03_05_JNS.2 2/23/05 3:18 PM Page 558 J Neurosurg 102:558–564, 2005 Use of an embolic protection system during endovascular recanalization of a totally occluded cervical internal carotid artery at the chronic stage Case report TOMOAKI TERADA, M.D., PH.D., HIROO YAMAGA, M.D., TOMOYUKI TSUMOTO, M.D., OSAMU MASUO, M.D., AND TORU ITAKURA, M.D., PH.D. Department of Neurological Surgery, Wakayama Medical University, Wakayama City, Japan √ A symptomatic internal carotid artery (ICA) occlusion with hemodynamic compromise was treated at its chronic stage by using an endovascular technique. An embolic protection system was used during the recanalization procedure to prevent stroke by reversing the flow from the distal ICA to the common carotid artery. The totally occluded ICA was completely recanalized through percutaneous transluminal angioplasty and stent placement. The patient’s symptom (transient ischemic attack) disappeared completely after treatment with no new neurological deficit. Single-photon emission computerized tomography findings confirmed improvement of the hemodynamic compromise, and no new high-intensity spots appeared on diffusion-weighted magnetic resonance imaging after treatment. This case shows that endovascular recanalization by using an embolic protection device can be considered as an alternative treatment for symptomatic ICA occlusion with hemodynamic compromise and refractoriness to antiplatelet therapy, even in the chronic stage of the illness. KEY WORDS • arterial occlusion • embolic protection • internal carotid artery • percutaneous transluminal angioplasty • stent I T is well known that occlusion of the cervical ICA results in chronic hypoperfusion10,16 and causes cerebral ischemia. The beneficial effects of extracranial–intracranial bypass surgery for this type of ischemia have been disproved by the results of a cooperative study,16 although the procedure’s efficacy in improving hemodynamic compromise has been reported.10 The recent development of endovascular therapy has enabled the recanalization of totally occluded iliac or subclavian arteries in the chronic stage.7,13 Nevertheless, there are no reports on the recanalization of the cervical ICA in the chronic stage, because of the risk of embolic stroke related to the recanalized artery. We report a case of successful endovascular recanalization of a totally occluded cervical ICA with cerebral hypoperfusion by using an embolic protection system.16 Case Report History and Examination. This 73-year-old man had a history of mild aphasia 1 month before admission. Magnetic resonance imaging and MR angiography at that time Abbreviations used in this paper: CA = carotid artery; CCA = common CA; CEA = carotid endarterectomy; ECA = external CA; ICA = internal CA; MCA = middle cerebral artery; MR = magnetic resonance; PTA = percutaneous transluminal angioplasty; SPECT = single-photon emission computerized tomography; TIA = transient ischemic attack. 558 FIG. 1. Imaging studies obtained 2 months before admission to our facility. Fluid-attenuated inversion-recovery MR images (upper) demonstrating a small high-intensity lesion in the left occipital lobe and multiple high-intensity spots in the bilateral corona radiata. Magnetic resonance angiograms (lower) revealing occlusion of the cervical ICA. J. Neurosurg. / Volume 102 / March, 2005 03_05_JNS.2 2/23/05 3:18 PM Page 559 Endovascular recanalization of totally occluded ICA FIG. 2. Angiograms obtained on admission to our facility. Left: The left ICA was totally occluded at the cervical carotid bifurcation. Center and Right: The intracranial ICA was opacified via the primitive trigeminal artery from the basilar artery, and the ophthalmic artery was opacified via the ECA. demonstrated a small infarction in the left occipital lobe and periventricular area and total occlusion of the left ICA (Fig. 1). Transient ischemic attacks of aphasia and/or right hemiparesis continued despite the administration of an antiplatelet drug (ticlopidine 200 mg). The patient was then transferred to our hospital. Cerebral angiography studies on admission demonstrated total occlusion of the cervical ICA even in the late venous phase, and the distal portion of the ICA was opacified via retrograde flow from the left ophthalmic artery and the primitive trigeminal artery (Fig. 2). Single-photon emission computerized tomography scanning with 99mTc–ethyl cysteinate dimer demonstrated cerebral hypoperfusion in the left MCA territory with reduced reactivity to the Diamox challenge test (Fig. 3). We diagnosed the patient’s TIA as hemodynamic ischemia given the hypoperfusion of the left cerebral hemisphere. Endovas- FIG. 3. Admission SPECT scans obtained when the patient was at rest (control), demonstrating reduced cerebral blood flow in the left MCA territory (upper). The SPECT scans obtained after the Diamox challenge revealed no increase in cerebral blood flow in the left MCA territory, whereas marked increase in blood flow was shown in the other areas (lower). Red indicates high flow; yellow, intermediate flow; and green to blue, slow flow. J. Neurosurg. / Volume 102 / March, 2005 559 03_05_JNS.2 2/23/05 3:18 PM Page 560 T. Terada, et al. FIG. 4. Schema of endovascular recanalization. A: A No. 10.5 French double-lumen balloon catheter was introduced in the CCA, and another occlusion balloon was placed at the orifice of the ECA. The No. 10.5 French balloon catheter was connected to the No. 4 French sheath in the femoral vein via a filter. Blood flow (red) was reversed from a distal to a proximal direction, as shown by the arrow. The gray column indicates the occluded portion of the ICA featured on the angiogram. B: The occluded ICA was penetrated by a guidewire, and the PTA balloon catheter was introduced into the petrous ICA, where it was patent, under the flow-reversal technique. A PTA was performed at the entire occluded ICA segment by changing the position of the balloon catheter from the petrous to the proximal ICA. Yellow dots indicate the debris that appeared during PTA, which was aspirated from the guiding catheter placed in the CCA. C: The occluded ICA was reconstituted except for the focus of the occlusion. The yellow portion in the ICA, which was a focus of occlusion, showed the dilated atheromatous plaque created by the PTA balloon. D: A self-expanding stent (white mesh column) was activated to cover the entire atheromatous plaque, which caused total occlusion of the ICA. Then, postdilatation was performed. Finally, the ICA was completely reconstituted. cular recanalization was planned considering that his symptoms were refractory to medication and SPECT scanning results demonstrated hemodynamic compromise. Endovascular recanalization with the aid of an embolic protection system16 was tried 3 weeks after initial angiography and 7 weeks after initial MR angiography. 560 Endovascular Procedure. A transcranial Doppler system was attached to the patient’s head to monitor the flow of the MCA and the high-intensity transient signal during and after the endovascular procedure. After applying a local anesthetic agent, a No. 10 French sheath was introduced into his left femoral artery and a No. 5 French sheath into his right femoral artery. A No. 4 French sheath was introduced into his right femoral vein to withdraw blood from the guiding catheter in the left CCA. A No. 5 French catheter and a No. 10.5 French double-lumen balloon catheter (Lilic; ArteriA Medical Science, Inc., San Francisco, CA) were introduced into the left CCA after systemic heparinization. Activating clotting time was maintained from 250 to 350 seconds during the procedure. A balloon catheter (Cattleya; ArteriA Medical Science, Inc.) was introduced into the proximal portion of the ECA to eliminate any flow. The balloon of the No. 10.5 French balloon catheter was placed in the ECA and inflated, and the arterial blood from the lumen of this same catheter was shunted to the femoral vein via a filter with 100-mm pores. At this time all flow from the left CA was converted from a distal to a proximal direction (Fig. 4). Flow reversal was intermittently examined by injecting saline into the connecting tube between the guiding catheter and filter and confirmed by clearance of the injected saline from the arterial to the venous side. A 0.014-in guidewire (Transend; Boston Scientific, Natick, MA) and microcatheter (Transit II; Cordis Neurovascular, Inc., Miami, FL) were introduced to cross the totally occluded ICA while feeling for any resistance from the guidewire. The guidewire easily crossed the occluded lesion but the microcatheter did not. Thus, these instruments were withdrawn and a 0.035-in guidewire (Terumo Corp., Tokyo, Japan) and a No. 4 French catheter were used to cross the lesion. This guidewire penetrated the same occlusion point and the catheter followed. Slight resistance from the bifurcation was felt at the 7-cm distal point of the ICA, and thus the 0.35-in guidewire was exchanged for the 0.014-in guidewire and microcatheter system. The latter instruments easily crossed the occluded portion where the 0.035-in guidewire had penetrated. They were advanced to the cavernous portion where the patency of the ICA was demonstrated on an angiogram, although a small dissection was made at the petrous portion by the guidewire. Superselective angiography from the microcatheter in the cavernous ICA confirmed that the microcatheter was in the true lumen. The microcatheter was withdrawn and exchanged for a 3.5 3 15 mm PTA balloon catheter (Gateway; Boston Scientific). The balloon was inflated from the cavernous portion of the ICA initially at 6 atm for 30 seconds and moved gradually to the proximal portion of the ICA to dilate the entire artery from the cavernous to the petrous portion; at the C-1 vertebral level the catheter was exchanged for a 4 3 40 mm PTA balloon catheter (Savvy; Cordis Neurovascular, Inc.). The ICA was dilated in a manner similar to that of the bifurcation of the cervical CA. After PTA, an angiogram from the guiding catheter with balloon deflation exhibitied the dilated and patent ICA with narrowing at the bifurcation and a small dissection at the petrous portion (Fig. 5 left). At this time several high-intensity transient signals were recorded, as was elevation of the mean flow velocity from 52 to 80 cm/second on the transcranial Doppler monitor. The lesion of the occlusion was judged to be located on the proximal ICA; then an 8 3 40 mm self-expanding stent (SMART; Cordis J. Neurosurg. / Volume 102 / March, 2005 03_05_JNS.2 2/23/05 3:18 PM Page 561 Endovascular recanalization of totally occluded ICA FIG. 5. Left: Angiogram obtained after PTA from the cavernous ICA to the cervical ICA, demonstrating dissection and stenosis at the origin of the cervical ICA. Center: Angiogram obtained after stent placement for the residual stenosis, revealing complete reconstitution of the ICA. Right: An angiogram of the left intracranial arteries that were opacified in an antegrade fashion with no embolic occlusion, although a small dissection was noticed at the petrous portion. Neurovascular, Inc.) was activated to cover the stenotic portion and dilated using a 5 3 20 mm PTA balloon catheter (Savvy; Cordis Neurovascular, Inc.) under flow-reversal conditions. Finally, the occluded portion was successfully opened. The occlusion balloon in the CCA was kept inflated for 3 minutes to withdraw debris from the ICA by the retrograde flow from the distal ICA to the CCA after postdilation. The balloon in the ECA was deflated and withdrawn, and the proximal balloon was deflated. An angiogram demonstrated a dilated ICA (Fig. 5 center). It revealed no embolic occlusion of the left MCA and anterior cerebral artery, although a small arterial dissection was found at the petrous portion of the ICA (Fig. 5 right). No new neurological symptom appeared during or after the procedure. The No. 10 French sheath puncture point was closed using a suture closing device and the right femoral artery was manually compressed after withdrawing the No. 5 French sheath until hemostasis resulted. Debris of varying sizes was identified in the filter connected between the guiding catheter and the femoral vein. Systemic heparinization was continued for 24 hours, and antiplatelet drugs (200 mg ticlopidine and 100 mg aspirin) were administered after the endovascular treatment. Postoperative Course. No new lesion appeared on diffusion-weighted MR imaging 3 days after the procedure, although high-intensity areas derived from previous infarcts were shown in the occipital and periventricular areas (Fig. 6). On the 4th day after treatment, SPECT scanning revealed an increase in cerebral blood flow together with the recovery of vascular reactivity for the Diamox challenge in the left cerebral hemisphere (Fig. 7). An angiogram obtained 4 months after treatment demonstrated a patent ICA with 40% stenosis at the previously ocJ. Neurosurg. / Volume 102 / March, 2005 cluded portion, and the small dissection at the petrous ICA had completely disappeared (Fig. 8). No new neurological deficit or TIA occurred after treatment. Discussion Endovascular recanalization has been performed for totally occluded subclavian arteries or iliac arteries at the chronic stage7,13,20 and for totally occluded ICAs in the acute stage.12,14,18 No reports on the recanalization of a totally occluded cervical ICA at the chronic stage appear in the literature, however. The main reason this treatment has not been tried is the risk of cerebral embolism during the recanalization procedure. Recently, various protective devices have been developed to reduce embolic complications related to CA stent insertion.4,9,11,16,19 Distal protection systems such as a balloon protection system or filter wire do not prevent cerebral embolism during lesion crossing, however.4,9,11,19 Ohki, et al.,16 developed a proximal protection system for use during CA stent placement. Their concept of protection involves reversing the flow of the ICA from a distal to a proximal direction by occluding the CCA and the proximal ECA and drawing the blood flow from the distal portion of the guiding catheter. This process is achieved by making a shunt between the proximal end of the guiding catheter and the femoral vein. During this reversed condition, blood flow is directed always from the distal to the proximal portion; therefore, the risk of causing embolic complications related to recanalization of a totally occluded ICA is drastically reduced. The problem in recanalizing the occluded ICA is the difficulty in identifying the occlusion point. Based on the angiographic findings in the present case, the occlusion point 561 03_05_JNS.2 2/23/05 3:18 PM Page 562 T. Terada, et al. FIG. 6. Diffusion-weighted MR images obtained 3 days after endovascular recanalization. No new high-intensity signals were demonstrated when compared with the fluid-attenuated inversion-recovery image obtained before treatment, which had revealed the high-intensity area in the occipital lobe. was considered to be located between the petrous and the cervical ICA, although it was suspected to be at the cervical ICA bifurcation, judging from the commonality of the lesion and the shape of the stump. It was necessary to secure the true lumen from the proximal ICA to the cavernous ICA. We performed PTA from the distal to the proximal portion of the ICA and finally determined that the occluded lesion was located at the proximal cervical ICA. We recommend performing PTA at the cervical ICA by using a longer balloon catheter initially if the guidewire meets with resistance at the proximal ICA and the tip of the guidewire moves without resistance at the distal portion of the cervical ICA. As for the long-term results, totally occluded iliac or subclavian arteries show lower restenosis rates after recanalization7,13,20 than does the coronary artery.2,6 The difference between them seems to come down to the size of the native artery. If the diameter of the native artery is greater than 3 mm, the restenosis rate will be low, as seen in the iliac or subclavian artery. Therefore, the restenosis rate can be supposed to be low in the totally occluded cervical ICA. Some kind of revascularization was necessary in the patient in the present case, because antiplatelet therapy was ineffective in preventing TIA and hemodynamic ischemia 562 was proven by SPECT scanning results. Extracranial–intracranial bypass surgery was considered as one of the alternatives, but the beneficial effects of this surgery have been disproved by data from a cooperative study.8 Recently, the effect of bypass surgery for major cerebral artery occlusive diseases with hemodynamic compromise has been studied in the Carotid Occlusion Surgery Study,1 although the final results have yet to be reported. Surgical recanalization of a chronically occluded ICA was initially performed by Shucart and Garrido.17 They performed CEA for a totally occluded ICA, and the distal portion of the occlusion was opened using a Fogarty balloon catheter.5 Four cases of total ICA occlusion with retrograde filling of the intracranial ICA to the inferior portion of the carotid siphon were treated successfully. Nevertheless, this surgical treatment is not popular now for the following reasons. The success rate is not high,21 and there exist several risks, such as those associated with general anesthesia; occlusion of the ECA, which works as a collateral blood supply; embolic stroke from the occluded vessel; and rupture of the CA3 as described by Shucart and Garrido.17 The patients in the four cases reported by Shucart and Garrido were successfully treated; in one case, however, asymptomatic occlusion of the branch of the MCA was demonstrated. The advantages of endovascuJ. Neurosurg. / Volume 102 / March, 2005 03_05_JNS.2 2/23/05 3:18 PM Page 563 Endovascular recanalization of totally occluded ICA FIG. 7. Single-photon emission computerized tomography scans obtained after endovascular recanalization. The cerebral blood flow when the patient was at rest increased in the left MCA territory compared with that before treatment (upper). The vascular reactivity for the Diamox challenge also recovered (lower). lar recanalization over surgical recanalization are that the procedure is performed using a local anesthetic and fluoroscopic control. Therefore, even in the event that recanalization failed, endovascular therapy seems less invasive compared with surgical recanalization and general anesthesia. Nevertheless, embolic protection during the entire procedure is essential for endovascular therapy to maintain its advantages over surgical recanalization. Endovascular recanalization was performed using the system described by Ohki and colleagues.16 This procedure was successful and effective considering the disappearance of the patient’s TIAs and the improvement demonstrated on SPECT studies. Furthermore, the system worked successfully to prevent cerebral embolism during the recanalization procedure, as revealed on diffusion-weighted MR imaging, which showed no new high-intensity spots after recanalization. Note, however, that this system is a bit complicated, and inappropriate use of the requisite devices may result in serious complications. Therefore, this type of treatment must be performed by well-trained physicians to prevent embolic complication during recanalization.13 J. Neurosurg. / Volume 102 / March, 2005 FIG. 8. Angiograms obtained 4 months after recanalization. Left: A 40% stenosis was demonstrated at the previous occlusion point. Right: The petrous ICA was widely open and the dissection had been cured. 563 03_05_JNS.2 2/23/05 3:18 PM Page 564 T. Terada, et al. The unsolved problem related to endovascular recanalization of totally occluded ICAs is the risk of hyperperfusion. This therapy is applied in patients with hemodynamic compromise, and immediate vascular reconstruction is conducted by recanalization just as in CEA. In CEA, hyperperfusion syndrome occurs in patients with severe hemodynamic compromise;15 therefore, this type of patient would seem to have a high risk of hyperperfusion when undergoing endovascular recanalization. Controlling blood pressure will be very important in preventing hyperperfusion syndrome after endovascular recanalization. Conclusions Recanalization of the totally occluded cervical ICA at the chronic stage is possible and effective in cases with symptomatic hemodynamic compromise, if distal embolism is prevented by the reversal-flow technique. References 1. Adams HP Jr, Power WJ, Grubb RL Jr, Clarke WR, Woolson RF: Preview of a new trial of extracranial-to-intracranial arterial anastomosis: the carotid occlusion surgery study. Neurosurg Clin N Am 12:613–624, 2001 2. Antoniucci D, Valenti R, Santoro GM, Bolognese L, Trapani M, Cerisano G, et al: Restenosis after coronary stenting in current clinical practice. Am Heart J 135:510–518, 1998 3. Barker WF, Stern WE, Krayenbuhl H, Senning A: Carotid endarterectomy complicated by carotid cavernous sinus fistula. Ann Surg 167:568–572, 1968 4. Cremonesi A, Manetti R, Setacci F, Setacci C, Castriota F: Protected carotid stenting: clinical advantages and complications of embolic protection devices in 442 consecutive patients. Stroke 34:1936–1941, 2003 5. Davie JC, Richardson R: Distal internal carotid thrombo-embolectomy using a Fogarty catheter in total occlusion. Technical note. J Neurosurg 27:171–177, 1967 6. di Mario C, Reimers B, Almagor Y, Moussa I, Di Francesco L, Ferraro M, et al: Procedural and follow up results with a new balloon expandable stent in unselected lesions. Heart 79:234–241, 1998 7. Duber C, Klose KJ, Kopp H, Schmiedt W: Percutaneous transluminal angioplasty for occlusion of the subclavian artery: shortand long-term results. Cardiovasc Intervent Radiol 15:205–210, 1992 8. The EC-IC Bypass Study Group: Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke. Results of an international randomized trial. N Engl J Med 313: 1191–1200, 1985 9. Eckert B, Zeumer H: Editorial comment—carotid artery stenting 564 with or without protection devices? Strong opinions, poor evidence! Stroke 34:1941–1943, 2003 10. Ishikawa T, Kuroda S, Hokin K, Kamiyama H, Abe H: [Can ECIC bypass prevent brain ischemia from recurring?] No Shinkei Geka 26:823–829, 1998 (Jpn) 11. Kastrup A, Groschel K, Krapf H, Brehm BR, Dichgans J, Schulz JB: Early outcome of carotid angioplasty and stenting with and without cerebral protection devices: a systemic review of the literature. Stroke 34:813–819, 2003 12. Komiyama M, Nishio A, Noshijima Y: Endovascular treatment of acute thrombotic occlusion of the cervical internal carotid artery associated with embolic occlusion of the middle cerebral artery: case report. Neurosurgery 34:359–364, 1994 13. Mathias KD, Luth I, Haarmann P: Percutaneous transluminal angioplasty of proximal subclavian artery occlusions. Cardiovasc Intervent Radiol 16:214–218, 1993 14. Nesbit GM, Clark WM, O’Neill OR, Barnwell SL: Intracranial intraarterial thrombolysis facilitated by microcatheter navigation through an occluded cervical internal carotid artery. J Neurosurg 84:387–392, 1996 15. Ogasawara K, Yukawa H, Kobayashi M, Mikami C, Konno H, Terasaki K, et al: Prediction and monitoring of cerebral hyperperfusion after carotid endarterectomy by using single-photon emission computerized tomography scanning. J Neurosurg 99: 504–510, 2003 16. Ohki T, Parodi J, Veith FJ, Bates M, Bade M, Chang D, et al: Efficacy of a proximal occlusion catheter with reversal of flow in the prevention of embolic events during carotid artery stenting: an experimental analysis. J Vasc Surg 33:504–509, 2001 17. Shucart WA, Garrido E: Reopening some occluded carotid arteries. Report of four cases. J Neurosurg 45:442–446, 1976 18. Terada T, Tsuura M, Matsumoto H, Masuo O, Tsumoto T, Yamaga H, et al: Endovascular therapy for stenosis of the petrous or cavernous portion of the internal carotid artery: percutaneous transluminal angioplasty campared with stent placement. J Neurosurg 98:491–497, 2003 19. Terada T, Tsuura M, Matsumoto H, Masuo O, Yamaga H, Tsumoto T, et al: Results of endovascular treatment of internal carotid artery stenosis with a newly developed balloon protection catheter. Neurosurgery 53:617–625, 2003 20. Van Walraven LA, Andhyiswara T, van der Linden TN, Yo TI: The use of vascular stents in the treatment of iliac artery occlusion. Int J Angiol 9:232–235, 2000 21. Wylie EJ, Ehrenfeld WK: Extracranial Occlusive Cerebrovascular Disease: Diagnosis and Management. Philadelphia: WB Saunders, 1970, pp 121–129 Manuscript received April 6, 2004. Accepted in final form November 1, 2004. Address reprint requests to: Tomoaki Terada, M.D., Department of Neurological Surgery, Wakayama Medical University, 811–1 Kimiidera, Wakayama City, 641–0012 Japan. email: teradato@ wakayama-med.ac.jp. J. Neurosurg. / Volume 102 / March, 2005