid artery was frequently obtained through the inflation of a 5F intravascular Fogarty catheter (Edwards Lifesciences Corporation, Irvine, Calif). Selective shunting was used in the presence of preoperative severe stenosis and/or occlusion of other major cerebral vessels (contralateral carotid artery, vertebral arteries) or intraoperative finding of nonpulsatile reflux from the distal ICA. Carotid artery reconstruction depended on the severity and extent of the lesion and was adapted to each case at the discretion of the vascular surgeon. Preference was given to the simplest procedure. Dacron patch (Hemacarotid Patch; Intervascular Datascope, La Ciotat, France) angioplasty with or without intimectomy was used whenever it was possible. In
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cases of obvious smooth plaque suggesting myointimal hyperplasia, intimectomy was not performed and a simple patch angioplasty was performed. When the extent of the lesion rendered the use of a bypass mandatory, a prosthetic polytetrafluoroethylene graft (Thin-walled tubular graft; GoreTex, Flagstaff, Ariz) was used, except in the presence of a distal ICA with reduced diameter (⬍3.5 mm) where a saphenous vein graft was used. At the end of the procedure, selective angiography was performed to assess the patency of the repair. Postoperatively, all patients returned to a conventional hospital ward and were generally discharged at day 3-4 in the absence of any complication. Unless contraindicated, an oral antiplatelet agent (aspirin 75-250 mg daily or clopidogrel 75 mg daily) was administered to all patients before surgery and life-long. Follow-up. Duplex ultrasound scan was performed at 1 month, 6 months, 12 months, and yearly in the absence of a neurologic event and/or duplex scan anomaly. Data regarding long-term survival, neurologic state, and anatomic lesions of the ipsilateral carotid were retrospectively collected using medical charts and/or direct contact with the patient (or his relatives in case of death) by phone call. Freedom from neurologic event was defined as the absence of any ipsilateral neurologic event (transient ischemic attack and minor stroke included) after the procedure. Freedom from restenosis was defined as the absence of tertiary stenosis ⬎50% (NASCET criteria) or occlusion of the ipsilateral carotid artery on duplex ultrasound scan examination during follow-up. Statistical analysis. Demographic and periprocedural characteristics are shown as number (%) or mean ⫾ SD. Kaplan-Meier (KM) analysis was conducted to estimate survival, freedom from restenosis, neurologic event, and reintervention. The Statistical Package for the Social Sciences (SPSS) software version 13.0 (SPSS Inc, Chicago, Ill) was used for the statistical analysis. RESULTS One hundred nineteen consecutive patients operated on for RCS were subjected to further analysis. This subset represents 2.8% of the 4245 carotid reconstructions performed in our department during the same period. All were managed using OS and we never used CAS for RCS during this period. Demographics. Ninety-two patients (77%) were male and the mean age at reintervention was 69.6 ⫾ 8.9 years (range, 45-86). Cardiovascular risk factors were mainly a history of tobacco use in 69% and hypertension in 68% (Table I). Several patients presented with multifocal atherosclerosis including coronary artery disease (any symptom of heart ischemia, antecedent of coronary revascularization, and/or positive stress test) in 33%, and peripheral arterial disease (any peripheral arterial symptoms resulting from occlusive disease and/or antecedent of limb revascularization) in 22%. Thirty-four patients (29%) had a history of vascular surgery including aortoiliac repair in 18 (12 for aneurysm and 6 for occlusive disease), lower limb revascu-
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Table I. Preoperative clinical data of 119 patients who underwent an open surgery for recurrent carotid stenosis in our department (1989-2006)
Table III. Early postoperative complications (⬍30 days) in 119 patients who underwent an open surgery for recurrent carotid stenosis in our department (1989-2006)
Preoperative clinical data
Early postoperative complications (⬍30 days)
No. (%)
Deaths Including: Stroke Nonfatal neurologic complications Including: Stroke Transient ischemic attack Extra neurologic systemic complications Including: Myocardial infarction Local complications Including: Hematoma evacuation Cranial nerve injury
1 (0.8)
General Total population Age (years) Time from primary CAE (months) Male Left side Indication Symptomatic Including: TIA Stroke Asymptomatic Cardiovascular risk factors Tobacco use Hypertension Dyslipidemia Diabetes Chronic renal insufficiency Cardiovascular diseases Coronaropathy artery disease Including: myocardial infarction Peripheral arterial disease Previous arterial repair Aortoiliac* Lower limb CABG Renal artery Superior mesenteric artery
No. (%) 119 (100) 69.6 ⫾ 8.9 59.4 ⫾ 54.5 92 (77) 67 (56) 49 (41) 29 (24) 20 (17) 70 (59) 82 (69) 81 (68) 70 (59) 19 (16) 12 (10) 39 (33) 15 (13) 26 (22) 18 (15) 16 (13) 15 (13) 3 (3) 2 (2)
CAE, Carotid artery endarterectomy; TIA, transient ischemic attack; CABG, aorto-coronary bypass graft. *Including, 12 aneurysms and 6 occlusive disease.
Table II. Intraoperative technical adaptations used in our series Intraoperative technical adaptations Division of the occipital artery Division of the posterior belly of the digastric muscle Mobilization of the hypoglossal nerve Division of the stylohyoid muscles No technical adaptation
1 (0.8) 5 (4.2) 2 (1.7) 3 (2.5) 1 (0.8) 1 (0.8) 6 (5.0) 1 (0.8) 5 (4.2)
Table IV. Late complications (⬎30 days after the procedure) in 118 patients who survived the intervention after a mean follow-up of 53 ⫾ 48 months Late complications (⬎30 days)
No. (%)
Ipsilateral stroke Including: Ischemic Hemorrhagic Transient ischemic attack Recurrent occlusive disease Including: 50% to 80% stenosis 80% to 99% stenosis Ipsilateral carotid occlusion Tertiary intervention
3 (2.5) 2 (1.7) 1 (0.8) 1 (0.8) 7 (5.9) 5 (4.2) 1 (0.8) 2 (1.7)* 2 (1.7)
*Including one asymptomatic occlusion discovered during the immediate post-operative period.
N (%) 9 (8) 5 (4) 3 (3) 2 (2) 103 (87)
larization in 16, coronary bypass in 15, renal revascularization in 3, and superior mesenteric artery revascularization in 2 cases. The primary carotid intervention was an endarterectomy with patch suture in 56 patients (47%), an endarterectomy with direct suture in 41 patients (34%), a carotid bypass in 12 patients (10%), and an eversion in 10 patients (8%). The RCS was located on the left carotid in 67 cases (56%). The average time from the primary CAE to the intervention for RCS was 59.4 ⫾ 54.5 months (range, 2-204). Forty-nine patients (41%) were symptomatic. The main symptom was a transient ischemic attack (TIA) in 29 cases (including 8 amaurosis fugax) and a recent (⬍3 months) cerebral infarction with or without superimposed TIA in 20 cases. The remaining 70 asymptomatic patients
presented with high-grade RCS ⬎80% and/or rapidly progressive RCS on duplex ultrasound scan study. All patients underwent preoperative duplex ultrasound scan, and the second imaging method was a CT scan in 24 cases (20%), an MRI in 20 cases (17%), and an angiography in 75 cases (63%). Of note, no complication of carotid angiography was noted in this series. Surgical management. We always used an anterior approach along the sternocleidomastoid muscle and never used a retrojugular approach. In 103 patients (87%), the approach was defined as “simple” by the senior surgeon and did not necessitate any technical adaptation when compared to a primary approach. In the remaining 16 cases (13%), several technical modifications were used and are summarized in Table II. Intimectomy with patch angioplasty was used in 63 patients (53%) whereas prosthetic bypass graft was used in 31 patients (26%), isolated patch angioplasty in 13 patients (11%), and others (saphenous bypass, carotid eversion, resection-anastomosis) in 12 patients (11%). Macroscopic examination of the plaque revealed myointimal hyperplasia in 45 patients (38%) and atherosclerosis in the other cases.
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Fig. (a) Actuarial plots of freedom from restenosis, (b) freedom from reintervention, (c) freedom from neurologic events and (d) survival after open surgery for carotid restenosis.
Postoperative complications. One patient (0.8%) died during the 30-day perioperative period (Table III). This death was secondary to an immediate severe postoperative ipsilateral ischemic stroke in an 85-year-old female who underwent a prosthetic bypass graft for a symptomatic RCS. The mechanism of this event remains poorly understood because good reflux was noted intraoperatively (clamping time ⬍30 minutes) and postoperative angiography did not demonstrate any clear anomaly of brain perfusion. Nonfatal stroke occurred in 3 cases (2.5%). All were ischemic and ipsilateral to the operated carotid artery (Rankin score: 3, 3 and 4, respectively). Three patients (2.5%) experienced a TIA. One additional patient suffered a nonfatal postoperative myocardial infarction. Consequently, the rate of combined perioperative mortality and stroke morbidity (CMSM) is 3.3% for our series. Local operative morbidity consisted in 5 cases (4.2%) of CNI including recurrent laryngeal nerve palsy in 2 cases, hypoglossal nerve injury in 2 cases, and facial nerve injury in 1 case. All but 1 had completely recovered 1 year after the intervention. One patient (0.8%) with wound hematoma
necessitated an emergent surgical drainage. All but one (0.8%) repaired ICA were patent on the predischarge duplex ultrasound scan. Two external carotids were occluded (1.7%). These 3 last patients did not suffer any neurologic symptoms. Follow-up. With a mean follow-up of 53 ⫾ 48 months (range, 1-204), 39 patients were lost and 25 patients expired (Table IV and Fig). Two patients experienced ipsilateral ischemic stroke at 14 and 24 months. The first one was related to an ipsilateral carotid occlusion and the second presented with a 40% tertiary RCS. Other complications were one ipsilateral hemorrhagic stroke at 2 months, and one contralateral ischemic stroke at 70 months. Recurrent occlusive disease was found in 7 patients: 5 patients were noted to have a 50% to 80% tertiary RCS at 6, 39, 41, 49, and 73 months, 1 patient was discovered to have a 90% tertiary RCS at 78 months, and 1 patient was found to have an asymptomatic total occlusion of the ICA at 132 months. From those, 2 patients were given tertiary open surgery for RCS. One was for a severe asymptomatic 90% RCS and the second was indicated for
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Table V. Early and long-term results of consequent series (⬎30 vessels) reporting on open surgery for recurrent carotid stenosis Early results (⬍30 days)
Author
Period 16
Long-term results
No. Nonfatal patients stroke Death CMSM CNI (carotids) % % % %
Stoney et al Das et al17 Piepgras et al18 Bartlett et al19 Treiman et al20
1957-1975 29 (32) 1979-1983 61 (65) 1972-1984 51 (57) 1957-1985 94 (103) 1974-1991 162 (162)
0 1.5 10.5 1.9 2.5
3.1 3.1 0 1.9 1.2
3.1 4.6 10.5 3.8 3.7
Gagne et al21 Meyer et al22 AbuRahma et al23 Coyle et al24 Raithel25 O’Donnell et al26 Ballinger et al27 Mansour et al28 Rockman et al29 Hill et al30 Gorlitzer et al31 Archie Jr32 O’Hara et al12 AbuRahma et al33 Abou-Zamzam et al34 Cho et al35 Rockman et al36 Stoner et al13
1970-1991 1972-1992
42 (47) 82 (92)
0 5.4
0 4.3
0 9.7
1988-1993 1983-1992 NS
42 (46) 69 (69) 64 (66)
7 1.4 3.1
0 2.9 0
7 4.3 3.1
6.5 0 4.7
1983-1994 44 (48) 1984-1995 67 (74) 1976-1996 69 (82) 1980-1996 74 (82) 1993-1998 40 (40) 1992-1998 41 (42) 1981-1999 66 (69) 1989-1999 199 (206)
2.1 1.4 4.8 3.7 0 2.4 2.9 3.4
2.1 1.4 0 0 0 0 0 1
4.2 2.8 4.8 3.7 0 2.4 2.9 4.4
1996-2000
3.4
0
3.4
1990-2000 56 (56) 1990-2000 64 (66) 1992-2002 89 (89) 1989-2000 145 (153)
3.6 3 5.6 1.9
1.8 0 0 0
5.4 3 5.6 1.9
1.8 6 7.9 1.3
Mehta et al37 Jain et al38 De Borst et al39 Attigah et al40 Present series
1981-2002 59 (59) 1988-2005 80 (83) 1985-2006 72 (73) 1989-2007 NS (41) 1989-2006 119 (119)
1.7 0 0 4.9 2.5
0 1.2 0 0 0.8
1.7 1.2 0 4.9 3.3
3.4 7.2 1.4 0 4.2
58 (58)
Follow-up (months)
NS NS 10.8 23 NS NS 19.4 NS 2.4 35 (bypass) 64 (redo CAE) 4.5 54 NS NS
Neurologic Tertiary Carotid Tertiary event RCS occlusion CAE % % % % 3.6 5.1 NS NS 3.7 26 9.8 NS
3.6 NS NS NS 9.3 21.9 4.5 NS
0 NS NS NS 5.6 1 9 NS
3.6 NS NS NS 0 19 7 NS
30.9 57 NS
2.5 1.8 NS
11 NS NS
0 NS NS
2.5 NS NS
18.9 15.7 7.3 1.2 7.2 14.3 4.3 1
NS 48.2 NS 35 14 NS 50 51.6
NS 10.9 NS 5.4 0 NS 6.1 8.7
NS NS 6.1 4.9 10 NS 13 5/7/3*
NS NS NS 6.1 2.5 NS 0 6
NS NS NS 5.4 2.6 NS 4.5 NS
17
22.1
NS
0
0
0
29 51.6 34.6 52.8 45 (redo CAE) 19 (eversion) 50.9 52 70.3 53
1.8 8 NS NS
3.7 8 6.3 9.1
1.9 1.6 1 1.3
3.6 0 8 NS
0 4.6 4.3 0 8.5
3.4 NS 13.7 NS 5.0
0 1.2 0 NS 2.5
1.7 9.6 7.1 9.7 1.7
CMSM, Combined operative mortality and stroke morbidity; CNI, cranial nerve injury; RCS, recurrent carotid stenosis ⬎50%; CAE, carotid artery endarterectomy; NS, not stated. Neurologic events includes both transient ischemic attack and stroke. *Percentage of patients presenting with a 40% to 59%, a 60% to 79% and an 80% to 99% tertiary RCS, respectively.
a symptomatic (ipsilateral TIA) 50% tertiary RCS. This last patient was the only one to experience a TIA during follow-up. The main late complications are summarized in Table IV. At 5 years, estimated rates of freedom from tertiary RCS ⬎50%, freedom from reintervention, freedom from any neurologic event, and survival were 91%, 99%, 89%, and 91%, respectively. KM curves are presented in Fig, a-d. DISCUSSION The long-term results observed in this large series assess the durability of OS in the treatment of RCS, and contrast with the absence of long-term data regarding CAS for RCS. For the last 30 years, CAE has become a widely used procedure in preventing stroke. At the same time, improvement of noninvasive imaging techniques (duplex ultrasound scan, CT, and MRI) has allowed a better detection of
RCS after primary CAE. Studies regarding primary CAE found a wide range in RCS incidence, depending on the surgical technique (use of patch angioplasty or primary closure), the method used for detection, the definition of RCS, and the length of follow-up.5 Although the incidence of RCS is not clearly known, the proportion of procedures performed for RCS is between 1% and 10% (2.8% in our department) of open carotid procedures.12,13,16-40 However, RCS seems to become a more common indication for CAS, as demonstrated in the recent publication of the Society for Vascular Surgery (SVS) vascular registry data: the treatment of an RCS accounted for 1.2% of 3259 open surgical carotid procedures vs 22.3% of 2763 CAS procedures between 2005 and 2007.41 This finding suggests the acceptance of CAS as first-line therapy for RCS by many surgeons despite the lack of supporting evidence.
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Coscas et al 1129
Table VI. Early and long-term results of consequent series (⬎30 vessels) reporting on transluminal angioplasty with or without stenting for recurrent carotid stenosis Early results (⬍30 days)
Author
Period 10
New et al Vitek et al49 Bowser et al50 Mc Donnell et al51 De Borst et al52 Bettendorf et al53 Kadhkhodayan et al54 Cuadra et al55 Mehta et al11 Aburahma et al56 Attigah et al40 Vos et al57
No. patients (carotids)
Long-term results
Nonfatal Neurologic Tertiary Carotid Tertiary stroke Deaths CMSM CNI Follow-up events RCS occlusion intervention % % % % (months) % % % %
1998-NS 338 (358) NS 99 (110) 1997-2002 50 (52)
2.5 3 2
1.2 1 2
3.7 4 4
0 0 0
14 20 22
0 0 2
6.0 NS 16
0 NS 0
2.6 NS 8
1994-2001
25 (30)
0
3
3
0
20
0
10**
0
10
1998-2004
55 (57)
0
0
0
0
36
3.6
19
1.7
11.4
2002-2006
33 (45)
3
0
3
0
10
0
6.1*
0
NS
1996-2005 75 (83) 1996-2006 NS (118) 1996-2006 223 (NS)
3.6 2.5 1.4
0 2.5 0
3.6 5.1 1.4
0 0 0
22.4 NS NS
6 NS NS
4.8 NS NS
0 NS NS
0 NS NS
2001-2008 112 (112) 1989-2007 NS (45) 1997-2006 72 (72)
0.9 0 0
0 0 0
0.9 0 0
0 0 0
25 24.8 NS
1.8 0 NS
15 NS NS
0 NS NS
3.6 2.2 NS
CMSM, Combined operative mortality and stoke morbidity; CNI, cranial nerve injury; RCS, recurrent carotid stenosis ⬎50%; CAE, carotid artery endarterectomy; Neurologic events includes both transient ischemic attack and stroke. NS, not stated. *RCS ⬎80%. **RCS ⬎90%.
The reasons why some patients develop RCS whereas most do not remains poorly understood. Although tobacco use,42 female gender43 and hyperlipidemia44 were considered to be associated with RCS, these findings are controversial45 and the natural history of RCS remains poorly known. Some controversies exist about the risk of ipsilateral stroke in the setting of an RCS.46,47 However, most authors recommend treatment of lesions at high risk for stroke, such as ⬎50% stenosis for symptomatic RCS and ⬎80% stenosis for asymptomatic RCS, and this was our approach to the patients reported in this study. Although these recommendations are similar to those for primary CAE, the upper limit of acceptable stroke/death rate for OS in the management of RCS has been defined to be lower than 10%.48 In fact, all published series since 1995 have reported rates of CMSM between 0% and 5.6% and our early results are consistent with those previously reported (Table V).12,13,16-40 The surgical approach to RCS is reputed to be challenging. However, in our series, 103 (87%) of the 119 cases were defined as “simple” by the senior surgeon and did not require any technical adaptation in comparison to a primary approach. In our practice, the surgical approach to an RCS was not as technically demanding as surgeons supporting CAS argue. Should care be taken to first control the carotid in nonpreviously dissected areas, the rest of the procedure does not carry any major technical difficulty. Moreover, primary CAE is a commonly performed procedure with which all vascular surgeons are familiar. Our rate of CNI after OS for RCS is 4.2%, which is consistent with other reports (Table V).12,13,16-40 Al-
though CAS eliminates the risk of CNI, it must be emphasized that CNI are usually temporary as were all but one in this study. Regarding the rate of immediate neurologic and/or fatal complications, our results seem to be similar to those reported in previous series (Table V)12,13,16-40 but also to those published with CAS (Table VI).10,11,49-57 Indeed, apart from two series of OS with a CMSM of 10.5, and 9.7%, respectively, all reported rates of CMSM were between 0% and 6.3% regardless of the technique used (Tables V and VI). Few studies have focused on long-term durability of both techniques. However, this consideration is of particular importance because of the age and expected longevity of patients with RCS. To our knowledge, only two large recent studies (⬎100 cases) have reported long-term results for OS in RCS. O’Hara et al12 reported on a late neurologic event rate of 8.7% in 196 patients undergoing OS for RCS and followed for a mean of 4.3 years. More than half of the late neurologic events were TIAs. At last follow-up, 6% of the ipsilateral carotid arteries were found to be occluded, 3% had an 80% to 99% stenosis, 7% had a 60% to 79% stenosis, 5% had a 40% to 59% stenosis, 16% had a 20% to 39% stenosis, and 63% had a 0% to 19% stenosis. Reporting on their results of secondary CAE over 153 RCS (145 patients), Stoner et al13 found similar results with rates of stroke and ⬎50% tertiary RCS of 4% and 9.2%, respectively, at 4.4 years. However, in a study published in 1992, Treiman et al20 reported 23 tertiary RCS of ⬎50% in a series of 105 redo CAEs with 64-month follow-up. Our rate of tertiary RCS is 5.0% with a mean follow-up of 53
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1130 Coscas et al
months. A longer follow-up period could result in a higher rate of tertiary RCS. In contrast, the long-term results of CAS remain in question. No large series describing the long-term results of CAS has been published to date. At intermediate followup, rates of RCS seem relatively high, perhaps leading to even more challenging tertiary procedures. In the most important published series of CAS for RCS (358 cases), the rate of significant tertiary RCS ⬎50% was 6% at 6 months, which is similar to the rate observed in this series after 53 months of follow-up.10 Although the rate of tertiary RCS after CAS is acceptable at 6-month follow-up, it can be expected to increase with longer follow-up. Studies by AbuRahma33 and de Borst52 have shown tertiary RCS rates after CAS of 24% and 19% with mean follow-up periods of 18 and 36 months, respectively.32,52 In this single center report on OS for RCS, we were limited by the retrospective nature of the analysis and incomplete follow-up in an important proportion of patients. Moreover, although early results demonstrated stroke and mortality rates in the range of those usually reported for the treatment of primary carotid stenosis, it should be emphasized that our patients were not routinely examined by a neurologist during the postoperative period. Also, our team has extensive experience with open carotid procedures (⬎350/year). Our results may not be generalizable to lower volume centers. The lack of prospective randomized trial, the heterogeneity of reported data through the literature (Table V and VI) and the absence of standardized criteria for long-term success can only allow for tentative conclusions regarding the management of RCS. Clearly, late tertiary RCS is a concerning problem, more common after CAS, and follow-up paradigms should be defined as a function of the technique used to treat RCS. In perspective medical therapy, OS and CAS will improve their results in the following years. The generalization of the prescriptions of antiplatelet medications and statins,58 the refinement of perioperative protocols after OS, and the use of new CAS technical adjuncts like cerebral protection devices and drug-eluting stents59 will lead the vascular surgical community to undertake new evaluations in the future. CONCLUSION The results of this series support OS as a durable treatment for RCS. The low rates of both perioperative and long-term neurologic and anatomic complications observed after OS compare favorably with those reported for CAS and suggest that OS remains the preferred option for the treatment of severe RCS. The comparison between OS and CAS for RCS suffers from the absence of standardized follow-up paradigms after primary OS and the lack of a prospective randomized trial comparing the two techniques. Considering these findings and the age and expected longevity of patients presenting with RCS, OS remains the first line treatment for RCS in our center.
AUTHOR CONTRIBUTIONS Conception and design: RC, LC, FK Analysis and interpretation: RC, LC, FK Data collection: RC, BR, NG-C, TC, CdT Writing the article: RC, FK Critical revision of the article: RC, LC, FK Final approval of the article: RC, BR, NG-C, TC, CdT, LC, EK, FK Statistical analysis: RC, FK Obtained funding: Not applicable Overall responsibility: RC, FK REFERENCES 1. [No authors listed.] Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med 1991;325:445-53. 2. Barnett HJ, Taylor DW, Eliasziw M, Fox AJ, Ferguson GG, Haynes RB, et al. Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med 1998; 339:1415-25. 3. [No authors listed.] Endarterectomy for asymptomatic carotid artery stenosis. Executive Committee for the Asymptomatic Carotid Atherosclerosis Study. JAMA 1995;273:1421-8. 4. Halliday A, Mansfield A, Marro J, Peto C, Peto R, Potter J, et al. Prevention of disabling and fatal strokes by successful carotid endarterectomy in patients without recent neurological symptoms: randomised controlled trial. Lancet 2004;363:1491-502. 5. Lattimer CR, Burnand KG. Recurrent carotid stenosis after carotid endarterectomy. Br J Surg 1997;84:1206-19. 6. Mas JL, Chatellier G, Beyssen B, Branchereau A, Moulin T, Becquemin JP, et al. Endarterectomy versus stenting in patients with symptomatic severe carotid stenosis. N Engl J Med 2006;355:1660-71. 7. SPACE Collaborative Group, Ringleb PA, Allenberg J, Brückmann H, Eckstein HH, Fraedrich G, et al. 30 day results from the SPACE trial of stent-protected angioplasty versus carotid endarterectomy in symptomatic patients: a randomised non-inferiority trial. Lancet 2006;368:1239-47. 8. Mas JL, Trinquart L, Leys D, Albucher JF, Rousseau H, Viguier A, et al. Endarterectomy versus angioplasty in patients with symptomatic severe carotid stenosis (EVA-3S) trial: results up to 4 years from a randomised, multicentre trial. Lancet Neurol 2008;7:885-92. 9. Eckstein HH, Ringleb P, Allenberg JR, Berger J, Fraedrich G, Hacke W, et al. Results of the stent-protected angioplasty versus carotid endarterectomy (SPACE) study to treat symptomatic stenoses at 2 years: a multinational, prospective, randomised trial. Lancet Neurol 2008;7:893-902. 10. New G, Roubin GS, Iyer SS, Vitek JJ, Wholey MH, Diethrich EB, et al. Safety, efficacy, and durability of carotid artery stenting for restenosis following carotid endarterectomy: a multicenter study. J Endovasc Ther 2000;7:345-52. 11. Mehta RH, Zahn R, Hochadel M, Ischinger T, Jung J, Hauptmann KE, et al. Comparison of in-hospital outcomes of patients with versus without previous carotid endarterectomy undergoing carotid stenting (from the German ALKK CAS Registry). Am J Cardiol 2007;99:1288-93. 12. O’Hara PJ, Hertzer NR, Karafa MT, Mascha EJ, Krajewski LP, Beven EG. Reoperation for recurrent carotid stenosis: early results and late outcome in 199 patients. J Vasc Surg 2001;34:5-12. 13. Stoner MC, Cambria RP, Brewster DC, Juhola KL, Watkins MT, Kwolek CJ, et al. Safety and efficacy of reoperative carotid endarterectomy: a 14-year experience. J Vasc Surg 2005;41:942-9. 14. Autorité de Santé H. [Vascular prevention after cerebral infarct or transient ischemic attack. Recommendations. March 2008] [Article in French] Rev Neurol (Paris) 2008;164 Spec No 3:F229-34.
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