Abstract

BACKGROUND:

There is a theoretical concern that a thrombus may be dislodged distally when crossing the occluded segment during recanalization of a complete occlusion.

OBJECTIVE:

To assess the immediate postprocedural brain diffusion-weighted image (DWI) findings following endovascular recanalization using an embolic protection device for proximal internal carotid artery (ICA) occlusion.

MATERIALS AND METHODS:

We retrospectively identified 12 patients who underwent stent implantation for sudden symptomatic occlusion of the proximal ICA. In 8 patients, no additional intracranial occlusions were identified. In 4 patients, an additional intracerebral thrombus was detected in the middle cerebral artery. Distal protection devices were used in all cases. We evaluated the presence and amount of retrieved embolic fragments in the distal protection devices. The incidence and location of postprocedural emboli were determined using DWI.

RESULTS:

Recanalization of the proximal ICA was achieved in all patients. After complete occlusion of the proximal ICA was demonstrated, primary passage of the embolic protection device through the occluded ICA was gently navigated in 7 patients. However, this was not possible in 5 patients. Three patients developed new lesions on postprocedural DWI. Of the 12 patients in which distal protection devices were used, debris was detected in 7 patients.

CONCLUSION:

In endovascular revascularization of proximal ICA occlusion, postprocedural emboli occur less frequently than reported in a systematic review of the DWI literature. The real risk of dislodging thrombi appears to be from plaque fragment mobilization by angioplasty, rather than from crossing an occluded segment.

Embolization that derives from plaque fragment mobilization is a well-known complication of endovascular therapies, and cerebral protection devices have been developed and are currently being used widely in carotid artery stenting (CAS) procedures to limit cerebral embolism. The role of cerebral protection during an endovascular procedure for revascularization is still under investigation, but cerebral protection is feasible and effective, and it appears to reduce the risks of postprocedural neurologic events.1

Compared with angioplasty for stenotic lesions in the internal carotid artery (ICA), the application of distal protection devices in complete ICA occlusion is a concern in which the thrombus may be dislodged distally when crossing the occluded segment in the ICA. However, in acute symptomatic ICA occlusion, there are strong associations between recanalization and clinical outcomes.2 Some authors have reported successful recanalization of patients with acute stroke symptoms secondary to ICA occlusion in a case report and case series with or without protection devices.35

We performed a postprocedural brain diffusion-weighted image (DWI) immediately following endovascular recanalization using embolic protection devices for proximal ICA occlusion to assess the risk of dislodging thrombi while crossing an occluded segment.

MATERIALS AND METHODS

Patients

Twelve patients with segmental occlusion of the proximal ICA were treated with CAS with a distal protection device. Our definition of a proximal ICA occlusion was nonvisualization of the cervical ICA, with a patent petrous portion and siphon due to retrograde filling of the ICA via the circle of Willis and the ophthalmic artery, which was defined by Kniemeyer et al.68 Ten patients were male and 2 were female. The age ranged from 58 to 87 years, with a mean of 69.4 years. In 8 patients, no additional intracranial occlusions were detected at the time of angiography and/or other imaging studies, including contrast enhanced magnetic resonance angiography (MRA) or computed tomography angiography (CTA), obtained before the intervention. In 4 patients, an additional intracerebral thrombus was detected at the time of angiography and/or other imaging studies (MRA or CTA) before the intervention in the middle cerebral artery (MCA). Sudden severe symptomatic occlusion of the proximal ICA occurred in all cases with the exception of a patient with a proximal ICA occlusion and transient dysarthria.

CAS Procedure

All 12 patients underwent a complete physical and neurological examination before and immediately after the endovascular intervention. Written informed consent for endovascular thrombolysis was obtained from each patient and/or their relatives after giving a thorough explanation of the risks and benefits of the procedure. Angiography was performed using a monoplane (Advantx LCA; General Electric, Paris, France) or biplane angiography unit (Axiom Artis; Siemens, Erlangen, Germany). Diagnostic angiograms of both common carotid arteries or ICAs and both vertebral arteries were initially performed to confirm the presence of an occlusion and evaluate the retrograde filling of the cervical ICA. The luminal diameter of the cervical ICA was also analyzed.

CAS was performed under local anesthesia and full anticoagulation, a 3000 to 5000 IU bolus of heparin (50 IU/kg of body weight), followed by continuous infusion of 1000 to 2000 IU of heparin per hour to double the baseline activated clotting time.

An 8F cerebral guiding catheter was introduced into the common carotid artery via the transfemoral route unilaterally. A distal protection device (FilterWire, Boston Scientific, Natick, Massachusetts, and SpideRx, eV3, Plymouth, Minnesota) was advanced through the proximal ICA occlusion first. Care was taken to probe the origin of the occluded ICA gently with a distal protection device. If there was little or no resistance to probing, a distal protection device was gently advanced into the high cervical ICA, usually the petrous portion of the ICA. After placement of the distal protection device, the proximal ICA occlusion segment was predilated with a coronary balloon (2-3 mm) (Sprinter balloon catheter; Medtronic, Inc., Minneapolis, Minnesota). Following predilatation, a self-expanding stent (Carotid Wallstent, Boston Scientific, Galway, Ireland; and Precise, Cordis, Miami Lakes, Florida) was placed across the occlusion, followed by postdilation using a 4- to 6-mm-diameter balloon (Amiia balloon catheter, Johnson & Johnson, New Brunswick, New Jersey; and Ultrasoft-SV, Boston Scientific Co., Natick, Massachusetts) (Figure 1). If there was resistance to probing the placement of the distal protection device, a steerable guide wire was gently negotiated from the ipsilateral common carotid artery through the occlusion into the distal cervical ICA. Attempts were made to cross the lesion with a 0.014-inch microwire (Transcend-14; Boston Scientific Co., Natick, Massachusetts) in most cases. The microcatheter was then advanced over the wire into the distal ICA, where manual injection of contrast was performed to confirm the position within the true lumen and to determine the length of the occlusion. The microcatheter was exchanged for a small-diameter coronary angioplasty balloon (2.0 or 3.0 mm) (Sprinter balloon catheter; Medtronic, Inc., Minneapolis, Minnesota), which was inflated to 6 to 8 atm to predilate the occlusion (Figure 2). A distal protection device was then advanced parallel to the microwire and deployed in the high cervical ICA, usually the petrous portion of the ICA. A self-expanding stent (Carotid Wallstent or Precise) was then placed across the occlusion, followed by postdilation using a balloon, 4 to 6 mm in diameter.

FIGURE 1.

CAS procedures in proximal ICA occlusion in case 6. A, confirmation of an ICA occlusion. Left carotid angiogram shows occlusion at the origin of the ICA. B, confirmation of a proximal ICA occlusion: visualization of the cervical ICA due to retrograde filling of the ICA via the circle of Willis and/or ophthalmic artery. C, navigation of a distal protection device. A distal protection device is placed at the high cervical ICA. The luminal diameter of the deployed area of a distal protection device is less than 3 mm. D, stenting and postdilatation. The diameter of the distal ICA of the occlusion, including the deployed area of a distal protection device (arrow), is dilated more than 4 to 5 mm. E, preprocedural DWI (upper 2 rows) shows multiple small high signal intensities in the left cerebral hemisphere (both ACA and MCA territories). Postprocedural DWI (lower 2 rows) shows no new lesions on the postdilatation DWI. ACA, anterior cerebral artery; DWI, diffusion-weighted image; ICA, internal carotid artery; MCA, middle cerebral artery.

FIGURE 1.

CAS procedures in proximal ICA occlusion in case 6. A, confirmation of an ICA occlusion. Left carotid angiogram shows occlusion at the origin of the ICA. B, confirmation of a proximal ICA occlusion: visualization of the cervical ICA due to retrograde filling of the ICA via the circle of Willis and/or ophthalmic artery. C, navigation of a distal protection device. A distal protection device is placed at the high cervical ICA. The luminal diameter of the deployed area of a distal protection device is less than 3 mm. D, stenting and postdilatation. The diameter of the distal ICA of the occlusion, including the deployed area of a distal protection device (arrow), is dilated more than 4 to 5 mm. E, preprocedural DWI (upper 2 rows) shows multiple small high signal intensities in the left cerebral hemisphere (both ACA and MCA territories). Postprocedural DWI (lower 2 rows) shows no new lesions on the postdilatation DWI. ACA, anterior cerebral artery; DWI, diffusion-weighted image; ICA, internal carotid artery; MCA, middle cerebral artery.

FIGURE 2.

Resistance to probing the placement of the distal protection device in case 5 who had transient dysarthria. A, the severely stenotic lesion (2 months ago, not seen) progress to complete occlusion at the proximal ICA. B, there is visualization of the short segment occlusion at the proximal ICA only on CTA (arrow). C, there is resistance to probing the placement of the distal protection device. A small-diameter coronary angioplasty balloon is inflated to 6 to 8 atm to first predilate the occlusion. D, after stenting and postdilatation, there was full dilatation of the proximal and distal carotid artery. CTA, computed tomography angiography; ICA, internal carotid artery.

FIGURE 2.

Resistance to probing the placement of the distal protection device in case 5 who had transient dysarthria. A, the severely stenotic lesion (2 months ago, not seen) progress to complete occlusion at the proximal ICA. B, there is visualization of the short segment occlusion at the proximal ICA only on CTA (arrow). C, there is resistance to probing the placement of the distal protection device. A small-diameter coronary angioplasty balloon is inflated to 6 to 8 atm to first predilate the occlusion. D, after stenting and postdilatation, there was full dilatation of the proximal and distal carotid artery. CTA, computed tomography angiography; ICA, internal carotid artery.

A final ipsilateral carotid angiogram was performed to confirm reestablishment of antegrade flow and to evaluate the luminal diameter of the distal protection device deployment area in the cervical ICA. The intervention was considered a technical success if the occlusion was crossed and stented, with a final residual stenotic diameter less than 20%, and thrombolysis in myocardial infarction (TIMI) antegrade flow grade 3. After the procedure, the patient received 100 mg of aspirin and 75 mg of clopidogrel (Plavix; Sanofi-Synthelabo, Inc., Seoul, Korea) daily for 1 year. In addition, low-molecular-weight heparin (2850 IU/0.3 mL) (Fraxiparine; Sanofi-Synthelabo, Inc.) was subcutaneously administered twice daily for 2 days.

Data Collection

All clinical, angiographic, and procedural data were retrospectively collected from the medical chart and recorded on standardized forms by a physician. The presence and amount of retrieved embolic fragments in the distal protection devices were evaluated. The amount of retrieved embolic material was classified as mild, moderate, or large. A mild amount of retrieved embolic material was defined as absence of hemodynamic blood flow disturbance, and no embolic fragments detected within the distal protection device. A moderate amount of retrieved embolic material was defined as absence of hemodynamic blood flow disturbance with detection of embolic fragments within the distal protection device. A large amount of retrieved embolic material was defined as temporary occlusion of the ICA by debris.

All patients underwent DWI just before and within 24 hours after endovascular revascularization. The incidence and location of acute, postprocedural microemboli were determined by new signal intensities on postprocedural DWI.

RESULTS

Technical Results

Successful recanalization of the occluded proximal ICA segment was achieved in all patients. There was no vessel perforation or extravasation. After complete occlusion of the proximal ICA was demonstrated, primary passage of the embolic protection device through the occluded ICA was gently navigated in 7 patients. However, this was not possible in 5 patients in whom mechanical resistance was encountered during passage. Therefore, once the microwire crossed the occluded segment, a small-diameter coronary angioplasty balloon was used to cross the lesion and advance the embolic protection device (Table 1). After placement of the embolic protection device, angiography was performed and confirmed underlying atherosclerotic stenosis in all cases.

Table.

Patient Characteristics, Procedure Materials, and DWI Findingsa

No distal ICA occlusion was found after recanalization in any of the 12 patients. In 4 patients, an additional intracerebral occlusion was detected at the time of angiography and/or other imaging studies (MRA or CTA) in the MCA (M1 segment) before the intervention. In 4 patients with occlusions of the M1 segment, all received mechanical thrombolysis using a guidewire (Agility; Cordis Endovascular, Miami. Lakes, FL). After selective mechanical thrombolysis of the intracerebral thrombus, complete recanalization of TIMI 3 was achieved in 1 patient, partial recanalization of TIMI 2 in 2 patients, and failed recanalization in 1 patient.

Debris was not detected in 5 patients (mild); the presence of debris was detected in 7 of 12 patients that received distal protection devices. In 4 of 7 patients (moderate), embolic fragments were detected without hemodynamic flow disturbances. In 3 of 7 patients (large), temporary reocclusion of the ICA by debris was encountered, and the occluded ICA was recanalized after retrieving the distal protection devices.

Imaging (DWI and Angiography) Results

On the postprocedural DWI, 3 patients developed new focal brain lesions (Figure 3). Among the 3 patients, one experienced an additional M1 occlusion with new infarctions in the MCA territory after selective thrombolysis of the M1 occlusion. In 2 patients with no additional intracerebral occlusions, small infarctions in the MCA territory or the border zone were demonstrated. The remaining 9 patients developed no new lesions on the immediate DWI (Figure 1). Among 3 patients that developed new lesions on the postprocedural DWI, 2 patients developed new focal brain lesions (2/7, 29%) in the group where the occlusion was crossed with the filter (7 patients) and 1 patient developed new focal brain lesions (1/5, 20%) in the group where the lesion was crossed and had angioplasty before the filter was deployed (5 patients).

FIGURE 3.

New lesions on the postprocedural DWI in case 4. A, confirmation of an ICA occlusion. Carotid angiogram shows occlusion at the origin of the ICA and retrograde filling of the distal ICA through the ophthalmic artery. B, after stenting and postdilatation, there was full dilatation of the proximal and distal carotid artery. C, preprocedural DWI (left) reveals multiple small high signal intensities in the left cerebral hemisphere, especially in the border zone. Postprocedural DWI (right) reveals multiple new embolic lesions in the frontoparietal lobe (arrows). DWI, diffusion-weighted image; ICA, internal carotid artery.

FIGURE 3.

New lesions on the postprocedural DWI in case 4. A, confirmation of an ICA occlusion. Carotid angiogram shows occlusion at the origin of the ICA and retrograde filling of the distal ICA through the ophthalmic artery. B, after stenting and postdilatation, there was full dilatation of the proximal and distal carotid artery. C, preprocedural DWI (left) reveals multiple small high signal intensities in the left cerebral hemisphere, especially in the border zone. Postprocedural DWI (right) reveals multiple new embolic lesions in the frontoparietal lobe (arrows). DWI, diffusion-weighted image; ICA, internal carotid artery.

On angiography, the luminal diameter of the deployed area of the distal protection device (usually the petrous portion of the ICA) was less than 3 mm in all patients. After stenting and/or angioplasty, the diameter of the distal ICA, from the occlusion, including the deployed area of the distal protection device, was dilated to more than 4 to 5 mm in all patients (Figure 1D). The length of the occluded segment was predicted based on careful analysis of angiography and other imaging studies (contrast-enhanced carotid MRA or CTA) in all patients. The occluded segment was short and confined to the occluded proximal ICA in all patients. No patient experienced thrombosis inside the nonopacified proximal ICA.

Clinical Results

The average National Institutes of Health Stroke Scale score was 17.7, with the exception of 1 patient who presented with transient dysarthria. The clinical details of each patient are summarized in Table 1. No new neurological deficit related to the treated lesion was evident during or after the procedure. After stent placement, 9 of 12 patients including a patient with a proximal ICA occlusion and transient dysarthria had improved markedly, whereas 3 cases showed no change.

DISCUSSION

Revascularization of carotid occlusion in the context of acute stroke is controversial and is not currently the standard of care. Among patients with acute ICA occlusion presenting with severe neurological deficits, 16% to 55% will die, 40% to 60% will have severe neurological disabilities, and only 2% to 12% will have a good functional recovery.9 There is a firm association between recanalization and clinical outcome.2 Some authors have reported successful recanalization in patients with symptoms of acute stroke secondary to ICA occlusion in case reports or series with or without distal protection devices.2,3,913 The literature on stent placement and angioplasty of a completely occluded ICA shows successful revascularization in 73% to 100%.35 Although good results have been reported from several centers, concerns have been raised regarding dislodgment of thrombi while crossing the occluded segment by any device.14 Although several authors have reported the application of distal protection devices in acute ICA occlusion in case series,35 CAS with a distal protection device has not gained popularity in the management of ICA occlusion. Among various reasons is the risk of embolization while crossing the occluded segment.

In this study, we performed a postprocedural brain DWI immediately after endovascular recanalization using embolic protection devices for proximal ICA occlusion to assess the risk of thrombi dislodgment while crossing the occluded segment, and evaluated the presence and amount of retrieved embolic material in the distal protection devices. This is the first case series to evaluate the frequency and significance of thrombi dislodgment associated with revascularization procedures involving complete ICA occlusion.

DWI is a very sensitive and specific technique for diagnosing cerebral ischemia. This technique is widely accepted as a marker of ischemic complications in many interventional and surgical procedures.15,16 In a systematic review of the literature, application of cerebral protection devices (33% [with] vs 45% [without]; P < .01) significantly reduced the incidence of new ipsilateral DWI lesions after CAS.17

There are 3 distinctively different approaches to cerebral protection: distal occlusion balloons, distal filtration devices, and proximal occlusion catheters (Parodi's system). Each approach has its own strengths and weaknesses.14

In this study, distal embolic protection devices were used (distal filtration devices) instead of distal occlusion balloons and proximal occlusion catheters (Parodi's system). This was based on the presumption that the patient had short segment occlusion in the proximal ICA, which did not extend to the petrous segment, and that the risk of artery-to-artery embolism in the ICA occlusion traversing an occluded vascular segment would be low owing to the absence of antegrade flow.5

In this series, the length of the occlusion was usually determined by contrast-enhanced carotid MRA or CTA before the intervention (Figure 2); a small manual injection of contrast media was also performed via microcatheter to confirm distal ICA patency in the patients in whom the protection device could not be passed primarily.

All patients were treated with the FilterWire EZ Embolic Protection System (FilterWire EZ), except for one. This is based on the assumption that the distal artery was markedly collapsed in the occluded ICA, which will then be markedly dilated following recanalization.

Size selection of a distal protection device is based on the reference vessel diameter in the area where the filter basket will be expanded. In most of the distal protection devices, a filter with a slightly larger diameter (1-1.5 mm) than the reference vessel diameter was selected. However, in our experience, the vessel diameter in the area where the distal protection device will be deployed was less than 3 mm based on angiography. After stenting and/or angioplasty, the diameter of the distal ICA of the occlusion, including the deployed area of a distal protection device, was dilated more than 4 to 5 mm in all patients. Therefore, we concluded that a free-sized distal protection device, such as the FilterWire EZ Embolic Protection System, would be more useful than a size-dependent device (such as the SpideRX). The free-sized distal protection device was covered fully, even if the vessel diameter in the area where the distal protection device was deployed was markedly dilated. Traversing an occluded vascular segment has been described in coronary arteries, bypass grafts, and the extremities.12

In theory, there is a risk of dislodging thrombi while crossing the occluded segment. In this study, 3 patients developed new focal brain lesions on the postprocedural DWI, of whom one had an additional M1 occlusion and demonstrated new infarctions in the MCA territory after selective thrombolysis of the occlusion. Two patients with no additional intracerebral occlusions had small infarctions in the MCA territory or border zone. The actual risk of dislodging a trailing thrombus in the ICA distal to the occlusion was observed in only 3 of 12 patients. The remaining 9 patients did not develop new lesions on the immediate DWI. Among 3 patients that developed new lesions on the postprocedural DWI, 2 patients developed new focal brain lesions (2/7, 29%) in the group where the occlusion crossed with the filter (7 patients) and 1 patient developed new focal brain lesions (1/5, 20%) in the group where the lesion crossed and had angioplasty before deployment of the filter (5 patients). Even if there is a theoretical concern that a thrombus may be dislodged distally, when crossing the occluded segment during recanalization of a complete occlusion, the actual rate of new lesions was roughly the same on the DWI when compared with a systematic review of the medical literature.17

In our experience, even when the dislodged thrombi were not detected on angiography, they were observed on the DWI. The incidence of new ipsilateral DWI lesions was 25% (3/12), lower than reported in a systematic review of the literature.17 However, the results of this study are limited by the small number of cases studied. Even if distal embolic protection devices were used (distal filtration devices) in this study, the fact that the proximal occlusion catheters (or other commercially available flow-diversion devices) do not need to cross the lesion to provide protection is especially valuable when plaques associated with a tight stenosis or with a tortuous ICA are being treated.14 In cases of carotid artery occlusion, such as in this case series, the ability of the proximal occlusion catheter to prevent embolization before crossing the lesion with a guidewire may be an important advantage over other distal protection devices.14 Especially if there is resistance to probing the placement of the distal protection device initially, a proximal occlusion catheter with a balloon that could be inflated to create flow arrest or flow-diversion devices should be considered.

The presence of debris was detected in 7 of 12 patients with the use of distal protection devices. In 3 of 7 patients, temporary reocclusion of the ICA by debris was detected; the occluded ICA was recanalized after retrieving the distal protection devices. The poststent dilatation appears to be a major source of distal emboli over the initial passage across the occlusion.

CONCLUSION

Although this study has many limitations, postprocedural emboli occur less frequently than reported in a systematic review of the literature on DWI in endovascular revascularization of proximal ICA occlusion. The real risk of dislodging thrombi appears to be due to plaque fragment mobilization by angioplasty rather than to crossing an occluded segment. The application of cerebral protection devices significantly reduced the incidence of new distal emboli, even when an ICA was completely occluded.

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COMMENTS

Baik et al report diffusion-weighted imaging (DWI) changes postrevascularization in their limited but important series of 12 patients with acute, symptomatic carotid artery occlusions. They report a 100% revascularization rate with 25% of patients exhibiting new DWI changes on poststenting magnetic resonance imaging. None of these DWI changes were reported as being symptomatic. The authors compared their DWI rate with that reported in 2008 by Schnaudigel et al1 for a series of patients after routine carotid artery stenting. Schnaudigel et al reported a 37% rate of DWI changes poststenting. By comparison, fewer DWI changes were seen in this current series of patients with carotid occlusions. Baik et al contend that their use of distal protective devices was important because crossing the occlusion does not lead to as much embolic debris as poststenting angioplasty. In defense of this, the authors showed that debris was found in the filter after it was retrieved in 58% of patients.

We contend that carotid occlusions are often best opened with proximal protection in place, either with commercially available flow-diversion devices or with a guide catheter that has a balloon that can be inflated to create flow arrest. Even if the interventionist prefers to use distal protection, nothing is lost by using a balloon-guide catheter for proximal protection if the lesion cannot be crossed easily. The authors should consider a safer technique for opening carotid occlusions.

Opening of acute carotid occlusions should be reserved for symptomatic patients or patients who have significant perfusion asymmetry as seen on computed tomographic perfusion imaging or magnetic resonance perfusion imaging.

Mandy J. Binning

Elad I. Levy

Buffalo, New York

SK Baik et al report on a series of 12 patients who underwent carotid artery stenting after deployment of a distal protection device in the setting of acute symptomatic, short-segment proximal ICA occlusion. In 5 of the 12 patients, the distal protection device could not be navigated past the occlusion primarily and predilation with balloon angioplasty was required. Once the distal protection device was deployed, the occlusion was successfully recanalized in all of the patients by use of a self-expanding carotid stent followed by balloon angioplasty. Three of these patients developed new lesions on diffusion-weighted MRI which could be interpreted as the distal release of embolic material as a direct result of the recanalization process. The authors advocate for use of a distal protection device in this clinical scenario arguing that the rate of new DWI lesions is greater if a distal protection device is not used (as assessed from a systematic review). They theorize that distal embolization in this setting is caused by clot dislodgement at the time of angioplasty or stenting, and not from advancement of the distal protection device through the occlusion.

This study is significantly limited by a small sample size. The role of the distal protection device in acute ICA occlusion is however a very important question and calls for a head-to-head comparison before its use can be firmly advocated. At this point, I think it is reasonable to consider this as a reasonably safe and effective practice option although the data are still too sparse to accept this as the optimal or definitive management strategy.

Luke Tomycz

Robert A. Mericle

Nashville, Tennessee

1.
Schnaudigel S, Groschel K, Pilgram SM, Kastrup A. New brain lesions after carotid stenting versus carotid endarterectomy: a systematic review of the literature. Stroke. 2008;39:1911-1919.

ABBREVIATIONS

    ABBREVIATIONS
  • CAS

    carotid artery stenting;

  • CTA

    computed tomography angiography;

  • DWI

    diffusion-weighted image;

  • ICA

    internal carotid artery;

  • MCA

    middle cerebral artery;

  • MRA

    magnetic resonance angiography;

  • TIMI

    thrombolysis in myocardial infarction