- Email: [email protected]
Estimation and Recanalization of Chronic Occluded Internal Carotid Artery: Hybrid Operation by Carotid Endarterectomy and Endovascular Angioplasty
Original Article
Estimation and Recanalization of Chronic Occluded Internal Carotid Artery: Hybrid Operation by Carotid Endarterectomy and Endovascular Angioplasty Bing Liu, Wei Wei, Yongli Wang, Xinyu Yang, Shuyuan Yue, Jianning Zhang
OBJECTIVE: Proper treatment for chronic occluded internal carotid artery (ICA) has not been determined. Endovascular recanalization may cause arterial injury and distal embolism. Hybrid recanalization for chronic occluded ICA was performed, and its safety and effectiveness were estimated.
-
METHODS: From March 2011 to March 2017, 21 patients were treated by hybrid recanalization with >1 year of follow-up. The ICA was totally occluded from the cervical segment to the cavernous, ophthalmic, or supraclinoid segment. Clinical characteristics, treatment strategy, recanalization rate, and main adverse events were reviewed retrospectively.
was occluded by the plaque at the ophthalmic or supraclinoid segment with the thrombus retrograde to the cervical segment.
-
RESULTS: Initial recanalization was achieved in 15 patients (71.4%). Successful revascularization was more likely if the ICA was occluded with the plaque at the carotid bifurcation and the thrombus anterograde to the cavernous segment. There was no carotid dissection or intracranial hemorrhage. There were no new postprocedural neurologic deficits. Among 14 patients who underwent successful recanalization with follow-up, 1 patient had a repeat occlusion and another experienced about 50% restenosis.
-
CONCLUSIONS: Hybrid recanalization by carotid endarterectomy and arterial angioplasty is a safe treatment method for chronic totally occluded ICA. Recanalization was more likely to be successful if the ICA was occluded by the plaque at the carotid bifurcation with the thrombus anterograde to the cavernous segment than if the artery
-
INTRODUCTION
S
evere carotid artery stenosis is the most common cause of transient ischemic attack or stroke. Carotid endarterectomy (CEA) is effective for preventing stroke and has been accepted for >20 years as the primary treatment for patients with severe carotid artery stenosis. In recent years, these patients have also been treated with carotid artery stenting using an embolic protection device with noninferior results compared with CEA.1-3 Chronic internal carotid artery (ICA) occlusion is a relatively uncommon but important cause of transient ischemic attack and cerebral infarction.4 The annual rate of nonfatal stroke was reported to be 3%e10% in adults >60 years old with carotid occlusion.5 Recurrent ischemic events were seen in about 25% of patients with symptomatic carotid occlusion. The best treatment for chronic carotid artery occlusion has not been determined. Although extracranial-intracranial (EC-IC) artery bypass was performed for several decades, it failed to yield clinical benefit. A multicenter randomized trial comparing medical therapy alone with EC-IC bypass surgery added to best medical therapy showed no superiority of EC-IC bypass procedure compared with medical therapy.6 The Carotid Occlusion Surgery Study trial was stopped prematurely also as a result of lack of superiority.7 Endovascular recanalization has been introduced in recent years for the management of occluded carotid artery.8-10 Several technical problems must be considered during endovascular
Key words Carotid artery stenting - Carotid endarterectomy - Chronic occlusion - Hybrid operation - Internal carotid artery - Recanalization
Department of Neurosurgery, Tianjin Medical University General Hospital, Tianjin Neurological Institute, Tianjin, China
Abbreviations and Acronyms CEA: Carotid endarterectomy EC-IC: Extracranial-intracranial ICA: Internal carotid artery
Available online: www.sciencedirect.com
-
WORLD NEUROSURGERY -: e1-e9, - 2018
To whom correspondence should be addressed: Bing Liu, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.08.104 Journal homepage: www.WORLDNEUROSURGERY.org 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
www.WORLDNEUROSURGERY.org
e1
ORIGINAL ARTICLE BING LIU ET AL.
e2
www.SCIENCEDIRECT.com
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.08.104
ORIGINAL ARTICLE BING LIU ET AL.
recanalization procedures, including issues related to protecting the cerebral circulation from distal embolism, how to determine the true lumen, and how to successfully traverse a long occlusive lesion without incurring additional arterial injury, which remains technically challenging.11,12 Endovascular devices may traverse the false lumen in the occluded segment and induce artery dissection and pseudoaneurysm formation. Furthermore, the recanalization procedure cannot be achieved in this situation. In chronic cases, the carotid artery was usually occluded by atherosclerotic plaque and subsequent extensive thrombus. In the plaque segment, the true lumen was usually difficult to determine and traverse with endovascular devices. However, it was easier in the thrombus segment. The plaque at the carotid bifurcation could be removed by the endarterectomy, and then the true lumen in the ICA could be distinguished. Thus, recanalization of the occluded carotid artery may be achieved using combined endarterectomy and endovascular carotid angioplasty. From March 2011 to March 2017, 21 patients with symptomatic chronic totally occluded ICA were treated by hybrid recanalization, which included CEA and simultaneous endovascular angioplasty. The clinical characteristics, treatment strategy, and outcomes at 30 days were analyzed, and follow-up was conducted for >1 year. MATERIALS AND METHODS This study protocol was examined and approved by the Ethical Committee of Tianjin Medical University, an academic medical center. Patients with symptomatic chronic occluded ICA were recruited to be treated by the hybrid operation. All the benefits and disadvantages of the operation were carefully explained to the patients and their relatives, and the wishes of the patients were taken into considered in the selection of treatment. The operation was performed with the informed consent of the patients and their relatives. Data Collection Clinical characteristics, treatment strategy, and outcomes of patients who were treated from March 2011 to March 2017 with >1 year of follow-up were reviewed retrospectively. Patients were recruited for this research using specific criteria, as follows: 1) Patients had ICA occlusion extending from the cervical segment to the intracranial segment. 2) The intracranial ICA was patent with anastomotic branches from the external carotid artery usually via the ophthalmic artery, or from the vertebrobasilar artery via the posterior communicating artery, or from the contralateral ICA via the anterior communicating artery. 3) Patients had an ischemic attack (modified Rankin Scale score <3) or amaurosis or reduced cerebral infusion. 4) Patients were excluded if 1 of the following conditions was present: nonatherosclerotic carotid artery disease; history of bleeding disorder; renal insufficiency; congestive heart failure; or contraindication to heparin, aspirin, or clopidogrel. 5) If
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
the patient had unstable angina or acute myocardial infarction, the treatment was to be given at least 30 days later, when angina or myocardial infarction was controlled. 6) Older patients, especially patients >75 years old, with contralateral laryngeal nerve palsy, previous radical head/neck surgery or radiation therapy to the neck, or poor neurologic condition (modified Rankin Scale score 3) did not receive the therapy. Preoperative Evaluation A thorough medical and detailed cardiology evaluation was carried out for all patients. Medical therapy for comorbidities, such as hypertension, diabetes mellitus, and dyslipidemia, was optimized. All patients underwent digital subtraction angiography to confirm complete occlusion of the ICA, the occluded segment, and the established collateral filling to the ipsilateral intracranial ICA. Single-photon emission computed tomography was performed in all patients to evaluate cerebral perfusion. Treatment Procedure All authors were trained and specialized in CEA, endovascular carotid angioplasty, or both. The operation was performed by at least 2 authors, with one a specialist in CEA and the other a specialist in endovascular therapy. The procedure was supervised by another author to confirm whether or not the recanalization was successful. Patients usually underwent the procedure 3 weeks after the onset of ischemic events. A dual antiplatelet regimen with aspirin (100 mg) and clopidogrel (75 mg) was started at least 7 days before the procedure. The operation was performed under general anesthesia with continuous electroencephalogram monitoring. The procedure was performed in the hybrid operating room, in which both the open surgery and the endovascular procedure could be carried out simultaneously. The patients underwent placement of a 6-F sheath introducer via the percutaneous transfemoral route. A longitudinal incision parallel to the medial aspect of the sternocleidomastoid muscle was made to explore the common, internal, and external carotid arteries and superior thyroid artery. The ICA was explored as far as possible. Heparin (4000 IU) was given intravenously 5 minutes before the artery clamping. The common, external carotid, and superior thyroid arteries were clamped. A linear longitudinal incision was made first in the common carotid artery, and the atherosclerotic plaque could be seen at the carotid bifurcation. The incision was then extended distally to the ICA to the distal end of the plaque. The thrombus mostly adhered to the atherosclerotic plaque in the lumen and extended distally along the ICA to the intracranial segment. After removal of the plaque, the true lumen of the ICA could be determined. Then the endovascular equipment was used to enter the true lumen and advance the occluded segment through the
Figure 1. Successful recanalization of totally occluded internal carotid artery to cavernous segment (group A). (A) A 60-year-old man presented with left ischemic stroke, as shown on diffusion-weighted imaging performed 4 weeks before the operation. (B and C) The left internal carotid artery was totally occluded from the cervical segment to the cavernous segment (group A). (D) The right carotid artery provided blood flow via the anterior communicating artery to left anterior and middle cerebral arteries. (E) Atherosclerotic plaque and extensive thrombus are shown at the carotid bifurcation. (F) The plaque was removed. (G) After carotid endarterectomy, the true lumen of the internal carotid artery was determined. (H) Through the carotid incision, the thrombectomy was carried out by Fogarty balloon catheter. (I) The thrombus that was removed from the internal carotid artery is shown. (J) Successful recanalization of the left internal carotid artery was confirmed by angiography after closure of the cervical incision through the femoral route.
WORLD NEUROSURGERY -: e1-e9, - 2018
www.WORLDNEUROSURGERY.org
e3
ORIGINAL ARTICLE BING LIU ET AL.
e4
www.SCIENCEDIRECT.com
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.08.104
ORIGINAL ARTICLE BING LIU ET AL.
incised cervical segment, including a 0.035-inch standard guidewire with the support of a intracranial support catheter (Navien; Medtronic, Minneapolis, Minnesota, USA) and a 0.014-inch guidewire in combination with a microcatheter (Echelon 10; Medtronic). After successfully traversing through the occluded segment and reaching the intracranial patent segment, the Solitaire FR stent (Medtronic) or Fogarty balloon catheter (Edwards Lifesciences Corp., Irvine, California, USA) was advanced into the intracranial patent segment and was withdrawn to move the thrombus out from the incision of the cervical carotid artery. This procedure was performed 2 or 3 times. If the larger thrombus, rather than debris, came out of the incision, robust backflow of blood from the ICA could be seen. The ICA clamp was then placed distal to the incision. If the guidewire and catheter could not traverse through the occluded segment or no blood backflow came out from the incision, the recanalization was not unsuccessful. The closure of the carotid artery was performed with a 6-0 polypropylene suture. After closing the cervical incision, the patency of the treated ICA and the formation of carotid dissection and pseudoaneurysm were confirmed by angiography obtained through the transfemoral route. If there was remnant stenosis (>50%) at the cavernous or petrous segment, the 3.0-mm to 4.0mm balloon (Gateway; Boston Scientific, Marlborough, Massachusetts, USA) was advanced to the remnant stenosis site and inflated to normal pressure. The balloon catheter was then removed, and the intracranial stent delivery catheter (Apollo; MicroPort Medical Co., Ltd., Shanghai, China) was placed across the stenotic lesion, and the stent was deployed. On completion of the procedure, the 6-F sheath was removed, and hemostasis was obtained with a vascular closure device (Exoseal; Cordis Corporation, Miami Lakes, Florida, USA). Blood pressure was strictly controlled during the entire procedure. If the occluded carotid artery was successfully recanalized, the postprocedural mean arterial pressure was kept at 10%e20% below baseline to prevent cerebral reperfusion injury. All patients received both aspirin and clopidogrel for at least 3 months after the procedure, and aspirin was continued thereafter. The patients undergoing stent placement received low-molecular-weight heparin for 3 days after the procedure.
Outcome Assessment All patients were divided into 3 groups according to the distal site of the occluded ICA. If the ICA was occluded extending to the cavernous segment as demonstrated by the collateral blood flow, patients were allocated to group A; patients with occlusion extending to the ophthalmic segment were allocated to group B; and patients with occlusion extending to the supraclinoid segment were allocated to group C. Outcomes evaluated included revascularization of the occluded ICA, intracranial hemorrhage, carotid artery dissection and pseudoaneurysm formation, death from any
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
cause, and ipsilateral and contralateral major stroke within 30 days after the procedure. The main local complications, which included cervical or groin hematoma, infection, femoral pseudoaneurysm or arteriovenous fistula at the puncture site, lower limb arterial occlusion or thrombosis, and cranial nerve palsy, were also noted. Follow-up was performed for all patients, and long-term outcomes were assessed on death due to the treated carotid artery, ipsilateral major stroke, and target vessel revascularization between 30 days and 1 year. Target vessel revascularization was evaluated by Doppler 7 days after the procedure and then by Doppler or computed tomography angiography at 6 months and 1 year after the procedure.
RESULTS Clinical Characteristics From March 2011 to March 2017, 21 patients with symptomatic chronic occluded ICA were treated by hybrid recanalization. The mean age of all patients was 56 years (range, 41e66 years); 19 patients (90.5%) were men. Twenty patients presented with symptoms of cerebral infarction or transient ischemic attack, among whom 3 patients also had retinal infarction. The other patient did not have cerebral ischemia, only retinal infarction derived from the occluded carotid artery. All patients had reduced cerebral perfusion on the occluded side compared with the contralateral side. Although most patients had hypertension, diabetes mellitus, or coronary artery disease, no patients had severe systemic comorbidities, such as acute myocardial infarction, chronic obstructive pulmonary disease, or kidney dysfunction.
Recanalization Rate Initial recanalization was achieved in 15 patients (71.4%) with smooth flow through the entire ICA and residual stenosis <50%. In group A (n ¼ 13 patients), 12 patients underwent successful recanalization (Figure 1). In the patient with failed recanalization, after the incision of the carotid artery, an obvious plaque was found at the bifurcation. However, the endovascular devices could not traverse through the petrous segment after the removal of the plaque. In group B (n ¼ 6 patients), 3 patients had successful carotid artery revascularization. None had retinal infarction. However, the other 3 patients who had unsuccessful recanalization had retinal infarction. In these patients, no plaque was located at the carotid bifurcation, but thrombus was detected. After removal of the thrombus in the cervical segment of the ICA, endovascular devices could be advanced to the cavernous segment but could not traverse through the ophthalmic segment (Figure 2). In group C (n ¼ 2 patients), no recanalizations succeeded. The endovascular devices could not traverse through the occluded supraclinoid segment (Figure 3).
Figure 2. Unsuccessful recanalization of internal carotid artery occluded to ophthalmic segment and thrombus at cervical segment (group B). (A) A 53-year-old man presented with symptoms of ischemic stroke as shown on diffusion-weighted imaging and transient amaurosis of the left eye. (B) The left internal carotid artery was totally occluded from the cervical segment, not from the bifurcation, with a stumplike appearance. (C) The intracranial internal carotid artery was patent from the ophthalmic segment, with the anastomotic branches from the ophthalmic artery. (D) The thrombus, not the plaque, was found at the carotid artery incision. (E) The microcatheter and guidewire could not traverse through the ophthalmic segment (group B), and recanalization could not be achieved successfully.
WORLD NEUROSURGERY -: e1-e9, - 2018
www.WORLDNEUROSURGERY.org
e5
ORIGINAL ARTICLE BING LIU ET AL.
e6
www.SCIENCEDIRECT.com
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.08.104
ORIGINAL ARTICLE BING LIU ET AL.
Stents were placed in 7 of 15 patients with recanalization (Figure 4). Postprocedural Complications No patients died within 30 days after the procedure. There was no thrombogenesis and no intracranial hemorrhage during the procedure. There was no carotid dissection or pseudoaneurysm formation. No intracranial hemorrhage occurred after the carotid artery revascularization. No major stroke occurred after the operation, and no new postprocedural neurologic deficits were observed in any patient. Hyperperfusion syndrome was observed in 2 patients, with symptoms of headache that disappeared a few days later under the control of blood pressure. One patient had mild groin hematoma, but there were no patients with femoral pseudoaneurysm or arteriovenous fistula at the puncture site or lower limb arterial thrombosis. Three patients had moderate cervical hematoma but did not require surgical evacuation. Another patient had cervical incision infection. Follow-Up Revascularization of Target Vessel Among the patients who underwent the successful recanalization, 1 patient died of a heart attack 4 months after the operation. The other patients had >1 year of follow-up. During the follow-up period, no patients had ischemic stroke owing to the target vessel. One patient received carotid artery stenting of the collateral ICA owing to stenosis progression. Among these 14 patients, the revascularized carotid arteries in 12 patients were patent without restenosis. In the other 2 patients, the ICA was totally occluded again in 1 patient, and moderate restenosis (approximately 50%) occurred in another. Both patients presented with no symptoms and underwent no further operation and received only enhanced medication. There were no deaths among the patients who underwent unsuccessful recanalization. One patient had recurrent ischemic attack owing to the occluded carotid artery. Another patient had an ischemic stroke on the brainstem because of stenosis of the basilar artery, which did not manifest during the operation. Another patient received CEA of the contralateral carotid artery owing to severe stenosis. DISCUSSION The best treatment for patients with a completely occluded ICA has not been determined. Medical management alone may be inadequate, and revascularization may be beneficial in patients with impaired cerebral perfusion. In our series, all patients were enrolled because of neurologic deficit or objective hemisphere ischemia.
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
Endovascular recanalization of the occluded ICA was an accepted treatment technique for acute stroke, but it was rarely performed beyond the acute phase. There were some choices for the treatment of chronic occluded ICA, such as EC-IC bypass, CEA, or carotid artery stenting for the contralateral carotid artery stenosis if the contralateral carotid artery provided collateral blood flow to the occluded carotid artery and had moderate to severe stenosis. Recanalization of the chronic occluded carotid artery was reported initially by Terada et al.8; a patient underwent successful endovascular recanalization of a chronic occlusion with proximal protection of the carotid artery. Kao et al.13 reported successful in recanalization of 22 chronic ICA occlusions among 30 cases. A major concern in recanalization of a chronic carotid artery occlusion is the possibility of causing a distal embolism as a result of the thrombotic content of embolic debris released during the endovascular device manipulation.14,15 Thus, in endovascular recanalization, the proximal occlusion of the common carotid artery using an occlusion balloon is typically performed to reverse the flow with the goal of minimizing the risk of thromboembolic complications.16 Other important complications associated with endovascular intervention include carotid dissection and pseudoaneurysm formation,11 which have an incidence of up to 6% because of the inability to distinguish between the lumen and arterial wall in the occlusive lesion. In particular, the lesion was composed of plaque with calcification. This kind of lesion was solid, and there was usually almost no lumen. The endovascular devices had difficulty in traversing through it. However, it was easier to pass through the lesion composed of thrombus, which is usually attached to the plaque. Hybrid recanalization of chronic occluded ICA was carried out using a combination of CEA and endovascular angioplasty, which were performed simultaneously. The plaque at the carotid bifurcation and cervical ICA was removed through the incision in the carotid artery. The true lumen was then distinguished, and the endovascular equipment was used to enter the ICA and to pass through the thrombotic segment. This avoided carotid artery injury. If the equipment successfully reached the distal patent segment, it was retrieved from the incision. If the thrombectomy was performed successfully, backflow of the blood was seen, and the thrombus and debris flowed out from the carotid incision. This prevented thromboembolic complications. After closure of the carotid artery and the cervical incision, angiography was performed to confirm the patency of the ICA through the transfemoral route. If there was prominent stenosis in the ICA, carotid angioplasty, with or without stent placement, was performed. In our series, the patients with a totally occluded ICA were treated safely using the hybrid recanalization technique. There was no symptomatic ischemic stroke and no intracranial hemorrhage. Local complications occurred in a few patients. No patients experienced carotid dissection or pseudoaneurysm formation.
Figure 3. Unsuccessful recanalization of internal carotid artery occluded to supraclinoid segment (group C). (A) A 48-year-oldman presented with symptoms of left hemisphere stroke, as shown on diffusion-weighted imaging obtained 4 months prior. (B) Severe stenosis of the supraclinoid segment of the left internal carotid artery is shown on magnetic resonance angiography at that time. (C) The patient had been receiving medication since then. However, he subsequently presented with transient ischemic attack of the right limb. Digital subtraction angiography showed total occlusion of the left internal carotid artery from the cervical segment 4 months later. (D and E) The left intracranial internal carotid artery was patent with anastomosis from the vertebrobasilar artery via posterior communicating artery. Revascularization of the left internal carotid artery failed (group C).
WORLD NEUROSURGERY -: e1-e9, - 2018
www.WORLDNEUROSURGERY.org
e7
ORIGINAL ARTICLE BING LIU ET AL.
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
Figure 4. Successful recanalization with stent implantation. (A) A 63-year-old man with ischemic stroke had a right occluded internal carotid artery from the carotid bifurcation, and the cavernous segment was patent, as demonstrated on digital subtraction angiography. (B) After successful recanalization,
Success of the recanalization procedure depended on passing the guidewire and catheter through the occluded segment. The occlusion of an artery usually originated from the plaque, which arose mainly at the artery bifurcation, and then the thrombus
e8
www.SCIENCEDIRECT.com
angiography showed >50% remnant stenosis on the petrous segment of the right internal carotid artery. (C) The stenosis disappeared after the stent was deployed at the stenosis position. (D) Angiography performed 1 year later showed the internal carotid artery was patent.
extended anterograde or retrograde to the next bifurcation with significant collateral blood flow. It was difficult to traverse the endovascular devices through the plaque, which may induce artery dissection and pseudoaneurysm formation in the chronic
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.08.104
ORIGINAL ARTICLE BING LIU ET AL.
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
occluded segment. However, it was easy to traverse through the thrombus part. If the occlusion originated from the carotid bifurcation and the thrombus extended anterograde to the cavernous segment that was perfused by the collateral blood flow, usually from the ophthalmic artery (group A), successful recanalization was most possible. However, if the plaque was at the ophthalmic bifurcation of the ICA and the thrombus extended retrograde to the cervical bifurcation, where it exhibited an appearance of a tapered stump on the angiogram of the cervical segment (group B), no plaque, but thrombus, was found at the cervical segment, and the guidewire could not usually pass through the plaque at the ophthalmic segment. Recanalization may be unsuccessful, especially in patients with retinal infarction. If the collateral blood flow from the external carotid artery could not anastomose with the ophthalmic segment (group C), the plaque was usually located at the supraclinoid segment. Recanalization mostly could not be done. The anastomotic blood flow was usually from the contralateral carotid artery through the anterior communicating artery or from the vertebrobasilar artery through the posterior communicating artery.
REFERENCES 1. 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;339:1415-1425. 2. Coward LJ, Featherstone RL, Brown MM. Safety and efficacy of endovascular treatment of carotid artery stenosis compared with carotid endarterectomy: a Cochrane systematic review of the randomized evidence. Stroke. 2005;36:905-911. 3. Qureshi AI, Kirmani JF, Divani AA, Hobson RW 2nd. Carotid angioplasty with or without stent placement versus carotid endarterectomy for treatment of carotid stenosis: a metaanalysis. Neurosurgery. 2005;56:1171-1179. 4. Flaherty ML, Flemming KD, McClelland R, Jorgensen NW, Brown RD Jr. Population-based study of symptomatic internal carotid artery occlusion: incidence and long-term follow-up. Stroke. 2004;35:e349-352. 5. Pierce GE, Keushkerian SM, Hermreck AS, Iliopoulos JI, Thomas JH. The risk of stroke with occlusion of the internal carotid artery. J Vasc Surg. 1989;9:74-80. 6. EC/IC Bypass Study Group. Failure of extracranialintracranial arterial bypass to reduce the risk of ischemic stroke. Results of an international randomized trial. N Engl J Med. 1985;313:1191-1200.
This study had some limitations. Because the patients were from a single center, the sample size was small. Only some patients with totally occluded ICA were treated with this hybrid operation. This means that it may not be suitable for every patient. Another problem was that some patients had carotid artery occlusion from the carotid dissection, which may originate from the petrous or cavernous ICA. This kind of occlusion usually could not be recanalized successfully. In chronic occlusion, the extended thrombus may be further organized. Endovascular devices may not be able to traverse through organized thrombus. CONCLUSIONS Combined CEA and endovascular carotid angioplasty was a safe method for revascularization of a totally occluded ICA. Careful selection of patients may increase the success rate. The original occlusion site from the carotid bifurcation and anastomotic flow within the cavernous segment from the external carotid artery may be indications for successful recanalization. Recanalization would be more likely to be unsuccessful if the ICA was occluded at the ophthalmic or supraclinoid segment and the thrombus lesion extended to the cervical segment.
7. Powers WJ, Clarke WR, Grubb RL Jr, Videen TO, Adams HP Jr, Derdeyn CP, et al. Extracranialintracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the Carotid Occlusion Surgery Study randomized trial. JAMA. 2011;306:1983-1992. 8. Terada T, Yamaga H, Tsumoto T, Masuo O, Itakura T. Use of an embolic protection system during endovascular recanalization of a totally occluded cervical internal carotid artery at the chronic stage. Case report. J Neurosurg. 2005;102: 558-564. 9. Kobayashi N, Miyachi S, Hattori K, Tanasawa T, Okada T, Endo O, et al. Carotid angioplasty with stenting for chronic internal carotid artery occlusion: technical note. Neuroradiology. 2006;48: 847-851. 10. Komiyama M, Yoshimura M, Honnda Y, Matsusaka Y, Yasui T. Percutaneous angioplasty of a chronic total occlusion of the intracranial internal carotid artery. Case report. Surg Neurol. 2006;66:513-518. 11. Lin MS, Lin LC, Li HY, Lin CH, Chao CC, Hsu CN, et al. Procedural safety and potential vascular complication of endovascular recanalization for chronic cervical internal carotid artery occlusion. Circ Cardiovasc Intervent. 2008;1:119-125.
13. Kao HL, Lin MS, Wang CS, Lin YH, Lin LC, Chao CL, et al. Feasibility of endovascular recanalization for symptomatic cervical internal carotid artery occlusion. J Am Coll Cardiol. 2007;49:765-771. 14. Thomas AJ, Gupta R, Tayal AH, Kassam AB, Horowitz MB, Jovin TG. Stenting and angioplasty of the symptomatic chronically occluded carotid artery. AJNR Am J Neuroradiol. 2007;28:168-171. 15. Bhatt A, Majid A, Kassab M, Gupta R. Chronic total symptomatic carotid artery occlusion treated successfully with stenting and angioplasty. J Neuroimaging. 2009;19:68-71. 16. Shojima M, Nemoto S, Morita A, Miyata T, Namba K, Tanaka Y, et al. Protected endovascular revascularization of subacute and chronic total occlusion of the internal carotid artery. AJNR Am J Neuroradiol. 2010;32:481-486.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 1 May 2018; accepted 13 August 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.08.104 Journal homepage: www.WORLDNEUROSURGERY.org
12. Rostambeigi N, Khatri R, Hassan AE, Qureshi AI. Duplex ultrasound assisted endovascular revascularization of chronic internal carotid artery occlusion: technical note. J Vasc Interv Neurol. 2013;6: 42-46.
WORLD NEUROSURGERY -: e1-e9, - 2018
Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
www.WORLDNEUROSURGERY.org
e9
Estimation and Recanalization of Chronic Occluded Internal Carotid Artery: Hybrid Operation by Carotid Endarterectomy and Endovascular Angioplasty Bing Liu, Wei Wei, Yongli Wang, Xinyu Yang, Shuyuan Yue, Jianning Zhang
OBJECTIVE: Proper treatment for chronic occluded internal carotid artery (ICA) has not been determined. Endovascular recanalization may cause arterial injury and distal embolism. Hybrid recanalization for chronic occluded ICA was performed, and its safety and effectiveness were estimated.
-
METHODS: From March 2011 to March 2017, 21 patients were treated by hybrid recanalization with >1 year of follow-up. The ICA was totally occluded from the cervical segment to the cavernous, ophthalmic, or supraclinoid segment. Clinical characteristics, treatment strategy, recanalization rate, and main adverse events were reviewed retrospectively.
was occluded by the plaque at the ophthalmic or supraclinoid segment with the thrombus retrograde to the cervical segment.
-
RESULTS: Initial recanalization was achieved in 15 patients (71.4%). Successful revascularization was more likely if the ICA was occluded with the plaque at the carotid bifurcation and the thrombus anterograde to the cavernous segment. There was no carotid dissection or intracranial hemorrhage. There were no new postprocedural neurologic deficits. Among 14 patients who underwent successful recanalization with follow-up, 1 patient had a repeat occlusion and another experienced about 50% restenosis.
-
CONCLUSIONS: Hybrid recanalization by carotid endarterectomy and arterial angioplasty is a safe treatment method for chronic totally occluded ICA. Recanalization was more likely to be successful if the ICA was occluded by the plaque at the carotid bifurcation with the thrombus anterograde to the cavernous segment than if the artery
-
INTRODUCTION
S
evere carotid artery stenosis is the most common cause of transient ischemic attack or stroke. Carotid endarterectomy (CEA) is effective for preventing stroke and has been accepted for >20 years as the primary treatment for patients with severe carotid artery stenosis. In recent years, these patients have also been treated with carotid artery stenting using an embolic protection device with noninferior results compared with CEA.1-3 Chronic internal carotid artery (ICA) occlusion is a relatively uncommon but important cause of transient ischemic attack and cerebral infarction.4 The annual rate of nonfatal stroke was reported to be 3%e10% in adults >60 years old with carotid occlusion.5 Recurrent ischemic events were seen in about 25% of patients with symptomatic carotid occlusion. The best treatment for chronic carotid artery occlusion has not been determined. Although extracranial-intracranial (EC-IC) artery bypass was performed for several decades, it failed to yield clinical benefit. A multicenter randomized trial comparing medical therapy alone with EC-IC bypass surgery added to best medical therapy showed no superiority of EC-IC bypass procedure compared with medical therapy.6 The Carotid Occlusion Surgery Study trial was stopped prematurely also as a result of lack of superiority.7 Endovascular recanalization has been introduced in recent years for the management of occluded carotid artery.8-10 Several technical problems must be considered during endovascular
Key words Carotid artery stenting - Carotid endarterectomy - Chronic occlusion - Hybrid operation - Internal carotid artery - Recanalization
Department of Neurosurgery, Tianjin Medical University General Hospital, Tianjin Neurological Institute, Tianjin, China
Abbreviations and Acronyms CEA: Carotid endarterectomy EC-IC: Extracranial-intracranial ICA: Internal carotid artery
Available online: www.sciencedirect.com
-
WORLD NEUROSURGERY -: e1-e9, - 2018
To whom correspondence should be addressed: Bing Liu, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.08.104 Journal homepage: www.WORLDNEUROSURGERY.org 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
www.WORLDNEUROSURGERY.org
e1
ORIGINAL ARTICLE BING LIU ET AL.
e2
www.SCIENCEDIRECT.com
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.08.104
ORIGINAL ARTICLE BING LIU ET AL.
recanalization procedures, including issues related to protecting the cerebral circulation from distal embolism, how to determine the true lumen, and how to successfully traverse a long occlusive lesion without incurring additional arterial injury, which remains technically challenging.11,12 Endovascular devices may traverse the false lumen in the occluded segment and induce artery dissection and pseudoaneurysm formation. Furthermore, the recanalization procedure cannot be achieved in this situation. In chronic cases, the carotid artery was usually occluded by atherosclerotic plaque and subsequent extensive thrombus. In the plaque segment, the true lumen was usually difficult to determine and traverse with endovascular devices. However, it was easier in the thrombus segment. The plaque at the carotid bifurcation could be removed by the endarterectomy, and then the true lumen in the ICA could be distinguished. Thus, recanalization of the occluded carotid artery may be achieved using combined endarterectomy and endovascular carotid angioplasty. From March 2011 to March 2017, 21 patients with symptomatic chronic totally occluded ICA were treated by hybrid recanalization, which included CEA and simultaneous endovascular angioplasty. The clinical characteristics, treatment strategy, and outcomes at 30 days were analyzed, and follow-up was conducted for >1 year. MATERIALS AND METHODS This study protocol was examined and approved by the Ethical Committee of Tianjin Medical University, an academic medical center. Patients with symptomatic chronic occluded ICA were recruited to be treated by the hybrid operation. All the benefits and disadvantages of the operation were carefully explained to the patients and their relatives, and the wishes of the patients were taken into considered in the selection of treatment. The operation was performed with the informed consent of the patients and their relatives. Data Collection Clinical characteristics, treatment strategy, and outcomes of patients who were treated from March 2011 to March 2017 with >1 year of follow-up were reviewed retrospectively. Patients were recruited for this research using specific criteria, as follows: 1) Patients had ICA occlusion extending from the cervical segment to the intracranial segment. 2) The intracranial ICA was patent with anastomotic branches from the external carotid artery usually via the ophthalmic artery, or from the vertebrobasilar artery via the posterior communicating artery, or from the contralateral ICA via the anterior communicating artery. 3) Patients had an ischemic attack (modified Rankin Scale score <3) or amaurosis or reduced cerebral infusion. 4) Patients were excluded if 1 of the following conditions was present: nonatherosclerotic carotid artery disease; history of bleeding disorder; renal insufficiency; congestive heart failure; or contraindication to heparin, aspirin, or clopidogrel. 5) If
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
the patient had unstable angina or acute myocardial infarction, the treatment was to be given at least 30 days later, when angina or myocardial infarction was controlled. 6) Older patients, especially patients >75 years old, with contralateral laryngeal nerve palsy, previous radical head/neck surgery or radiation therapy to the neck, or poor neurologic condition (modified Rankin Scale score 3) did not receive the therapy. Preoperative Evaluation A thorough medical and detailed cardiology evaluation was carried out for all patients. Medical therapy for comorbidities, such as hypertension, diabetes mellitus, and dyslipidemia, was optimized. All patients underwent digital subtraction angiography to confirm complete occlusion of the ICA, the occluded segment, and the established collateral filling to the ipsilateral intracranial ICA. Single-photon emission computed tomography was performed in all patients to evaluate cerebral perfusion. Treatment Procedure All authors were trained and specialized in CEA, endovascular carotid angioplasty, or both. The operation was performed by at least 2 authors, with one a specialist in CEA and the other a specialist in endovascular therapy. The procedure was supervised by another author to confirm whether or not the recanalization was successful. Patients usually underwent the procedure 3 weeks after the onset of ischemic events. A dual antiplatelet regimen with aspirin (100 mg) and clopidogrel (75 mg) was started at least 7 days before the procedure. The operation was performed under general anesthesia with continuous electroencephalogram monitoring. The procedure was performed in the hybrid operating room, in which both the open surgery and the endovascular procedure could be carried out simultaneously. The patients underwent placement of a 6-F sheath introducer via the percutaneous transfemoral route. A longitudinal incision parallel to the medial aspect of the sternocleidomastoid muscle was made to explore the common, internal, and external carotid arteries and superior thyroid artery. The ICA was explored as far as possible. Heparin (4000 IU) was given intravenously 5 minutes before the artery clamping. The common, external carotid, and superior thyroid arteries were clamped. A linear longitudinal incision was made first in the common carotid artery, and the atherosclerotic plaque could be seen at the carotid bifurcation. The incision was then extended distally to the ICA to the distal end of the plaque. The thrombus mostly adhered to the atherosclerotic plaque in the lumen and extended distally along the ICA to the intracranial segment. After removal of the plaque, the true lumen of the ICA could be determined. Then the endovascular equipment was used to enter the true lumen and advance the occluded segment through the
Figure 1. Successful recanalization of totally occluded internal carotid artery to cavernous segment (group A). (A) A 60-year-old man presented with left ischemic stroke, as shown on diffusion-weighted imaging performed 4 weeks before the operation. (B and C) The left internal carotid artery was totally occluded from the cervical segment to the cavernous segment (group A). (D) The right carotid artery provided blood flow via the anterior communicating artery to left anterior and middle cerebral arteries. (E) Atherosclerotic plaque and extensive thrombus are shown at the carotid bifurcation. (F) The plaque was removed. (G) After carotid endarterectomy, the true lumen of the internal carotid artery was determined. (H) Through the carotid incision, the thrombectomy was carried out by Fogarty balloon catheter. (I) The thrombus that was removed from the internal carotid artery is shown. (J) Successful recanalization of the left internal carotid artery was confirmed by angiography after closure of the cervical incision through the femoral route.
WORLD NEUROSURGERY -: e1-e9, - 2018
www.WORLDNEUROSURGERY.org
e3
ORIGINAL ARTICLE BING LIU ET AL.
e4
www.SCIENCEDIRECT.com
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.08.104
ORIGINAL ARTICLE BING LIU ET AL.
incised cervical segment, including a 0.035-inch standard guidewire with the support of a intracranial support catheter (Navien; Medtronic, Minneapolis, Minnesota, USA) and a 0.014-inch guidewire in combination with a microcatheter (Echelon 10; Medtronic). After successfully traversing through the occluded segment and reaching the intracranial patent segment, the Solitaire FR stent (Medtronic) or Fogarty balloon catheter (Edwards Lifesciences Corp., Irvine, California, USA) was advanced into the intracranial patent segment and was withdrawn to move the thrombus out from the incision of the cervical carotid artery. This procedure was performed 2 or 3 times. If the larger thrombus, rather than debris, came out of the incision, robust backflow of blood from the ICA could be seen. The ICA clamp was then placed distal to the incision. If the guidewire and catheter could not traverse through the occluded segment or no blood backflow came out from the incision, the recanalization was not unsuccessful. The closure of the carotid artery was performed with a 6-0 polypropylene suture. After closing the cervical incision, the patency of the treated ICA and the formation of carotid dissection and pseudoaneurysm were confirmed by angiography obtained through the transfemoral route. If there was remnant stenosis (>50%) at the cavernous or petrous segment, the 3.0-mm to 4.0mm balloon (Gateway; Boston Scientific, Marlborough, Massachusetts, USA) was advanced to the remnant stenosis site and inflated to normal pressure. The balloon catheter was then removed, and the intracranial stent delivery catheter (Apollo; MicroPort Medical Co., Ltd., Shanghai, China) was placed across the stenotic lesion, and the stent was deployed. On completion of the procedure, the 6-F sheath was removed, and hemostasis was obtained with a vascular closure device (Exoseal; Cordis Corporation, Miami Lakes, Florida, USA). Blood pressure was strictly controlled during the entire procedure. If the occluded carotid artery was successfully recanalized, the postprocedural mean arterial pressure was kept at 10%e20% below baseline to prevent cerebral reperfusion injury. All patients received both aspirin and clopidogrel for at least 3 months after the procedure, and aspirin was continued thereafter. The patients undergoing stent placement received low-molecular-weight heparin for 3 days after the procedure.
Outcome Assessment All patients were divided into 3 groups according to the distal site of the occluded ICA. If the ICA was occluded extending to the cavernous segment as demonstrated by the collateral blood flow, patients were allocated to group A; patients with occlusion extending to the ophthalmic segment were allocated to group B; and patients with occlusion extending to the supraclinoid segment were allocated to group C. Outcomes evaluated included revascularization of the occluded ICA, intracranial hemorrhage, carotid artery dissection and pseudoaneurysm formation, death from any
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
cause, and ipsilateral and contralateral major stroke within 30 days after the procedure. The main local complications, which included cervical or groin hematoma, infection, femoral pseudoaneurysm or arteriovenous fistula at the puncture site, lower limb arterial occlusion or thrombosis, and cranial nerve palsy, were also noted. Follow-up was performed for all patients, and long-term outcomes were assessed on death due to the treated carotid artery, ipsilateral major stroke, and target vessel revascularization between 30 days and 1 year. Target vessel revascularization was evaluated by Doppler 7 days after the procedure and then by Doppler or computed tomography angiography at 6 months and 1 year after the procedure.
RESULTS Clinical Characteristics From March 2011 to March 2017, 21 patients with symptomatic chronic occluded ICA were treated by hybrid recanalization. The mean age of all patients was 56 years (range, 41e66 years); 19 patients (90.5%) were men. Twenty patients presented with symptoms of cerebral infarction or transient ischemic attack, among whom 3 patients also had retinal infarction. The other patient did not have cerebral ischemia, only retinal infarction derived from the occluded carotid artery. All patients had reduced cerebral perfusion on the occluded side compared with the contralateral side. Although most patients had hypertension, diabetes mellitus, or coronary artery disease, no patients had severe systemic comorbidities, such as acute myocardial infarction, chronic obstructive pulmonary disease, or kidney dysfunction.
Recanalization Rate Initial recanalization was achieved in 15 patients (71.4%) with smooth flow through the entire ICA and residual stenosis <50%. In group A (n ¼ 13 patients), 12 patients underwent successful recanalization (Figure 1). In the patient with failed recanalization, after the incision of the carotid artery, an obvious plaque was found at the bifurcation. However, the endovascular devices could not traverse through the petrous segment after the removal of the plaque. In group B (n ¼ 6 patients), 3 patients had successful carotid artery revascularization. None had retinal infarction. However, the other 3 patients who had unsuccessful recanalization had retinal infarction. In these patients, no plaque was located at the carotid bifurcation, but thrombus was detected. After removal of the thrombus in the cervical segment of the ICA, endovascular devices could be advanced to the cavernous segment but could not traverse through the ophthalmic segment (Figure 2). In group C (n ¼ 2 patients), no recanalizations succeeded. The endovascular devices could not traverse through the occluded supraclinoid segment (Figure 3).
Figure 2. Unsuccessful recanalization of internal carotid artery occluded to ophthalmic segment and thrombus at cervical segment (group B). (A) A 53-year-old man presented with symptoms of ischemic stroke as shown on diffusion-weighted imaging and transient amaurosis of the left eye. (B) The left internal carotid artery was totally occluded from the cervical segment, not from the bifurcation, with a stumplike appearance. (C) The intracranial internal carotid artery was patent from the ophthalmic segment, with the anastomotic branches from the ophthalmic artery. (D) The thrombus, not the plaque, was found at the carotid artery incision. (E) The microcatheter and guidewire could not traverse through the ophthalmic segment (group B), and recanalization could not be achieved successfully.
WORLD NEUROSURGERY -: e1-e9, - 2018
www.WORLDNEUROSURGERY.org
e5
ORIGINAL ARTICLE BING LIU ET AL.
e6
www.SCIENCEDIRECT.com
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.08.104
ORIGINAL ARTICLE BING LIU ET AL.
Stents were placed in 7 of 15 patients with recanalization (Figure 4). Postprocedural Complications No patients died within 30 days after the procedure. There was no thrombogenesis and no intracranial hemorrhage during the procedure. There was no carotid dissection or pseudoaneurysm formation. No intracranial hemorrhage occurred after the carotid artery revascularization. No major stroke occurred after the operation, and no new postprocedural neurologic deficits were observed in any patient. Hyperperfusion syndrome was observed in 2 patients, with symptoms of headache that disappeared a few days later under the control of blood pressure. One patient had mild groin hematoma, but there were no patients with femoral pseudoaneurysm or arteriovenous fistula at the puncture site or lower limb arterial thrombosis. Three patients had moderate cervical hematoma but did not require surgical evacuation. Another patient had cervical incision infection. Follow-Up Revascularization of Target Vessel Among the patients who underwent the successful recanalization, 1 patient died of a heart attack 4 months after the operation. The other patients had >1 year of follow-up. During the follow-up period, no patients had ischemic stroke owing to the target vessel. One patient received carotid artery stenting of the collateral ICA owing to stenosis progression. Among these 14 patients, the revascularized carotid arteries in 12 patients were patent without restenosis. In the other 2 patients, the ICA was totally occluded again in 1 patient, and moderate restenosis (approximately 50%) occurred in another. Both patients presented with no symptoms and underwent no further operation and received only enhanced medication. There were no deaths among the patients who underwent unsuccessful recanalization. One patient had recurrent ischemic attack owing to the occluded carotid artery. Another patient had an ischemic stroke on the brainstem because of stenosis of the basilar artery, which did not manifest during the operation. Another patient received CEA of the contralateral carotid artery owing to severe stenosis. DISCUSSION The best treatment for patients with a completely occluded ICA has not been determined. Medical management alone may be inadequate, and revascularization may be beneficial in patients with impaired cerebral perfusion. In our series, all patients were enrolled because of neurologic deficit or objective hemisphere ischemia.
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
Endovascular recanalization of the occluded ICA was an accepted treatment technique for acute stroke, but it was rarely performed beyond the acute phase. There were some choices for the treatment of chronic occluded ICA, such as EC-IC bypass, CEA, or carotid artery stenting for the contralateral carotid artery stenosis if the contralateral carotid artery provided collateral blood flow to the occluded carotid artery and had moderate to severe stenosis. Recanalization of the chronic occluded carotid artery was reported initially by Terada et al.8; a patient underwent successful endovascular recanalization of a chronic occlusion with proximal protection of the carotid artery. Kao et al.13 reported successful in recanalization of 22 chronic ICA occlusions among 30 cases. A major concern in recanalization of a chronic carotid artery occlusion is the possibility of causing a distal embolism as a result of the thrombotic content of embolic debris released during the endovascular device manipulation.14,15 Thus, in endovascular recanalization, the proximal occlusion of the common carotid artery using an occlusion balloon is typically performed to reverse the flow with the goal of minimizing the risk of thromboembolic complications.16 Other important complications associated with endovascular intervention include carotid dissection and pseudoaneurysm formation,11 which have an incidence of up to 6% because of the inability to distinguish between the lumen and arterial wall in the occlusive lesion. In particular, the lesion was composed of plaque with calcification. This kind of lesion was solid, and there was usually almost no lumen. The endovascular devices had difficulty in traversing through it. However, it was easier to pass through the lesion composed of thrombus, which is usually attached to the plaque. Hybrid recanalization of chronic occluded ICA was carried out using a combination of CEA and endovascular angioplasty, which were performed simultaneously. The plaque at the carotid bifurcation and cervical ICA was removed through the incision in the carotid artery. The true lumen was then distinguished, and the endovascular equipment was used to enter the ICA and to pass through the thrombotic segment. This avoided carotid artery injury. If the equipment successfully reached the distal patent segment, it was retrieved from the incision. If the thrombectomy was performed successfully, backflow of the blood was seen, and the thrombus and debris flowed out from the carotid incision. This prevented thromboembolic complications. After closure of the carotid artery and the cervical incision, angiography was performed to confirm the patency of the ICA through the transfemoral route. If there was prominent stenosis in the ICA, carotid angioplasty, with or without stent placement, was performed. In our series, the patients with a totally occluded ICA were treated safely using the hybrid recanalization technique. There was no symptomatic ischemic stroke and no intracranial hemorrhage. Local complications occurred in a few patients. No patients experienced carotid dissection or pseudoaneurysm formation.
Figure 3. Unsuccessful recanalization of internal carotid artery occluded to supraclinoid segment (group C). (A) A 48-year-oldman presented with symptoms of left hemisphere stroke, as shown on diffusion-weighted imaging obtained 4 months prior. (B) Severe stenosis of the supraclinoid segment of the left internal carotid artery is shown on magnetic resonance angiography at that time. (C) The patient had been receiving medication since then. However, he subsequently presented with transient ischemic attack of the right limb. Digital subtraction angiography showed total occlusion of the left internal carotid artery from the cervical segment 4 months later. (D and E) The left intracranial internal carotid artery was patent with anastomosis from the vertebrobasilar artery via posterior communicating artery. Revascularization of the left internal carotid artery failed (group C).
WORLD NEUROSURGERY -: e1-e9, - 2018
www.WORLDNEUROSURGERY.org
e7
ORIGINAL ARTICLE BING LIU ET AL.
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
Figure 4. Successful recanalization with stent implantation. (A) A 63-year-old man with ischemic stroke had a right occluded internal carotid artery from the carotid bifurcation, and the cavernous segment was patent, as demonstrated on digital subtraction angiography. (B) After successful recanalization,
Success of the recanalization procedure depended on passing the guidewire and catheter through the occluded segment. The occlusion of an artery usually originated from the plaque, which arose mainly at the artery bifurcation, and then the thrombus
e8
www.SCIENCEDIRECT.com
angiography showed >50% remnant stenosis on the petrous segment of the right internal carotid artery. (C) The stenosis disappeared after the stent was deployed at the stenosis position. (D) Angiography performed 1 year later showed the internal carotid artery was patent.
extended anterograde or retrograde to the next bifurcation with significant collateral blood flow. It was difficult to traverse the endovascular devices through the plaque, which may induce artery dissection and pseudoaneurysm formation in the chronic
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.08.104
ORIGINAL ARTICLE BING LIU ET AL.
HYBRID RECANALIZATION OF CHRONIC OCCLUDED ICA
occluded segment. However, it was easy to traverse through the thrombus part. If the occlusion originated from the carotid bifurcation and the thrombus extended anterograde to the cavernous segment that was perfused by the collateral blood flow, usually from the ophthalmic artery (group A), successful recanalization was most possible. However, if the plaque was at the ophthalmic bifurcation of the ICA and the thrombus extended retrograde to the cervical bifurcation, where it exhibited an appearance of a tapered stump on the angiogram of the cervical segment (group B), no plaque, but thrombus, was found at the cervical segment, and the guidewire could not usually pass through the plaque at the ophthalmic segment. Recanalization may be unsuccessful, especially in patients with retinal infarction. If the collateral blood flow from the external carotid artery could not anastomose with the ophthalmic segment (group C), the plaque was usually located at the supraclinoid segment. Recanalization mostly could not be done. The anastomotic blood flow was usually from the contralateral carotid artery through the anterior communicating artery or from the vertebrobasilar artery through the posterior communicating artery.
REFERENCES 1. 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;339:1415-1425. 2. Coward LJ, Featherstone RL, Brown MM. Safety and efficacy of endovascular treatment of carotid artery stenosis compared with carotid endarterectomy: a Cochrane systematic review of the randomized evidence. Stroke. 2005;36:905-911. 3. Qureshi AI, Kirmani JF, Divani AA, Hobson RW 2nd. Carotid angioplasty with or without stent placement versus carotid endarterectomy for treatment of carotid stenosis: a metaanalysis. Neurosurgery. 2005;56:1171-1179. 4. Flaherty ML, Flemming KD, McClelland R, Jorgensen NW, Brown RD Jr. Population-based study of symptomatic internal carotid artery occlusion: incidence and long-term follow-up. Stroke. 2004;35:e349-352. 5. Pierce GE, Keushkerian SM, Hermreck AS, Iliopoulos JI, Thomas JH. The risk of stroke with occlusion of the internal carotid artery. J Vasc Surg. 1989;9:74-80. 6. EC/IC Bypass Study Group. Failure of extracranialintracranial arterial bypass to reduce the risk of ischemic stroke. Results of an international randomized trial. N Engl J Med. 1985;313:1191-1200.
This study had some limitations. Because the patients were from a single center, the sample size was small. Only some patients with totally occluded ICA were treated with this hybrid operation. This means that it may not be suitable for every patient. Another problem was that some patients had carotid artery occlusion from the carotid dissection, which may originate from the petrous or cavernous ICA. This kind of occlusion usually could not be recanalized successfully. In chronic occlusion, the extended thrombus may be further organized. Endovascular devices may not be able to traverse through organized thrombus. CONCLUSIONS Combined CEA and endovascular carotid angioplasty was a safe method for revascularization of a totally occluded ICA. Careful selection of patients may increase the success rate. The original occlusion site from the carotid bifurcation and anastomotic flow within the cavernous segment from the external carotid artery may be indications for successful recanalization. Recanalization would be more likely to be unsuccessful if the ICA was occluded at the ophthalmic or supraclinoid segment and the thrombus lesion extended to the cervical segment.
7. Powers WJ, Clarke WR, Grubb RL Jr, Videen TO, Adams HP Jr, Derdeyn CP, et al. Extracranialintracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the Carotid Occlusion Surgery Study randomized trial. JAMA. 2011;306:1983-1992. 8. Terada T, Yamaga H, Tsumoto T, Masuo O, Itakura T. Use of an embolic protection system during endovascular recanalization of a totally occluded cervical internal carotid artery at the chronic stage. Case report. J Neurosurg. 2005;102: 558-564. 9. Kobayashi N, Miyachi S, Hattori K, Tanasawa T, Okada T, Endo O, et al. Carotid angioplasty with stenting for chronic internal carotid artery occlusion: technical note. Neuroradiology. 2006;48: 847-851. 10. Komiyama M, Yoshimura M, Honnda Y, Matsusaka Y, Yasui T. Percutaneous angioplasty of a chronic total occlusion of the intracranial internal carotid artery. Case report. Surg Neurol. 2006;66:513-518. 11. Lin MS, Lin LC, Li HY, Lin CH, Chao CC, Hsu CN, et al. Procedural safety and potential vascular complication of endovascular recanalization for chronic cervical internal carotid artery occlusion. Circ Cardiovasc Intervent. 2008;1:119-125.
13. Kao HL, Lin MS, Wang CS, Lin YH, Lin LC, Chao CL, et al. Feasibility of endovascular recanalization for symptomatic cervical internal carotid artery occlusion. J Am Coll Cardiol. 2007;49:765-771. 14. Thomas AJ, Gupta R, Tayal AH, Kassam AB, Horowitz MB, Jovin TG. Stenting and angioplasty of the symptomatic chronically occluded carotid artery. AJNR Am J Neuroradiol. 2007;28:168-171. 15. Bhatt A, Majid A, Kassab M, Gupta R. Chronic total symptomatic carotid artery occlusion treated successfully with stenting and angioplasty. J Neuroimaging. 2009;19:68-71. 16. Shojima M, Nemoto S, Morita A, Miyata T, Namba K, Tanaka Y, et al. Protected endovascular revascularization of subacute and chronic total occlusion of the internal carotid artery. AJNR Am J Neuroradiol. 2010;32:481-486.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 1 May 2018; accepted 13 August 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.08.104 Journal homepage: www.WORLDNEUROSURGERY.org
12. Rostambeigi N, Khatri R, Hassan AE, Qureshi AI. Duplex ultrasound assisted endovascular revascularization of chronic internal carotid artery occlusion: technical note. J Vasc Interv Neurol. 2013;6: 42-46.
WORLD NEUROSURGERY -: e1-e9, - 2018
Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
www.WORLDNEUROSURGERY.org
e9