Tae Hong Lee, MD, Kyung Pil Park, MD 2, Chang Hwa Choi, MD 3, Hak Jin Kim, MD, Chang Won Kim, MD

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1 Case Report Urgent Recanalization Using Stents for Acute Internal Carotid Artery Occlusion in Progressive Stroke Patients with Contralateral Chronic Carotid Occlusion Tae Hong Lee, MD, Kyung Pil Park, MD 2, Chang Hwa Choi, MD 3, Hak Jin Kim, MD, Chang Won Kim, MD The prognosis of symptomatic bilateral internal carotid artery occlusion is extremely poor. To our knowledge, there are few reports regarding the proper management of this catastrophic event. We present two cases of progressive stroke with acute internal carotid artery occlusion and contralateral chronic carotid occlusion, who were treated by urgent recanalization using stents. In two cases, complete recanalization was achieved and the clinical outcomes were favorable. We suggest that early endovascular treatment using stents may salvage the occluded vessel and may also offer a more successful clinical outcome. Further study will be necessary in order to define the proper management of this catastrophic event. Key Words : Arterial occlusive disease; Internal carotid artery thrombosis; Cerebral revascularization; Stent Reestablishing cerebral blood flow in a timely fashion during an acute stroke has been shown to be efficacious in improving patient outcomes (1, 2). Partial or complete occlusion of the internal carotid artery (ICA) is a familiar consequence of severe atherosclerosis as seen in the elderly. Complete obstruction of both ICAs is rare. The rapid onset of bilateral ICAs occlusion would be expected to bring about devastating neurological sequelae and probably not be compatible with survival unless it could be treated (3). However, to 1 Department of Diagnostic Radiology, Pusan National University Hospital, Pusan; 2 Department of Neurology, Pusan National University Hospital, Pusan; 3 Department of Neurosurgery, Pusan National University Hospital, Pusan, Republic of Korea. Received May 2, 2006; accepted after revision July 7, Correspondence to: Tae Hong Lee, MD, Department of Diagnostic Radiology, Pusan National University Hospital 10, 1-Ga, Ami-dong, Seo-gu, Pusan , Republic of Korea Tel Fax drcello@pusan.ac.kr Neurointervention 2006;1:76-82 our knowledge, reports regarding the proper management of this catastrophic event are uncommon. We present two cases of successful recanalization using stents for acute ICA occlusion in progressive stroke patients with contralateral chronic ICA occlusion. CASE REPORTS Case 1 A 46-year-old right-handed man presented with left hand numbness, especially in the fourth and fifth fingers. The subjective weakness of the left hand had persisted for a month. There were no other abnormalities on initial neurologic examination. MR diffusion images (Sonata; Siemens, Germany) showed acute infarction in the watershed zones of the right ICA territories (Fig. 1A). MR angiography (MRA) revealed occlusion of the right proximal ICA and focal severe stenosis of the left distal ICA (Fig. 1B). After three 76 Neurointervention 1, August 2006

2 Urgent Recanalization Using Stents for Acute Internal Carotid Artery Occlusion in Progressive Stroke Patients with Contralateral Chronic Carotid Occlusion A B C D E F G H I Fig. 1. Case 1 with acute left ICA and chronic right ICA occlusion. A and B. MR diffusion (A) and angiography (B) images show the acute infarction in the watershed zones of the right ICA territories, occlusion of the right ICA (thin arrow), and focal severe stenosis of the left cavernous ICA (thick arrow). C and D. After aggravation of the ischemic symptoms, the MR diffusion images revealed the progression of acute infarction in bilateral ICA territories. E. Anterior oblique view of the right CCA angiogram shows complete occlusion (arrow) of the right proximal ICA with a blunted end, suggesting chronic occlusion. F and G. Lateral views of the left CCA angiogram show the tapering occlusion (F, arrow) of the left proximal ICA and distal ICA collateral flow (G, arrow) from the ophthalmic artery. H. Anterior view of the right VA angiogram demonstrates that bilateral ICAs are supplied with collaterals through the posterior communicating arteries. I. After deployment of two self-expandable stents (arrows), the lateral magnified radioscopic view reveals partial recanalization of the cervicopetrous ICA. Neurointervention 1, August

3 Tae Hong Lee, et al. J K L M N O Fig. 1. J. Three additional balloon-expandable coronary stents are successfully deployed on the lateral magnified radioscopic view. K. After angioplasty with five stents, the occluded left ICA was successfully recanalized on the lateral view of the left CCA angiogram. L. Anteroposterior view of the left ICA angiogram immediately after recanalization reveals antegrade left ICA flow and sufficient collaterals via the anterior communicating artery to the side of the contralateral ICA occlusion. M-P. On the three-month follow-up angiogram of the left ICA, there is increased flow in bilateral ICAs, decreased collaterals from the posterior circulation, and no in-stent restenosis. P days, the patient was admitted to the emergency department with dysarthria and mild motor weakness of his left upper arm. His National Institutes of Health Stroke Scale (NIHSS) score was 2. MR diffusion images showed acute infarction in the watershed zones of bilateral ICAs territories. After eight hours, the patient presented with decreased mentality, global aphasia, gaze preference to the left side, and right hemiparesis. At this time, his NIHSS score was 15 and MR diffusion images 78 (Fig. 1C & 1D) showed the progression of acute infarction. Digital subtraction angiography (Multistar; Siemens, Germany) performed 11 hours after deterioration of his symptoms demonstrated the bilateral proximal ICAs occlusion. The right ICA occlusion (Fig. 1E) was presumed to be chronic because of the bluntended occlusion and sufficient collaterals through the posterior circulation, which reconstituted the right ICA territory. The left proximal ICA (Fig. 1F) was occluded Neurointervention 1, August 2006

4 with a smoothly tapered end. Because a previous MRA showed severe stenosis of the left distal ICA and the left common carotid artery (CCA) angiogram showed retrograde intracerebral flow through the ophthalmic artery (Fig. 1G), the cause of the left ICA occlusion was considered to be atherothrombosis. Right vertebral angiogram showed that the posterior circulation supplied both ICAs territories (Fig. 1H). Owing to the severity of the clinical stroke, the extent of the thrombus and the long symptom duration over the time window for thrombolysis, we decided to perform mechanical recanalization using stents from the proximal ICA to the distal ICA rather than chemical thrombolysis. The patient received heparin intravenously throughout the procedure in order to maintain an activated clotting time (ACT) between 200 and 250s. An 8F guiding catheter (Envoy; Cordis Corporation, USA) was advanced to the left CCA, and it was connected to a continuous saline flush. Considering the possibility to produce embolic debris from the long occluded segment, we maintained the saline flush rapidly in order for the embolic debris to flow to the external carotid artery (ECA). A in microwire (Transend; Boston Scientific Corporation, USA) was placed into the distal ICA crossing the occluded segment. Then two self-expandable stents (8 56-mm Carotid Wallstent; Boston Scientific Corporation, USA; 6 40-mm SelfX Xpert; Jomed, Netherlands) and three coronary balloon-expandable stents (4 26-mm, 4 23-mm, and 4 19-mm Flexmaster; Jomed, Netherlands) were advanced over the microwire and positioned across the stenosis in order (Fig. 1I & 1J). Before the deployment of a fifth stent, a 10-mg abxicimab (Reopro; Centocor, Netherlands) was injected intra-arterially to prevent thromboembolic complications. The final left ICA angiogram showed complete recanalization of the occluded ICA, antegrade flow to the left anterior and middle cerebral arteries (ACA and MCA), and right ICA territorial flow through the anterior communicating artery (Fig. 1K & 1L). After the procedure, hemostasis of the femoral artery was achieved using an occlusion device (Angioseal, St. Jude Medical, Belgium). The patient was medicated daily with 100 mg aspirin and 75 mg clopidogrel (Plavix; Sanofi-Synthelabo, Korea) indefinitely; 2850 IU/0.3 ml of low-molecular-weight nadroparin calcium (Fraxiparine; Sanofi-Synthelabo, Korea) were also administered subcutaneously twice or three times a day for at least three days. The patient had progressive clinical improvement after recanalization of the left occluded ICA. On the second postprocedural day, his mental state became alert and his motor weakness was mildly improved. On the tenth postprocedural day, his NIHSS score was 8 and his global aphasia had begun to improve. On the 24th day, the patient was discharged without significant neurologic deficit except for disturbed memory recall. On the three-month clinical and angiographic follow-up, there had been no further ischemic events or in-stent restenosis (Fig. 1M- 1P). Case 2 A 57-year-old right-handed man was referred to our facility for further treatment of right motor weakness and aphasia. MR T2-weighted images from the referring institution showed right chronic cerebral infarction and focal high signal intensities in the watershed zones of the left basal ganglia and frontal lobe. Seven hours after arrival at our hospital, his symptoms progressed to right hemiparesis and global aphasia. At that time, his NIHSS score was 13. MR diffusion images showed progression of the acute infarction. MRA revealed occlusion of the bilateral proximal ICA. Emergent cerebral angiography confirmed the total occlusion of the right proximal ICA with a blunt end, suggesting a chronic occlusion and approximately a 3-mm segmental occlusion of the left ICA just proximal to the ophthalmic artery (Fig. 2A- 2C). The visualized left proximal ICA was narrow and its diameter was barely maintained by the tentorial arterial flow. The territories of the both ICAs were supplied by collateral flow from posterior circulation and from the left ophthalmic artery. Because the cerebral infarction progressed despite medical treatment and the time window from the onset of the clinical symptoms to the beginning of endovascular treatment was more than six hours, we decided to perform mechanical recanalization. Under local anesthesia, a 6F Envoy guiding catheter was positioned in the left cervical ICA. The occluded segment was crossed with a in microwire. A 1.5-mm diameter, 11-mm long coronary balloon (Maestro, Jomed, Netherlands) was then advanced over the microwire into the occluded portion of the left cavernous ICA. After confirming the position of the pre-dilatation balloon in the lesion, the balloon was inflated to nominal pressure (8 atm). With the wire in place, the balloon catheter was withdrawn. Then a 3.0-mm diameter, 19-mm long balloon-expandable coronary stent (Flexmaster) was advanced over the microwire and positioned across the lesion using a roadmapping technique. After confirming the correct stent positioning under the road-mapping image and external markings, the stent was deployed by inflating the Neurointervention 1, August

5 Tae Hong Lee, et al. A B C D E F Fig. 2. Case 2 with acute left cavernous ICA and chronic right proximal ICA occlusion. A. Lateral angiogram of the left ICA shows complete occlusion (arrow) just distal to the tentorial branches. B and C. Lateral (B) and anteroposterior (C) views of the left CCA arteriogram show distal ICA flow through the ophthalmic artery (black arrow). The distal end (white arrow) of the occlusion segment of the left ICA is proximal to the ophthalmic artery. D. Lateral magnified radioscopic view demonstrates that the balloon-mounted stent is deployed by inflating the balloon (arrow) E. Lateral magnified angiogram of the left ICA shows smooth dilatation of the occluded segment (arrow) and antegrade ophthalmic flow. F. Anteroposterior view of the left ICA angiogram immediately after stenting reveals antegrade left ICA flow and sufficient collaterals via the anterior communicating artery to the side of the contralateral ICA occlusion. balloon to 15 atm (Fig. 2D). The lesion was not fully dilated by ballooning less than 15 atm. Therefore the cause of the left ICA occlusion was considered as the atherothrombosis. The left ICA angiogram immediately after stent placement showed complete recanalization of the occluded segment (Fig. 2E). After 10 minutes, the ICA angiogram revealed acute in-stent thrombosis, which was dissolved with an intra-arterial injection of abciximab through the guiding catheter. Final angiography revealed a patent ICA, antegrade filling of the ACA and MCA, and no remaining in-stent thrombus (Fig. 2F). After the procedure, the patient was medicated daily with 100 mg aspirin and 75 mg clopidogrel indefinitely and experienced progressive clinical improvement. On the 5th days, NIHSS score was 6 and his global aphasia 80 began to improve. On the two-month clinical and angiographic follow-up, there had been no further ischemic events or in-stent restenosis. DISCUSSION In 1954, Fisher described patients with bilateral ICA occlusion who presented with coma and bilateral neurological deficit resembling thrombosis of the basilar artery (4). Recently, Kwon et al (3) reported six patients with bilateral ICA occlusion who presented with sudden loss of consciousness, quadriplegia, and internally intact brainstem reflex. Five patients underwent intra-arterial thrombolysis but failed to recanalize the occluded ICA. They soon lost brainstem reflex and died within three days. Neurointervention 1, August 2006

6 The presumptive causes of acute ICA occlusion were atherothrombosis, cardiac embolism, or dissection of cervical arteries following head trauma (3, 5). In the past, occlusion of both carotid arteries was performed deliberately in cases of radical neck dissection for carcinoma (6). In our cases, acute occlusion of the ICA was present and had an appearance consistent with thrombotic occlusion secondary to atherosclerosis. These patients did not have embologenic cardiac diseases or trauma history. It is noteworthy that the ICA on one side was occluded with a round blunted end, suggesting chronic occlusion. It may therefore be suggested that in the presence of a preceding asymptomatic or symptomatic occlusion of one ICA, an additional occlusion of the opposite ICA produced massive infarcts in both ICAs territories (3). However, occlusion of bilateral ICAs does not necessarily produce massive, bilateral infarction. According to a previous study (7), a majority of the patients with bilateral ICA occlusion had only mild neurologic deficits. In addition, there was a case of a young man with complete obstruction of bilateral ICAs. He was followed by noninvasive studies and in the subsequent year showed marked neurological improvement (8). The methods to restore blood flow to ischemic human brain are mechanical recanalization or chemical thrombolysis using fibrinolytics such as tissue plasminogen activator (tpa) or urokinase, The former appears to shorten the time to thrombus dissolution and may have fewer hemorrhagic effects, however, it has the potential for injury to the vessel, hemolysis, and distal embolization. To the contrary, the latter method has seldom produced vessel injury and distal embolization but it is somewhat time-consuming and has increased risk of intracranial hemorrhage (1, 9). In contrast to intracranial thrombolysis, reestablishing ICA patency usually entails large clot volume removal, the bulk of which is usually fresh clot secondary to in situ thrombosis with a high-grade carotid stenosis. Chemical thrombolysis is less than ideally suited for this purpose because the prolonged infusion times and high dose of fibrinolytics necessary for lysis of a large clot burden may increase the hemorrhagic complication (10). Moreover, the risk of embolizing plaque fragments into the major intracranial arteries such as the ACA or MCA may be increased. In our cases, the reasons we performed mechanical recanalization using stents instead of intra-arterial thrombolysis or only balloon angioplasty, were as follows. We worried about hemorrhagic complications related to the fibrinolytics because the time interval from the onset of the clinical symptoms to the beginning of endovascular treatment was more than 6 hours and a high dose of fibrinolytics would be needed for thrombolysis of the large clot volume. Secondly, we thought that the risk of the clot embolism to the ACA or MCA might be increased when the occluded ICA was partially recanalized with fibrinolytic agents or only by balloon angioplasty. In summary, the prognosis of symptomatic bilateral ICA occlusion is extremely poor. If ICA is occluded acutely in patients with or without contralateral chronic ICA occlusion, early endovascular treatment may salvage the vessel and offer a better clinical outcome. However, further study will be necessary in order to identify the proper management of this catastrophic event. References 1. The National Institute of Neurological Disorders and Stroke rt-pa Stroke Study Group. Tissue plasminogen activator for acute ischemic stroke. N Engl J Med 1995;333: Furlan A, Higashida R, Wechsler L, Gent M, Rowley H, Kase C, et al. Intra-arterial prourokinase for acute ischemic stroke. The PROACT II study: a randomized controlled trial. Prolyse in Acute Cerebral Thromboembolism. JAMA 1999;282:2003? Kwon SU, Lee SH, Kim JS. Sudden coma from acute bilateral internal carotid artery territory infarction. Neurology 2002;58: Fisher M. Occlusion of carotid arteries: further experiences. Arch Neurol Psychiatry 1954;72: Gouny P, Nowak C, Smarrito S, Fadel E, Hocquet-Cheynel C, Nussaume O. Bilateral thrombosis of the internal carotid arteries after a closed trauma. Advantages of magnetic resonance imaging and review of the literature. J Cardiovasc Surg (Torino) 1998;39: Catlin D. A case of carcinoma of the larynx surviving bilateral carotid ligation. Ann Surg 1960;152: Catala M, Rancurel G, Raynaud C, Leder S, Kieffer E, Koskas F. Bilateral occlusion of the internal carotid arteries: analysis of a series of 19 patients. Rev Neurol (Paris) 1995;151: Sadun AA, Sebag J, Bienfang DC. Complete bilateral internal carotid artery occlusion in a young man. J Clin Neuroophthalmol 1983;3: Greenberg RK, Ouriel K, Srivastava S, Shortell C, Ivancev K, Waldman D, et al. Mechanical versus chemical thrombolysis: an in vitro differentiation of thrombolytic mechanisms. J Vasc Interv Radiol 2000;11: Bellon RJ, Putman CM, Budzik RF, Pergolizzi RS, Reinking GF, Norbash AM. Rheolytic thrombectomy of the occluded internal carotid artery in the setting of acute ischemic stroke. AJNR Am J Neuroradiol 2001;22: Neurointervention 1, August

7 2006; 1: Key Words : Arterial occlusive disease; Internal carotid artery thrombosis; Cerebral revascularization; Stent 82 Neurointervention 1, August 2006

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