- Email: [email protected]
Carotid artery stenting in patients with near occlusion: A single-center experience and comparison with recent studies
Clinical Neurology and Neurosurgery 115 (2013) 1976–1981
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Carotid artery stenting in patients with near occlusion: A single-center experience and comparison with recent studies Seungnam Son a,c , Dae Seob Choi b,c,∗ , Soo-Kyoung Kim a,c , Heeyoung Kang a , Ki-Jong Park a , Nack-Cheon Choi a,c , Oh-Young Kwon a , Byeong Hoon Lim a,c a
Department of Neurology, Gyeongsang National University School of Medicine, Jinju, South Korea Department of Radiology, Gyeongsang National University School of Medicine, Jinju, South Korea c Gyeongnam Regional Cardiocerebrovascular Disease Center, Jinju, South Korea b
a r t i c l e
i n f o
Article history: Received 27 February 2013 Received in revised form 10 April 2013 Accepted 4 June 2013 Available online 29 June 2013 Keywords: Carotid artery stenosis Carotid artery stenting Cerebral hyperperfusion Embolic protection devices Stroke prevention
a b s t r a c t Objective: The optimal management strategy for carotid artery near occlusion is still controversial. Nevertheless, prior studies about carotid artery stenting in patients with near occlusion reported both technically and clinically inspiring results. To define the effectiveness, safety, and clinical outcomes of carotid artery stenting in patients with near occlusion, we analyzed our experiences and compared with recent studies. Methods: We performed 24 carotid artery stenting procedures in 24 patients with near occlusion between January 2010 and July 2012. The patient group comprised 20 men (83.3%) and four women (16.7%) with a mean age of 69.5 years (range, 53–85 years). Eighteen patients had prior stroke or transient ischemic attack (75%), and six patients were asymptomatic (25%). Results: Successful stent insertion was achieved in 23 of 24 patients (95.8%). Cerebral hyperperfusion syndrome and post-procedural vascular events occurred in four patients, and all of these developed within 24 h after the procedure (17.4%; two: hyperperfusion syndrome, two: acute myocardial infarction). The mean follow-up period after carotid artery stenting was 16.7 ± 9.2 months (range, 6–32 months). No stroke related to carotid artery stenting or significant restenosis of the inserted stent developed during the follow-up period. Conclusions: Carotid artery stenting in patients with near occlusion seems to be a technically feasible and effective method to prevent stroke recurrence. But hyperperfusion syndrome and post-procedural vascular event rates may be high, as shown in this study. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Atherosclerotic carotid artery disease is a well-known risk factor for ischemic stroke. Based on the results of the North American Symptomatic Carotid Endarterectomy Trial (NASCET), an increased degree of carotid stenosis is associated with a risk for ipsilateral stroke in patients with symptomatic and asymptomatic carotid stenosis [1]. But in a subgroup analysis of the NASCET study in which subjects were subdivided 90–99% stenosis into 90–94% stenosis and near-occlusion groups, patients with near occlusion had a lower risk of stroke within 1 year compared with patients with 90–94% stenosis (11% vs. 35%) [2]. The perioperative risk was similar in the two stenosis subgroups (approximately 6%), so it
∗ Corresponding author at: Department of Radiology, Gyeongsang National University School of Medicine, 79 Gangnam-ro, Jinju 660-702, South Korea. Tel.: +82 55 750 8201; fax: +82 55 758 1568. E-mail address: [email protected] (D.S. Choi). 0303-8467/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2013.06.001
was thought that surgery for near occlusion carries no benefit for patients [2]. However, surgically treated patients did not suffer stroke in a carotid endartrectomy (CEA) study of near occlusion, but ipsilateral stroke occurred in 33% of medically treated patients [3]. In 2005, Fox et al. reviewed the angiography results of 1216 patients in the NASCET and European Carotid Surgery Trial (ESCT) [4], and reclassified 262 patients as near occlusion (137 NASCET patients and 125 ECST patients) using their own criteria. Of these, 15.1% of the patients treated medically versus 10.9% of the patients treated surgically suffered an ipsilateral stroke within 3 years [5]. Although a high stroke incidence has been reported in medically treated patients, and surgical intervention has proven benefits, the decision for revascularization in patients with carotid near occlusion still remains unclear, and the optimal management strategy for carotid artery near occlusion is still not established [6]. Carotid artery stenting (CAS) is an alternative to CEA and has received the same recommendation class in recent guidelines [7]. CAS is not inferior to CEA for treating patients with severe stenosis of the internal carotid artery (ICA) with an embolic protection
S. Son et al. / Clinical Neurology and Neurosurgery 115 (2013) 1976–1981
device (EPD) [8]. However, selecting the stenotic artery and passing an EPD through the stenotic segment is not always possible in patients with a near occlusion. Nevertheless, previous studies in patients with carotid artery near occlusion indicate that CAS is technically safe and feasible and that it provides effective protection against stroke recurrence [9–14]. In this study, we retrospectively analyzed 24 patients with carotid artery near occlusion who were treated with CAS within the past 3 years. The effectiveness, safety, and clinical outcomes of CAS in patients with near occlusion were assessed, and the results were compared with those of recent studies.
2. Materials and methods 2.1. Patients Ninety-nine CAS procedures were performed in 91 patients at our institute between January 2010 and July 2012. We reviewed all clinical and angiographic data of those patients. The criteria of Fox et al. for carotid artery near occlusion were used [5]: (1) delayed cranial arrival of ICA contrast compared with that of the external carotid artery (ECA); (2) intracranial collaterals seen as cross-filling of contralateral vessels or ipsilateral contrast dilution; (3) obviously reduced diameter of the ICA compared with the opposite ICA; or (4) reduction in ICA diameter compared with the ipsilateral ECA. Angiography from 24 CAS procedures in 24 patients met two or more criteria, and these patients were included in this study as patients with near occlusion. The patient group comprised 20 men (83.3%) and four women (16.7%) with a mean age of 69.5 years (range, 53–85 years). Eighteen patients had prior stroke or transient ischemic attack (TIA) (75%), and six patients were asymptomatic (25%). Stroke risk factors included hypertension (83.3%), smoking (54.2%), diabetes (45.8%), hyperlipidemia (41.7%), coronary artery disease (37.5%), and peripheral vascular disease (12.5%). Carotid stenosis was diagnosed using gadolinium (Gadovist, Gadobutrol; Schering, Berlin, Germany)-enhanced magnetic resonance angiography and/or iopromide (Ultravist; Schering)enhanced computed tomography angiography in all patients. Among the 18 symptomatic patients, three had a disabling hemispheric stroke and underwent emergent CAS (mean interval from stroke symptom onset to CAS: 10.8 ± 8.8 h; range, 2.5–20 h), and the remaining 15 patients had non-disabling stroke or TIA and underwent scheduled CAS (mean interval from stroke symptom onset to CAS: 19.3 ± 25.8 days; range, 7–110 days). Carotid stenosis was found during the preoperative evaluation for a coronary artery bypass graft (CABG) or a hemorrhoidectomy operation in three of six asymptomatic patients, and two with symptomatic subclavian artery stenosis were found during the course of additional vascular evaluation. An assessment of cerebral vascular reserve capacity (VRC) using acetazolamide-activated technetium 99-m hexamethylpropyleneamine oxime brain single-photon emission computed tomography (SPECT) was performed in 17 patients (70.8%, symptomatic: 12 of 18 patients, asymptomatic: five of six patients). Inadequate VRC was observed in 13 patients (76.5%, symptomatic: 12 of 12 patients, asymptomatic: one of five patients). All patients were prescribed dual-antiplatelet agents (75 mg/day clopidogrel with 100 mg/day aspirin) and high-dose atorvastatin (80 mg/day) for at least 7 days before CAS. Loading doses of clopidogrel (300 mg) with aspirin (300 mg) and atorvastatin (80 mg/day) were prescribed for emergency cases. Informed consent was obtained from at least two legal representatives of each patient before CAS and also this study was approved by our institutional review board (IRB).
1977
2.2. Intervention protocol All interventions were performed by one experienced neurointerventionalist with/without a neurologist who was a trained neurointerventionalist. First, the femoral artery was punctured under local anesthesia, and a 6F femoral sheath was placed. Diagnostic four-vessel angiography followed to confirm the exact degree of stenosis and the collateral vessels. Next, the 6F femoral sheath was changed to a 6F shuttle catheter and placed distal to the common carotid artery. An EPD was prepared and navigated through the stenotic segment and placed on distal ICA. When the EPD could not be navigated farther due to a tight stenosis, an exchange length 0.014-in. microguidewire (Transcend 300 Floppy microwire; Boston Scientific, Fremont, CA, USA) was used for navigation and was pre-dilated without distal protection using a 2–3 mm balloon to allow the EPD to cross the stenosis. After installing the EPD, pre-dilatation using a 4–5-mm balloon (Aviator plus PTA balloon; Cordis, Miami Lakes, FL, Ultra-soft SV balloon; Boston Scientific) was performed. The stent was selected according to the ICA course: a closed-cell stent was used in a straight course, and an open-cell stent was used in a curved course. Postdilation of the stent was performed after stent deployment using a 5- or 6-mm balloon in selected patients. Heparinized saline was continuously infused through the shuttle catheter to prevent incatheter thrombosis, and 3000 U bolus heparin was injected before stent deployment. Intravenous (IV) atropine and/or IV dopamine was administered when severe hemodynamic effects (bradycardia, asystole, or hypotension) developed after inflating the balloon. Patients who underwent CAS were monitored in the stroke unit or intensive care unit for 24 h with continuous blood pressure, oxygen saturation, and electrocardiographic monitoring and underwent a neurological examination hourly. We conducted massive blood pressure (Bp) control in patients with poor VRC on preprocedural SPECT to prevent development of cerebral hyperperfusion syndrome (CHS). We maintained a systolic Bp level of 110–120 mmHg during the 24 h after the procedure in those patients. In contrast, 200–250 cc/h massive hydration therapy was performed in cases of hypotension persisting after CAS, using normal saline and/or a volume expander with/without IV dopamine infusion until systolic Bp was >100 mmHg. Follow-up diffusionweighted image (DWI) for detecting procedure-related cerebral infarction was recommended to all patients the day after CAS.
2.3. Follow-up Patients who showed no additional neurological deficits after CAS were usually discharged within 3 days after CAS with 75 mg/day clopidogrel, 100 mg/day aspirin, and 20–40 mg/day atorvastatin. These medications were continued for at least 6 months after CAS. A neurological examination was repeated on the discharge day and the day patients visited the outpatient department. A follow-up vascular evaluation was recommended for all patients at 6 and 12 months after CAS and annually thereafter.
3. Results 3.1. Interventional results Based on four-vessel angiography, eight of 24 patients (33.3%) achieved two criteria, seven patients (29.2%) achieved three criteria, and nine patients (37.5%) achieved all four criteria. Criterion 1 was present in 22 of 24 patients (91.7%), criterion 2 in 17 patients (70.8%), criterion 3 in 18 patients (75%), and criterion 4 in 16 patients (66.7%). Contralateral ICA stenosis >70% was found in five
1978
S. Son et al. / Clinical Neurology and Neurosurgery 115 (2013) 1976–1981
Fig. 1. Actual images of carotid artery stenting (CAS) of a patient with a near occlusion on the left side. (A) Pre-procedural basal extracranial lateral projection angiogram. Note the severe stenosis of the left proximal internal carotid artery (ICA) and poorly visible ICA flow (white arrow). (B) Pre-procedural basal intracranial antero-posterior (AP) projection angiogram. Left middle cerebral artery (MCA) and anterior cerebral artery (ACA) flows are also poorly visible (white arrowhead). (C) Postprocedural extracranial lateral projection angiogram. The Precise stent was successfully inserted into a pre-existing stenotic portion of the proximal ICA, and restoration of ICA flow is visible. (D) Post-procedural intracranial AP projection angiogram. Left ACA and MCA flows were also restored.
patients (20.8%), and two had complete occlusion (median degree of contralateral ICA stenosis: 15 ± 33%; range, 5–100%). Stents were successfully inserted in 23 of 24 patients (95.8%, Fig. 1). We could not navigate into the true lumen in one patient, so the procedure failed (Fig. 2). An EPD was used in 22 of 23 patients (95.7%): FilterWire EZ (Boston Scientific/Target Therapeutics) in 18 (81.8%) and Emboshield (Abbott Vascular, Redwood City, CA, USA) in four (18.2%). Eight of 22 patients needed pre-dilation to pass the EPD (36.4%). Additional pre-dilation of the stenosis to allow stent deployment after installing the EPD was required in all patients, except one patient, who was sufficiently dilated after pre-dilation. A stent was implanted in all patients after angioplasty: Precise PRO RX stent (Cordis) in 11 (47.8%), carotid WallStent (Boston Scientific/Target Therapeutics) in eight (34.8%), and a Protégé RX carotid stent (ev3 Inc., Irvine, CA, USA) in four (17.4%). Additionally, 14 of 23 patients (60.9%) required post-dilation after placing the stent. Transient hemodynamic alterations such as hypotension and bradycardia were observed in some patients during and/or after balloon inflation. Transient bradycardia was recovered by encouraging coughing in all patients. But, hypotension persisted in four patients (17.4%) after the procedure and lasted about 24 h. Three recovered after massive hydration therapy, but one needed an additional IV dopamine infusion. No major vascular access site complications were recorded. The mean total procedural time including four-vessel angiography was 69.4 ± 22.5 min (range, 30–115 min). CHS and post-procedural vascular events occurred in four patients (17.4%), and all developed within 24 h after CAS. CHS occurred in two patients (8.7%): one patient (asymptomatic, assessment of VRC was not done) developed a generalized tonic–clonic (GTC) type seizure after the stent was deployed but recovered completely, whereas another patient (symptomatic, inadequate VRC, CAS performed 15 days after stroke onset) developed aphasia 2 h after the procedure and died due to a ipsilateral intracerebral hemorrhage (ICH) despite evacuation of the hematoma (Fig. 3). Another two patients developed acute myocardial infarction (AMI) after CAS: one patient (symptomatic, assessment of VRC was not done due to emergent CAS) underwent the CABG operation 20 days after CAS, and another patient (symptomatic, inadequate VRC) recovered after medical treatment. Eighteen of 23 patients underwent followup DWI the next day after CAS. As a result, 16 of 18 patients (88.9%) showed one or more focal infarctions, but no clinical symptoms were observed in any patient.
3.2. Follow-up results Twenty of 23 patients (87%) received regular clinical follow-up of at least 6 months. The mean follow-up period was 16.7 ± 9.2 months (range, 6–32 months). Among these, only one patient developed an additional infarction 3 months after CAS, but it was not associated with CAS (symptomatic, CAS to right ICA but infarction occurred on the right pons). Ten of 20 patients (50%) underwent follow-up imaging as recommended in the protocol, and an additional four patients were imaged only once (one at 6 months, three at 12 months). Four of 14 patients (2: Precise, 1: Wall, 1: Protégé) showed mild intimal hyperplasia (<30%) on 12-month follow-up imaging, but no additional intervention was needed in any patient. 4. Discussion The term “carotid artery near occlusion” is rather ambiguous [5,15–17]. Generally, near occlusion of the carotid artery is defined as the presence of severe stenosis in the ICA and decreased perfusion distal to the stenosis, resulting in diminished or absent distal carotid flow [15–17]. Such an appearance has been referred to as a “pseudo-occlusion,” “near occlusion,” or an “angiographic string sign”[5,15–17]. We used the near-occlusion criteria of Fox et al., which were published in 2005 [5]. If a patient had one criterion, the sensitivity and specificity was 90.6% and 84.4%, respectively, and if they had two or more criteria, the sensitivity and specificity were 90.6% and 93.8%. But, specificity increased to 96.9% in patients with three or more criteria, whereas sensitivity decreased to 59.4% and 31.3%, respectively [5]. Thus, we chose “two or more criteria present” for near occlusion. We found six studies about CAS in patients with near occlusion through searches on Pubmed and Google [9–14]. Two studies were conducted at the same institute by the same investigators [9,13]. Thus, we choose the study that contained more patients [13]. All were retrospective observational studies due to the rarity of near occlusion (Table 1) [10–14]. Among them, four studies included only 9–24 patients, as in our study [10–12,14], but the authors reported their 10 years of experience with 116 patients in another study [13]. The procedural and clinical results of CAS in patients with near occlusion were inspiring in that study. In 189 patients from five studies, the technical success rate was 99.5%, and only one patient failed CAS [14]. Additionally, only six patients
S. Son et al. / Clinical Neurology and Neurosurgery 115 (2013) 1976–1981
1979
Fig. 2. Actual images of a patient who underwent a failed left-sided carotid artery stenting (CAS). (A and B) basal extracranial (A) and intracranial (B) pre-procedural anteroposterior (AP) projection angiogram. Angiographic string sign is shown. (C) Extracranial AP projection angiogram during the procedure. Microguidewire and microcatheter cannot pass the stenotic portion of the proximal internal carotid artery (ICA) (black arrow in A).
suffered post-procedural vascular events (3.2%; five patients: TIA [13,14], one patient: cardiac death [10], and additional one patient developed AMI but 21 days after CAS [11]). CAS did not succeed in one patient, and CHS and post-procedural vascular events occurred in four patients in our study. CAS is performed on more than 40 cases annually at our institute, and the neurointerventionalist at our institute has performed more than 300 CAS procedures during the past 10 years. Thus, the failed CAS in one patient was not associated with technical inexperience. This is the first study of CAS in patients with near occlusion with high rates of CHS and post-procedural vascular events. The prevalence of CHS after CAS is quite low. In one study, only 10 CHS cases developed (2.4%) in 417 CAS procedures [18]. In another study, the prevalence was just 1.1% (five of 450 CAS) [19]. But the prevalence in our study was very high at 8.7% (two of 23 CAS).
Actually, we experienced only two cases of CHS in 99 CAS (2.0%) procedures, but both were patients with near occlusion. Fortunately, one patient who presented with GTC-type seizures just after stent deployment recovered completely and showed no neurological sequelae. But the other patient developed fatal ICH and eventually died. The development of CAS-associated ICH is very rare [19–21], and we have never experienced it before or after this patient. It was thought that the most important component of perioperative management to prevent CHS is control of systemic Bp [19–21]. However, Ogasawara et al. reported that poor postoperative Bp control is significantly associated with the development of ICH in patients with CHS after CEA but not CAS [22]. The maximum systolic Bp during and after the procedure in our patient with ICH did not exceed 120 mmHg. Thus, it may be that ICH in patients with CHS, and further more CHS after CAS, would not be prevented by
Fig. 3. Actual angiographic and computed tomography (CT) images of a patient with a fatal intracerebral hemorrhage (ICH) after carotid artery stenting (CAS). Severe stenosis of the proximal portion of the left internal carotid artery (ICA) (A) was successfully treated using a Precise stent (B). The patient developed aphasia with right hemiparesis about 2 h after CAS. A large ICH was observed on the CT image obtained immediately after symptom development (C).
1980
S. Son et al. / Clinical Neurology and Neurosurgery 115 (2013) 1976–1981
Table 1 Comparison of our study with other studies. Author
No. of Pts.
Symptomatic stenosis (%)
Use of EPD (%)
Success rate (%)
CHS (%)
Vascular complications
Follow-up (month)
Ipsilateral stroke recurr
Restenosis
Terada Nikas Barker González Spacek Our study
20 25 9 116 19 24
85 80 100 91 58 75
95 100a 67 79 84 96
100 100 100 100 95b 96
0 0 0 0 0 9
1c 1d None 4e 1f 2
25 12 12 36 6 17
None None 1g 1h None None
1i None None 8j 1k None
Author indicates the first author of each study; CAS, carotid artery stenting; CHS, cerebral hyperperfusion syndrome; EPD, embolic protection device; restenosis, significant restenosis on inserted stent >70% and/or required retreatment by angioplasty; TIA, transient ischemic attack. a 24 of 25 patients received a proximal protection device. One patient received a distal protection device. b Failed in one patient due to failure of guidewire passage through the stenosis. c One patient with chronic renal failure died after hemodialysis the day after CAS. d One patient developed acute myocardial infarction at day 21 after the procedure. e Four patients developed short-lasting ipsilateral TIAs within 15 min after CAS. f One patient developed a TIA during the postoperative hospitalization period. g One patient developed a possible TIA at 3 months after CAS. h Three patients experienced a stroke during follow up, only one of which was on the ipsilateral side. i One patient showed restenosis 6 months after CAS and was retreated with angioplasty. j Five patients showed restenosis >70% before month 6 after CAS, and three were retreated with angioplasty. Three patients showed asymptomatic occlusion. k One patient showed restenosis of >80% on a duplex ultrasound examination 1 month after CAS and was retreated with angioplasty.
strict Bp control only. In a pooled analysis study, CAS-associated ICH was related to technical inexperience (<100 cases), symptomatic lesions, severe stenosis >90%, maximal stenosis located distal to bifurcation, and preexisting cerebral infarction [20]. Our patient had symptomatic near occlusion and preexisting cerebral infarction on the ipsilateral basal ganglia. Additionally, we think that the development of ICH in this patient may have been associated with massive anticoagulation/antiplatelet agent therapy. However, on the prior studies, use of antiplatelet agent/anticoagulation is not associated with ICH after CEA [21] or CAS [19]. The patient suffered a renal infarction due to atrial fibrillation and had taken warfarin 4 months before CAS. The patient was prescribed additional aspirin and clopidogrel with warfarin for the CAS. It is regret that we did not delay the procedure in spite of the international normalized ratio of prothrombin time on the day of the procedure was higher than the recommended level (3.11). Four patients in our study showed persistent hypotension during the 24 h after CAS. Among them, two developed AMI within 24 h after CAS. Both patients revealed three-vessel coronary artery disease on the cardiac work-up. We thought initially that hypotension induced by CAS and excessive cardiac loading due to massive hydration therapy were possible inducing causes of the AMI, but hypotension itself seemed to be more important than excessive cardiac loading. During this study period, additional one patient not included this study (symptomatic, 90% stenosis on left ICA) developed AMI within 24 h after CAS. We performed massive Bp control, but not massive hydration therapy, after CAS due to poor VRC on pre-procedural SPECT. This patient also had three-vessel disease on the cardiac work-up and underwent a CABG operation 10 days after CAS. It is possible that post-procedural vascular event rates among patients with near occlusion who receive CAS are higher than has been recognized. We think that this may be associated with the possibility of high comorbidity from other vascular disease. We suspect hypotension as the main cause of post-procedural AMI. If Bp control is not crucial for preventing CHS, unconditional strict Bp control after CAS might be harmful to some patients. Because coronary heart disease and carotid artery disease share the same risk factors [23], there is a strong possibility of comorbid coronary heart disease in patients with carotid artery stenosis. Actually, a high proportion of patients with three-vessel coronary artery disease have comorbid carotid artery stenosis [24]. None of the patients who suffered from AMI in our study had a history of previous coronary heart disease, and there was no evidence of ischemic heart disease on the
pre-procedural electrocardiogram or echocardiogram, but they had asymptomatic three-vessel coronary artery disease. Thus, it is necessary to conduct a vascular imaging work-up to judge coronary artery status before CAS. Furthermore, proper Bp control according to coronary artery status would prevent the development of AMI after CAS. The long-term follow-up results of CAS in patients with near occlusion were outstanding. Stroke recurrence on the ipsilateral side of CAS has been reported in only two cases in two studies (one: possible TIA at 3 months after CAS [12]; one: stroke at 19 months after CAS [13]). In our study, no patient suffered a stroke on the ipsilateral side, but one patient developed a pontine infarction 3 months after CAS. In another study, the authors reported a very high rate of mortality within 6 months after CAS [14], but no neurological or cardiovascular complications related to CAS were reported in that study, and the causes of death were pneumonia, heart failure, and stroke on the contralateral side [14]. Additionally, restenosis >70% or occlusion of the inserted stent was reported in 10 patients in three studies (nine patients at 6 months [10,13], one patient at 1 month [14]), but all were asymptomatic [10,13,14].
5. Conclusions This study has major limitations, including retrospective nature of the analysis, absence of a control group, small number of patients, and relatively short follow-up. But we verified previous CAS results in patients with a carotid near occlusion and identified CAS as a technically feasible and effective method for preventing stroke by comparing our results with others in the literature. Although a high rate of CHS and post-procedural vascular events were observed in our study, particularly within 24 h after the procedure, these events could be avoided by cautious monitoring during and after the procedure and by conducting an appropriate pre-procedural work up.
Disclosures None.
Conflict of interest None.
S. Son et al. / Clinical Neurology and Neurosurgery 115 (2013) 1976–1981
References [1] North American Symptomatic Carotid Endarterectomy Trial (NASCET) Investigators. Clinical alert: benefit of carotid endarterectomy for patients with high-grade stenosis of the internal carotid artery. National Institute of Neurological Disorders and Stroke, Stroke and Trauma Division. Stroke 1991;22:816–7. [2] Morgenstern LB, Fox AJ, Sharpe BL, Eliasziw M, Barnett HJ, Grotta JC. The risks and benefits of carotid endarterectomy in patients with near occlusion of the carotid artery. Neurology 1997;48:911–5. [3] O’Leary DH, Mattle H, Potter JE. Atheromatous pseudo-occlusion of the internal carotid artery. Stroke 1989;20:1168–73. [4] European Carotid Surgery Trialists’ Collaborative Group. Randomised trial of endarterectomy for recently symptomatic carotid stenosis: final results of the MRC European Carotid Surgery Trial (ECST). Lancet 1998;351: 1379–87. [5] Fox AJ, Eliasziw M, Rothwell PM, Schmidt MH, Warlow CP, Barnett HJ. Identification, prognosis, and management of patients with carotid artery near occlusion. American Journal of Neuroradiology 2005;26:2086–94. [6] Yadav JS. Functional occlusions of the carotid artery (string signs): to treat or not to treat? Journal of the American College of Cardiovascular Interventions 2010;3:305–6. [7] Brott TG, Halperin JL, Abbara S, Bacharach J, Barr JD, Bush RL, et al. ASA/ACCF/AHA/AANN/AANS/ACR/ASNR/CNS/SAIP/SCAI/SIR/SNI S/SVM/SVS guideline on the management of patients with extracranial carotid and vertebral artery disease. Journal of the American College of Cardiology 2011;57:e16–94. [8] CAVATAS Investigators. Endovascular versus surgical treatment in patients with carotid stenosis in the Carotid and Vertebral Artery Transluminal Angioplasty Study (CAVATAS): a randomized trial. Lancet 2001;357: 1729–37. [9] Gil-Peralta A, González A, González-Marcos JR, Mayol A, Boza F, Ruano J, et al. Internal carotid artery stenting in patients with symptomatic atheromatous pseudo-occlusion. Cerebrovascular Disease 2004;17:105–12. [10] Terada T, Tsuura M, Matsumoto H, Masuo O, Tsumoto T, Yamaga H, et al. Endovascular treatment for pseudo-occlusion of the internal carotid artery. Neurosurgery 2006;59:301–9. [11] Nikas DN, Ghany MA, Stabile E, Sorropago G, Saccá S, Favero L, et al. Carotid artery stenting with proximal cerebral protection for patients with angiographic appearance of string sign. JACC: Cardiovascular Interventions 2010;3:298–304.
1981
[12] Barker CM, Gomez J, Grotta JC, Smalling RW. Feasibility of carotid artery stenting in patients with angiographic string sign. Catheterization and Cardiovascular Interventions 2010;75:1104–9. [13] González A, Gil-Peralta A, Mayol A, Gonzalez-Marcos JR, Moniche F, Aguilar M, et al. Internal carotid artery stenting in patients with near occlusion: 30-day and long-term outcome. American Journal of Neuroradiology 2011;32:252–8. [14] Spacek M, Martinkovicova L, Zimolova P, Veselka J. Mid-term outcomes of carotid artery stenting in patients with angiographic strong sign. Catheterization and Cardiovascular Interventions 2012;79:174–9. [15] Berman SS, Devine JJ, Erodes LS, Hunter GC. Distinguishing carotid artery pseudo-occlusion with color-flow Doppler. Stroke 1995;26:434–8. [16] Henderson RD, Eliasziw M, Fox AJ, Rothwell PM, Barnett HJ. Angiographically defined collateral circulation and risk of stroke in patients with severe carotid stenosis. North American Symptomatic Carotid Endartrectomy Trial (NASCET) group. Stroke 2000;31:128–32. [17] Lee DH, Gao FQ, Rankin RN, Pelz DM, Fox AJ. Duplex and color Doppler flow sonography of occlusion and near occlusion of the carotid artery. American Journal of Neuroradiology 1996;17:1267–74. [18] Grunwald IQ, Politi M, Reith W, Krick C, Karp K, Zimmer A, et al. Hyperperfusion syndrome after carotid stent angioplasty. Neuroradiology 2009;5:169–74. [19] Abou-Chebl A, Yadav JS, Reginelli JP, Bajzer C, Bhatt D, Krieger DW. Intracranial hemorrhage and hyperperfusion syndrome following carotid artery stenting: risk factors, prevention, and treatment. Journal of the American College of Cardiology 2004;43:1596–601. [20] Kang HS, Han MH, Kwon OK, Kwon BJ, Kim SH, Oh CW. Intracranial hemorrhage after carotid angioplasty: a pooled analysis. Journal of Endovascular Therapy 2007;14:77–85. [21] Ouriel K, Shortell CK, Illig KA, Greenberg RK, Green RM. Intracerebral hemorrhage after carotid endarterectomy: incidence, contribution to neurologic morbidity, and predictive factors. Journal of Vascular Surgery 1999;29:82–7. [22] Ogasawara K, Sakai N, Kuroiwa T, Hosoda K, Iihara K, Toyoda K, et al. Japanese society for treatment at neck in cerebrovascular disease study group. Intracranial hemorrhage associated with cerebral hyperperfusion syndrome following carotid endarterectomy and carotid artery stenting: retrospective review of 4494 patients. Journal of Neurosurgery 2007;107:1130–6. [23] Wilson PW, D’Agostino RB, Levy D, Belanger AM, Silbershatz H, Kannel WB. Prediction of coronary heart disease using risk factor categories. Circulation 1998;97:1837–47. [24] Tanimoto S, Ikari Y, Tanabe K, Yachi S, Nakajima H, Nakayama T, et al. Prevalence of carotid artery stenosis in patients with coronary artery disease in Japanese population. Stroke 2005;36:2094–8.
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Carotid artery stenting in patients with near occlusion: A single-center experience and comparison with recent studies Seungnam Son a,c , Dae Seob Choi b,c,∗ , Soo-Kyoung Kim a,c , Heeyoung Kang a , Ki-Jong Park a , Nack-Cheon Choi a,c , Oh-Young Kwon a , Byeong Hoon Lim a,c a
Department of Neurology, Gyeongsang National University School of Medicine, Jinju, South Korea Department of Radiology, Gyeongsang National University School of Medicine, Jinju, South Korea c Gyeongnam Regional Cardiocerebrovascular Disease Center, Jinju, South Korea b
a r t i c l e
i n f o
Article history: Received 27 February 2013 Received in revised form 10 April 2013 Accepted 4 June 2013 Available online 29 June 2013 Keywords: Carotid artery stenosis Carotid artery stenting Cerebral hyperperfusion Embolic protection devices Stroke prevention
a b s t r a c t Objective: The optimal management strategy for carotid artery near occlusion is still controversial. Nevertheless, prior studies about carotid artery stenting in patients with near occlusion reported both technically and clinically inspiring results. To define the effectiveness, safety, and clinical outcomes of carotid artery stenting in patients with near occlusion, we analyzed our experiences and compared with recent studies. Methods: We performed 24 carotid artery stenting procedures in 24 patients with near occlusion between January 2010 and July 2012. The patient group comprised 20 men (83.3%) and four women (16.7%) with a mean age of 69.5 years (range, 53–85 years). Eighteen patients had prior stroke or transient ischemic attack (75%), and six patients were asymptomatic (25%). Results: Successful stent insertion was achieved in 23 of 24 patients (95.8%). Cerebral hyperperfusion syndrome and post-procedural vascular events occurred in four patients, and all of these developed within 24 h after the procedure (17.4%; two: hyperperfusion syndrome, two: acute myocardial infarction). The mean follow-up period after carotid artery stenting was 16.7 ± 9.2 months (range, 6–32 months). No stroke related to carotid artery stenting or significant restenosis of the inserted stent developed during the follow-up period. Conclusions: Carotid artery stenting in patients with near occlusion seems to be a technically feasible and effective method to prevent stroke recurrence. But hyperperfusion syndrome and post-procedural vascular event rates may be high, as shown in this study. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Atherosclerotic carotid artery disease is a well-known risk factor for ischemic stroke. Based on the results of the North American Symptomatic Carotid Endarterectomy Trial (NASCET), an increased degree of carotid stenosis is associated with a risk for ipsilateral stroke in patients with symptomatic and asymptomatic carotid stenosis [1]. But in a subgroup analysis of the NASCET study in which subjects were subdivided 90–99% stenosis into 90–94% stenosis and near-occlusion groups, patients with near occlusion had a lower risk of stroke within 1 year compared with patients with 90–94% stenosis (11% vs. 35%) [2]. The perioperative risk was similar in the two stenosis subgroups (approximately 6%), so it
∗ Corresponding author at: Department of Radiology, Gyeongsang National University School of Medicine, 79 Gangnam-ro, Jinju 660-702, South Korea. Tel.: +82 55 750 8201; fax: +82 55 758 1568. E-mail address: [email protected] (D.S. Choi). 0303-8467/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2013.06.001
was thought that surgery for near occlusion carries no benefit for patients [2]. However, surgically treated patients did not suffer stroke in a carotid endartrectomy (CEA) study of near occlusion, but ipsilateral stroke occurred in 33% of medically treated patients [3]. In 2005, Fox et al. reviewed the angiography results of 1216 patients in the NASCET and European Carotid Surgery Trial (ESCT) [4], and reclassified 262 patients as near occlusion (137 NASCET patients and 125 ECST patients) using their own criteria. Of these, 15.1% of the patients treated medically versus 10.9% of the patients treated surgically suffered an ipsilateral stroke within 3 years [5]. Although a high stroke incidence has been reported in medically treated patients, and surgical intervention has proven benefits, the decision for revascularization in patients with carotid near occlusion still remains unclear, and the optimal management strategy for carotid artery near occlusion is still not established [6]. Carotid artery stenting (CAS) is an alternative to CEA and has received the same recommendation class in recent guidelines [7]. CAS is not inferior to CEA for treating patients with severe stenosis of the internal carotid artery (ICA) with an embolic protection
S. Son et al. / Clinical Neurology and Neurosurgery 115 (2013) 1976–1981
device (EPD) [8]. However, selecting the stenotic artery and passing an EPD through the stenotic segment is not always possible in patients with a near occlusion. Nevertheless, previous studies in patients with carotid artery near occlusion indicate that CAS is technically safe and feasible and that it provides effective protection against stroke recurrence [9–14]. In this study, we retrospectively analyzed 24 patients with carotid artery near occlusion who were treated with CAS within the past 3 years. The effectiveness, safety, and clinical outcomes of CAS in patients with near occlusion were assessed, and the results were compared with those of recent studies.
2. Materials and methods 2.1. Patients Ninety-nine CAS procedures were performed in 91 patients at our institute between January 2010 and July 2012. We reviewed all clinical and angiographic data of those patients. The criteria of Fox et al. for carotid artery near occlusion were used [5]: (1) delayed cranial arrival of ICA contrast compared with that of the external carotid artery (ECA); (2) intracranial collaterals seen as cross-filling of contralateral vessels or ipsilateral contrast dilution; (3) obviously reduced diameter of the ICA compared with the opposite ICA; or (4) reduction in ICA diameter compared with the ipsilateral ECA. Angiography from 24 CAS procedures in 24 patients met two or more criteria, and these patients were included in this study as patients with near occlusion. The patient group comprised 20 men (83.3%) and four women (16.7%) with a mean age of 69.5 years (range, 53–85 years). Eighteen patients had prior stroke or transient ischemic attack (TIA) (75%), and six patients were asymptomatic (25%). Stroke risk factors included hypertension (83.3%), smoking (54.2%), diabetes (45.8%), hyperlipidemia (41.7%), coronary artery disease (37.5%), and peripheral vascular disease (12.5%). Carotid stenosis was diagnosed using gadolinium (Gadovist, Gadobutrol; Schering, Berlin, Germany)-enhanced magnetic resonance angiography and/or iopromide (Ultravist; Schering)enhanced computed tomography angiography in all patients. Among the 18 symptomatic patients, three had a disabling hemispheric stroke and underwent emergent CAS (mean interval from stroke symptom onset to CAS: 10.8 ± 8.8 h; range, 2.5–20 h), and the remaining 15 patients had non-disabling stroke or TIA and underwent scheduled CAS (mean interval from stroke symptom onset to CAS: 19.3 ± 25.8 days; range, 7–110 days). Carotid stenosis was found during the preoperative evaluation for a coronary artery bypass graft (CABG) or a hemorrhoidectomy operation in three of six asymptomatic patients, and two with symptomatic subclavian artery stenosis were found during the course of additional vascular evaluation. An assessment of cerebral vascular reserve capacity (VRC) using acetazolamide-activated technetium 99-m hexamethylpropyleneamine oxime brain single-photon emission computed tomography (SPECT) was performed in 17 patients (70.8%, symptomatic: 12 of 18 patients, asymptomatic: five of six patients). Inadequate VRC was observed in 13 patients (76.5%, symptomatic: 12 of 12 patients, asymptomatic: one of five patients). All patients were prescribed dual-antiplatelet agents (75 mg/day clopidogrel with 100 mg/day aspirin) and high-dose atorvastatin (80 mg/day) for at least 7 days before CAS. Loading doses of clopidogrel (300 mg) with aspirin (300 mg) and atorvastatin (80 mg/day) were prescribed for emergency cases. Informed consent was obtained from at least two legal representatives of each patient before CAS and also this study was approved by our institutional review board (IRB).
1977
2.2. Intervention protocol All interventions were performed by one experienced neurointerventionalist with/without a neurologist who was a trained neurointerventionalist. First, the femoral artery was punctured under local anesthesia, and a 6F femoral sheath was placed. Diagnostic four-vessel angiography followed to confirm the exact degree of stenosis and the collateral vessels. Next, the 6F femoral sheath was changed to a 6F shuttle catheter and placed distal to the common carotid artery. An EPD was prepared and navigated through the stenotic segment and placed on distal ICA. When the EPD could not be navigated farther due to a tight stenosis, an exchange length 0.014-in. microguidewire (Transcend 300 Floppy microwire; Boston Scientific, Fremont, CA, USA) was used for navigation and was pre-dilated without distal protection using a 2–3 mm balloon to allow the EPD to cross the stenosis. After installing the EPD, pre-dilatation using a 4–5-mm balloon (Aviator plus PTA balloon; Cordis, Miami Lakes, FL, Ultra-soft SV balloon; Boston Scientific) was performed. The stent was selected according to the ICA course: a closed-cell stent was used in a straight course, and an open-cell stent was used in a curved course. Postdilation of the stent was performed after stent deployment using a 5- or 6-mm balloon in selected patients. Heparinized saline was continuously infused through the shuttle catheter to prevent incatheter thrombosis, and 3000 U bolus heparin was injected before stent deployment. Intravenous (IV) atropine and/or IV dopamine was administered when severe hemodynamic effects (bradycardia, asystole, or hypotension) developed after inflating the balloon. Patients who underwent CAS were monitored in the stroke unit or intensive care unit for 24 h with continuous blood pressure, oxygen saturation, and electrocardiographic monitoring and underwent a neurological examination hourly. We conducted massive blood pressure (Bp) control in patients with poor VRC on preprocedural SPECT to prevent development of cerebral hyperperfusion syndrome (CHS). We maintained a systolic Bp level of 110–120 mmHg during the 24 h after the procedure in those patients. In contrast, 200–250 cc/h massive hydration therapy was performed in cases of hypotension persisting after CAS, using normal saline and/or a volume expander with/without IV dopamine infusion until systolic Bp was >100 mmHg. Follow-up diffusionweighted image (DWI) for detecting procedure-related cerebral infarction was recommended to all patients the day after CAS.
2.3. Follow-up Patients who showed no additional neurological deficits after CAS were usually discharged within 3 days after CAS with 75 mg/day clopidogrel, 100 mg/day aspirin, and 20–40 mg/day atorvastatin. These medications were continued for at least 6 months after CAS. A neurological examination was repeated on the discharge day and the day patients visited the outpatient department. A follow-up vascular evaluation was recommended for all patients at 6 and 12 months after CAS and annually thereafter.
3. Results 3.1. Interventional results Based on four-vessel angiography, eight of 24 patients (33.3%) achieved two criteria, seven patients (29.2%) achieved three criteria, and nine patients (37.5%) achieved all four criteria. Criterion 1 was present in 22 of 24 patients (91.7%), criterion 2 in 17 patients (70.8%), criterion 3 in 18 patients (75%), and criterion 4 in 16 patients (66.7%). Contralateral ICA stenosis >70% was found in five
1978
S. Son et al. / Clinical Neurology and Neurosurgery 115 (2013) 1976–1981
Fig. 1. Actual images of carotid artery stenting (CAS) of a patient with a near occlusion on the left side. (A) Pre-procedural basal extracranial lateral projection angiogram. Note the severe stenosis of the left proximal internal carotid artery (ICA) and poorly visible ICA flow (white arrow). (B) Pre-procedural basal intracranial antero-posterior (AP) projection angiogram. Left middle cerebral artery (MCA) and anterior cerebral artery (ACA) flows are also poorly visible (white arrowhead). (C) Postprocedural extracranial lateral projection angiogram. The Precise stent was successfully inserted into a pre-existing stenotic portion of the proximal ICA, and restoration of ICA flow is visible. (D) Post-procedural intracranial AP projection angiogram. Left ACA and MCA flows were also restored.
patients (20.8%), and two had complete occlusion (median degree of contralateral ICA stenosis: 15 ± 33%; range, 5–100%). Stents were successfully inserted in 23 of 24 patients (95.8%, Fig. 1). We could not navigate into the true lumen in one patient, so the procedure failed (Fig. 2). An EPD was used in 22 of 23 patients (95.7%): FilterWire EZ (Boston Scientific/Target Therapeutics) in 18 (81.8%) and Emboshield (Abbott Vascular, Redwood City, CA, USA) in four (18.2%). Eight of 22 patients needed pre-dilation to pass the EPD (36.4%). Additional pre-dilation of the stenosis to allow stent deployment after installing the EPD was required in all patients, except one patient, who was sufficiently dilated after pre-dilation. A stent was implanted in all patients after angioplasty: Precise PRO RX stent (Cordis) in 11 (47.8%), carotid WallStent (Boston Scientific/Target Therapeutics) in eight (34.8%), and a Protégé RX carotid stent (ev3 Inc., Irvine, CA, USA) in four (17.4%). Additionally, 14 of 23 patients (60.9%) required post-dilation after placing the stent. Transient hemodynamic alterations such as hypotension and bradycardia were observed in some patients during and/or after balloon inflation. Transient bradycardia was recovered by encouraging coughing in all patients. But, hypotension persisted in four patients (17.4%) after the procedure and lasted about 24 h. Three recovered after massive hydration therapy, but one needed an additional IV dopamine infusion. No major vascular access site complications were recorded. The mean total procedural time including four-vessel angiography was 69.4 ± 22.5 min (range, 30–115 min). CHS and post-procedural vascular events occurred in four patients (17.4%), and all developed within 24 h after CAS. CHS occurred in two patients (8.7%): one patient (asymptomatic, assessment of VRC was not done) developed a generalized tonic–clonic (GTC) type seizure after the stent was deployed but recovered completely, whereas another patient (symptomatic, inadequate VRC, CAS performed 15 days after stroke onset) developed aphasia 2 h after the procedure and died due to a ipsilateral intracerebral hemorrhage (ICH) despite evacuation of the hematoma (Fig. 3). Another two patients developed acute myocardial infarction (AMI) after CAS: one patient (symptomatic, assessment of VRC was not done due to emergent CAS) underwent the CABG operation 20 days after CAS, and another patient (symptomatic, inadequate VRC) recovered after medical treatment. Eighteen of 23 patients underwent followup DWI the next day after CAS. As a result, 16 of 18 patients (88.9%) showed one or more focal infarctions, but no clinical symptoms were observed in any patient.
3.2. Follow-up results Twenty of 23 patients (87%) received regular clinical follow-up of at least 6 months. The mean follow-up period was 16.7 ± 9.2 months (range, 6–32 months). Among these, only one patient developed an additional infarction 3 months after CAS, but it was not associated with CAS (symptomatic, CAS to right ICA but infarction occurred on the right pons). Ten of 20 patients (50%) underwent follow-up imaging as recommended in the protocol, and an additional four patients were imaged only once (one at 6 months, three at 12 months). Four of 14 patients (2: Precise, 1: Wall, 1: Protégé) showed mild intimal hyperplasia (<30%) on 12-month follow-up imaging, but no additional intervention was needed in any patient. 4. Discussion The term “carotid artery near occlusion” is rather ambiguous [5,15–17]. Generally, near occlusion of the carotid artery is defined as the presence of severe stenosis in the ICA and decreased perfusion distal to the stenosis, resulting in diminished or absent distal carotid flow [15–17]. Such an appearance has been referred to as a “pseudo-occlusion,” “near occlusion,” or an “angiographic string sign”[5,15–17]. We used the near-occlusion criteria of Fox et al., which were published in 2005 [5]. If a patient had one criterion, the sensitivity and specificity was 90.6% and 84.4%, respectively, and if they had two or more criteria, the sensitivity and specificity were 90.6% and 93.8%. But, specificity increased to 96.9% in patients with three or more criteria, whereas sensitivity decreased to 59.4% and 31.3%, respectively [5]. Thus, we chose “two or more criteria present” for near occlusion. We found six studies about CAS in patients with near occlusion through searches on Pubmed and Google [9–14]. Two studies were conducted at the same institute by the same investigators [9,13]. Thus, we choose the study that contained more patients [13]. All were retrospective observational studies due to the rarity of near occlusion (Table 1) [10–14]. Among them, four studies included only 9–24 patients, as in our study [10–12,14], but the authors reported their 10 years of experience with 116 patients in another study [13]. The procedural and clinical results of CAS in patients with near occlusion were inspiring in that study. In 189 patients from five studies, the technical success rate was 99.5%, and only one patient failed CAS [14]. Additionally, only six patients
S. Son et al. / Clinical Neurology and Neurosurgery 115 (2013) 1976–1981
1979
Fig. 2. Actual images of a patient who underwent a failed left-sided carotid artery stenting (CAS). (A and B) basal extracranial (A) and intracranial (B) pre-procedural anteroposterior (AP) projection angiogram. Angiographic string sign is shown. (C) Extracranial AP projection angiogram during the procedure. Microguidewire and microcatheter cannot pass the stenotic portion of the proximal internal carotid artery (ICA) (black arrow in A).
suffered post-procedural vascular events (3.2%; five patients: TIA [13,14], one patient: cardiac death [10], and additional one patient developed AMI but 21 days after CAS [11]). CAS did not succeed in one patient, and CHS and post-procedural vascular events occurred in four patients in our study. CAS is performed on more than 40 cases annually at our institute, and the neurointerventionalist at our institute has performed more than 300 CAS procedures during the past 10 years. Thus, the failed CAS in one patient was not associated with technical inexperience. This is the first study of CAS in patients with near occlusion with high rates of CHS and post-procedural vascular events. The prevalence of CHS after CAS is quite low. In one study, only 10 CHS cases developed (2.4%) in 417 CAS procedures [18]. In another study, the prevalence was just 1.1% (five of 450 CAS) [19]. But the prevalence in our study was very high at 8.7% (two of 23 CAS).
Actually, we experienced only two cases of CHS in 99 CAS (2.0%) procedures, but both were patients with near occlusion. Fortunately, one patient who presented with GTC-type seizures just after stent deployment recovered completely and showed no neurological sequelae. But the other patient developed fatal ICH and eventually died. The development of CAS-associated ICH is very rare [19–21], and we have never experienced it before or after this patient. It was thought that the most important component of perioperative management to prevent CHS is control of systemic Bp [19–21]. However, Ogasawara et al. reported that poor postoperative Bp control is significantly associated with the development of ICH in patients with CHS after CEA but not CAS [22]. The maximum systolic Bp during and after the procedure in our patient with ICH did not exceed 120 mmHg. Thus, it may be that ICH in patients with CHS, and further more CHS after CAS, would not be prevented by
Fig. 3. Actual angiographic and computed tomography (CT) images of a patient with a fatal intracerebral hemorrhage (ICH) after carotid artery stenting (CAS). Severe stenosis of the proximal portion of the left internal carotid artery (ICA) (A) was successfully treated using a Precise stent (B). The patient developed aphasia with right hemiparesis about 2 h after CAS. A large ICH was observed on the CT image obtained immediately after symptom development (C).
1980
S. Son et al. / Clinical Neurology and Neurosurgery 115 (2013) 1976–1981
Table 1 Comparison of our study with other studies. Author
No. of Pts.
Symptomatic stenosis (%)
Use of EPD (%)
Success rate (%)
CHS (%)
Vascular complications
Follow-up (month)
Ipsilateral stroke recurr
Restenosis
Terada Nikas Barker González Spacek Our study
20 25 9 116 19 24
85 80 100 91 58 75
95 100a 67 79 84 96
100 100 100 100 95b 96
0 0 0 0 0 9
1c 1d None 4e 1f 2
25 12 12 36 6 17
None None 1g 1h None None
1i None None 8j 1k None
Author indicates the first author of each study; CAS, carotid artery stenting; CHS, cerebral hyperperfusion syndrome; EPD, embolic protection device; restenosis, significant restenosis on inserted stent >70% and/or required retreatment by angioplasty; TIA, transient ischemic attack. a 24 of 25 patients received a proximal protection device. One patient received a distal protection device. b Failed in one patient due to failure of guidewire passage through the stenosis. c One patient with chronic renal failure died after hemodialysis the day after CAS. d One patient developed acute myocardial infarction at day 21 after the procedure. e Four patients developed short-lasting ipsilateral TIAs within 15 min after CAS. f One patient developed a TIA during the postoperative hospitalization period. g One patient developed a possible TIA at 3 months after CAS. h Three patients experienced a stroke during follow up, only one of which was on the ipsilateral side. i One patient showed restenosis 6 months after CAS and was retreated with angioplasty. j Five patients showed restenosis >70% before month 6 after CAS, and three were retreated with angioplasty. Three patients showed asymptomatic occlusion. k One patient showed restenosis of >80% on a duplex ultrasound examination 1 month after CAS and was retreated with angioplasty.
strict Bp control only. In a pooled analysis study, CAS-associated ICH was related to technical inexperience (<100 cases), symptomatic lesions, severe stenosis >90%, maximal stenosis located distal to bifurcation, and preexisting cerebral infarction [20]. Our patient had symptomatic near occlusion and preexisting cerebral infarction on the ipsilateral basal ganglia. Additionally, we think that the development of ICH in this patient may have been associated with massive anticoagulation/antiplatelet agent therapy. However, on the prior studies, use of antiplatelet agent/anticoagulation is not associated with ICH after CEA [21] or CAS [19]. The patient suffered a renal infarction due to atrial fibrillation and had taken warfarin 4 months before CAS. The patient was prescribed additional aspirin and clopidogrel with warfarin for the CAS. It is regret that we did not delay the procedure in spite of the international normalized ratio of prothrombin time on the day of the procedure was higher than the recommended level (3.11). Four patients in our study showed persistent hypotension during the 24 h after CAS. Among them, two developed AMI within 24 h after CAS. Both patients revealed three-vessel coronary artery disease on the cardiac work-up. We thought initially that hypotension induced by CAS and excessive cardiac loading due to massive hydration therapy were possible inducing causes of the AMI, but hypotension itself seemed to be more important than excessive cardiac loading. During this study period, additional one patient not included this study (symptomatic, 90% stenosis on left ICA) developed AMI within 24 h after CAS. We performed massive Bp control, but not massive hydration therapy, after CAS due to poor VRC on pre-procedural SPECT. This patient also had three-vessel disease on the cardiac work-up and underwent a CABG operation 10 days after CAS. It is possible that post-procedural vascular event rates among patients with near occlusion who receive CAS are higher than has been recognized. We think that this may be associated with the possibility of high comorbidity from other vascular disease. We suspect hypotension as the main cause of post-procedural AMI. If Bp control is not crucial for preventing CHS, unconditional strict Bp control after CAS might be harmful to some patients. Because coronary heart disease and carotid artery disease share the same risk factors [23], there is a strong possibility of comorbid coronary heart disease in patients with carotid artery stenosis. Actually, a high proportion of patients with three-vessel coronary artery disease have comorbid carotid artery stenosis [24]. None of the patients who suffered from AMI in our study had a history of previous coronary heart disease, and there was no evidence of ischemic heart disease on the
pre-procedural electrocardiogram or echocardiogram, but they had asymptomatic three-vessel coronary artery disease. Thus, it is necessary to conduct a vascular imaging work-up to judge coronary artery status before CAS. Furthermore, proper Bp control according to coronary artery status would prevent the development of AMI after CAS. The long-term follow-up results of CAS in patients with near occlusion were outstanding. Stroke recurrence on the ipsilateral side of CAS has been reported in only two cases in two studies (one: possible TIA at 3 months after CAS [12]; one: stroke at 19 months after CAS [13]). In our study, no patient suffered a stroke on the ipsilateral side, but one patient developed a pontine infarction 3 months after CAS. In another study, the authors reported a very high rate of mortality within 6 months after CAS [14], but no neurological or cardiovascular complications related to CAS were reported in that study, and the causes of death were pneumonia, heart failure, and stroke on the contralateral side [14]. Additionally, restenosis >70% or occlusion of the inserted stent was reported in 10 patients in three studies (nine patients at 6 months [10,13], one patient at 1 month [14]), but all were asymptomatic [10,13,14].
5. Conclusions This study has major limitations, including retrospective nature of the analysis, absence of a control group, small number of patients, and relatively short follow-up. But we verified previous CAS results in patients with a carotid near occlusion and identified CAS as a technically feasible and effective method for preventing stroke by comparing our results with others in the literature. Although a high rate of CHS and post-procedural vascular events were observed in our study, particularly within 24 h after the procedure, these events could be avoided by cautious monitoring during and after the procedure and by conducting an appropriate pre-procedural work up.
Disclosures None.
Conflict of interest None.
S. Son et al. / Clinical Neurology and Neurosurgery 115 (2013) 1976–1981
References [1] North American Symptomatic Carotid Endarterectomy Trial (NASCET) Investigators. Clinical alert: benefit of carotid endarterectomy for patients with high-grade stenosis of the internal carotid artery. National Institute of Neurological Disorders and Stroke, Stroke and Trauma Division. Stroke 1991;22:816–7. [2] Morgenstern LB, Fox AJ, Sharpe BL, Eliasziw M, Barnett HJ, Grotta JC. The risks and benefits of carotid endarterectomy in patients with near occlusion of the carotid artery. Neurology 1997;48:911–5. [3] O’Leary DH, Mattle H, Potter JE. Atheromatous pseudo-occlusion of the internal carotid artery. Stroke 1989;20:1168–73. [4] European Carotid Surgery Trialists’ Collaborative Group. Randomised trial of endarterectomy for recently symptomatic carotid stenosis: final results of the MRC European Carotid Surgery Trial (ECST). Lancet 1998;351: 1379–87. [5] Fox AJ, Eliasziw M, Rothwell PM, Schmidt MH, Warlow CP, Barnett HJ. Identification, prognosis, and management of patients with carotid artery near occlusion. American Journal of Neuroradiology 2005;26:2086–94. [6] Yadav JS. Functional occlusions of the carotid artery (string signs): to treat or not to treat? Journal of the American College of Cardiovascular Interventions 2010;3:305–6. [7] Brott TG, Halperin JL, Abbara S, Bacharach J, Barr JD, Bush RL, et al. ASA/ACCF/AHA/AANN/AANS/ACR/ASNR/CNS/SAIP/SCAI/SIR/SNI S/SVM/SVS guideline on the management of patients with extracranial carotid and vertebral artery disease. Journal of the American College of Cardiology 2011;57:e16–94. [8] CAVATAS Investigators. Endovascular versus surgical treatment in patients with carotid stenosis in the Carotid and Vertebral Artery Transluminal Angioplasty Study (CAVATAS): a randomized trial. Lancet 2001;357: 1729–37. [9] Gil-Peralta A, González A, González-Marcos JR, Mayol A, Boza F, Ruano J, et al. Internal carotid artery stenting in patients with symptomatic atheromatous pseudo-occlusion. Cerebrovascular Disease 2004;17:105–12. [10] Terada T, Tsuura M, Matsumoto H, Masuo O, Tsumoto T, Yamaga H, et al. Endovascular treatment for pseudo-occlusion of the internal carotid artery. Neurosurgery 2006;59:301–9. [11] Nikas DN, Ghany MA, Stabile E, Sorropago G, Saccá S, Favero L, et al. Carotid artery stenting with proximal cerebral protection for patients with angiographic appearance of string sign. JACC: Cardiovascular Interventions 2010;3:298–304.
1981
[12] Barker CM, Gomez J, Grotta JC, Smalling RW. Feasibility of carotid artery stenting in patients with angiographic string sign. Catheterization and Cardiovascular Interventions 2010;75:1104–9. [13] González A, Gil-Peralta A, Mayol A, Gonzalez-Marcos JR, Moniche F, Aguilar M, et al. Internal carotid artery stenting in patients with near occlusion: 30-day and long-term outcome. American Journal of Neuroradiology 2011;32:252–8. [14] Spacek M, Martinkovicova L, Zimolova P, Veselka J. Mid-term outcomes of carotid artery stenting in patients with angiographic strong sign. Catheterization and Cardiovascular Interventions 2012;79:174–9. [15] Berman SS, Devine JJ, Erodes LS, Hunter GC. Distinguishing carotid artery pseudo-occlusion with color-flow Doppler. Stroke 1995;26:434–8. [16] Henderson RD, Eliasziw M, Fox AJ, Rothwell PM, Barnett HJ. Angiographically defined collateral circulation and risk of stroke in patients with severe carotid stenosis. North American Symptomatic Carotid Endartrectomy Trial (NASCET) group. Stroke 2000;31:128–32. [17] Lee DH, Gao FQ, Rankin RN, Pelz DM, Fox AJ. Duplex and color Doppler flow sonography of occlusion and near occlusion of the carotid artery. American Journal of Neuroradiology 1996;17:1267–74. [18] Grunwald IQ, Politi M, Reith W, Krick C, Karp K, Zimmer A, et al. Hyperperfusion syndrome after carotid stent angioplasty. Neuroradiology 2009;5:169–74. [19] Abou-Chebl A, Yadav JS, Reginelli JP, Bajzer C, Bhatt D, Krieger DW. Intracranial hemorrhage and hyperperfusion syndrome following carotid artery stenting: risk factors, prevention, and treatment. Journal of the American College of Cardiology 2004;43:1596–601. [20] Kang HS, Han MH, Kwon OK, Kwon BJ, Kim SH, Oh CW. Intracranial hemorrhage after carotid angioplasty: a pooled analysis. Journal of Endovascular Therapy 2007;14:77–85. [21] Ouriel K, Shortell CK, Illig KA, Greenberg RK, Green RM. Intracerebral hemorrhage after carotid endarterectomy: incidence, contribution to neurologic morbidity, and predictive factors. Journal of Vascular Surgery 1999;29:82–7. [22] Ogasawara K, Sakai N, Kuroiwa T, Hosoda K, Iihara K, Toyoda K, et al. Japanese society for treatment at neck in cerebrovascular disease study group. Intracranial hemorrhage associated with cerebral hyperperfusion syndrome following carotid endarterectomy and carotid artery stenting: retrospective review of 4494 patients. Journal of Neurosurgery 2007;107:1130–6. [23] Wilson PW, D’Agostino RB, Levy D, Belanger AM, Silbershatz H, Kannel WB. Prediction of coronary heart disease using risk factor categories. Circulation 1998;97:1837–47. [24] Tanimoto S, Ikari Y, Tanabe K, Yachi S, Nakajima H, Nakayama T, et al. Prevalence of carotid artery stenosis in patients with coronary artery disease in Japanese population. Stroke 2005;36:2094–8.