Journal of Vascular Surgery
Volume 47, Issue 4 , Pages 752-759, April 2008

Symptomatic acute occlusion of the internal carotid artery: Reappraisal of urgent vascular reconstruction based on current stroke imaging

Presented at the 2007 Vascular Annual Meeting, Baltimore, Md, Jun 6-10, 2007.

  • Barbara Theresia Weis-Müller, MD

      Affiliations

    • Clinic for Vascular Surgery and Kidney Transplantation, University Hospital of Düsseldorf, Heinrich-Heine-University of Düsseldorf, Düsseldorf, Germany
    • Corresponding Author InformationReprint requests: Barbara Theresia Weis-Müller, University Hospital of Düsseldorf, Heinrich-Heine-University of Düsseldorf, Moorenstr 5, 40225 Düsseldorf.
    • ,
  • Rita Huber, MD

      Affiliations

    • Clinic for Vascular Surgery and Kidney Transplantation, University Hospital of Düsseldorf, Heinrich-Heine-University of Düsseldorf, Düsseldorf, Germany
    • ,
  • Asya Spivak-Dats, MD

      Affiliations

    • Clinic for Vascular Surgery and Kidney Transplantation, University Hospital of Düsseldorf, Heinrich-Heine-University of Düsseldorf, Düsseldorf, Germany
    • ,
  • Bernd Turowski, MD

      Affiliations

    • Institute of Diagnostic Radiology, University Hospital of Düsseldorf, Heinrich-Heine-University of Düsseldorf, Düsseldorf, Germany
    • ,
  • Mario Siebler, MD

      Affiliations

    • Department of Neurology, University Hospital of Düsseldorf, Heinrich-Heine-University of Düsseldorf, Düsseldorf, Germany.
    • ,
  • Wilhelm Sandmann, MD

      Affiliations

    • Clinic for Vascular Surgery and Kidney Transplantation, University Hospital of Düsseldorf, Heinrich-Heine-University of Düsseldorf, Düsseldorf, Germany

Received 28 May 2007; accepted 12 November 2007. published online 15 February 2008.

Article Outline

Objective

We hypothesized that a subgroup of patients with frank stroke due to sudden occlusion of the internal carotid artery could safely undergo surgery to restore carotid patency and to rescue brain tissue not yet irreversibly damaged if current stroke diagnostic methods were applied.

Methods

From November 1997 to March 2007, 1810 patients underwent carotid endarterectomy of the internal carotid artery for occlusive disease at our department. Within the same period, 5369 patients were examined at our stroke unit, and 502 from this cohort underwent internal carotid artery reconstruction. A subgroup of 35 patients (28 men, 7 women; mean age, 61 ± 10 years) underwent urgent surgical revascularization due to an acute internal carotid artery occlusion ≤72 hours (mean 25 ± 17 hours) after the onset of stroke symptoms and ≤36 hours (mean 16 ± 10 hours) after admission to our stroke unit. Our diagnostic workup consisted of extracranial intracranial duplex sonography, cerebral computed tomography, digital subtraction angiography, magnetic resonance imaging, and angiography, including diffusion- and perfusion-weighted imaging, to discriminate between viable and irreversibly damaged brain tissue. The study excluded patients who presented an impaired level of consciousness, occlusion of the intracranial internal carotid artery, occlusion of the ipsilateral middle cerebral artery, or infarction more than one-third of the territory perfused by the middle cerebral artery. Imaging showed signs of recent ischemic infarction in all 35 cases. On admission, eight patients (23%) scored 0 to 2 points and 27 (77%) scored 3 to 5 points in Rankin scale.

Results

Confirmed by postoperative Doppler and duplex sonography at discharge, internal carotid artery patency could be achieved in 30 of 35 cases (86%). Intracranial hemorrhage occurred in two patients (6%) and reinfarction in another two (6%). Two patients died during their hospital stay (30-day mortality, 6%). Compared with the preoperative neurologic status, rates of clinical improvement (≥1 point in Rankin scale), stability, and deterioration were 57%, 31%, and 6%, respectively.

Conclusions

Restoration of blood flow in an acutely occluded internal carotid artery can only be achieved in the acute stage. Our pilot study demonstrated that a thorough diagnostic workup allows selection of patients who may benefit from urgent revascularization of acute internal carotid artery occlusion in the stage of an acute stroke. A prospective randomized multicenter trial comparing surgery with conservative medical treatment is needed.

 

The early attempts of the pioneers of vascular surgery to restore blood flow for acute occlusion of the internal carotid artery (ICA) often ended with catastrophic results, most likely due to postoperative intracranial hemorrhage.1, 2, 3, 4, 5 As a consequence, carotid surgery was more or less abandoned, although few experienced authors insisted that urgent surgery in selected patients could have good results.

Today, however, the diagnostic modalities available for evaluation of the vascular system and the brain are substantially different from those available at the time of the joint study.5 Ultrasound technology, angiography, and neuroimaging such as cerebral computed tomography (CT) or magnetic resonance imaging (MRI) with diffusion-weighted (DWI) and perfusion-weighted imaging (PWI) now allow for rapid and accurate diagnosis of extracranial and intracranial vascular occlusion and its associated acute ischemic stroke. Systemic thrombolytic therapy ≤3 hours after symptoms onset has been shown to be effective in reducing the severity of the neurologic sequelae of intracranial vascular occlusion.6, 7, 8, 9 Here we report a single-center experience with surgical revascularization of acute extracranial ICA occlusion in the acute stage. Our aim was to evaluate inclusion and exclusion criteria based on current diagnostic techniques to make emergency carotid surgery safe and effective.

Back to Article Outline

Methods 

Patients 

We prospectively followed up 35 consecutive patients from November 1997 to March 2007 who underwent urgent surgery for acute ICA occlusion ≤72 hours after the onset of neurologic symptoms and ≤36 hours after admission to our stroke unit. The study was approved by the local ethics committee, and patients or their close relatives gave informed consent.

During the study period, 1810 patients underwent carotid surgery for occlusive disease in our department. During this time, 5369 patients were examined at our stroke unit, and 502 symptomatic patients from this cohort were transferred to our department for ICA reconstruction. A subgroup of 35 patients (28 men, 7 women) with a mean age of 60.7 ± 10.6 years (range, 32-76 years) underwent urgent reconstruction of acute ICA occlusion within a mean of 24.1 ± 17.1 hours (median, 18; range, 6-66 hours) after symptoms onset and within a mean of 15.7 ± 9.5 hours (median, 11; range, 3-34 hours) after admission to our stroke unit.

Preoperative diagnostic work up 

All patients underwent a standardized protocol of clinical neurologic and ultrasound examination of the extracranial ICA by a staff neurologist, and all 35 patients underwent preoperative neuroimaging (cerebral CT or MRI, or both. including PWI and DWI assessment; Fig 1, Fig 2). When extracranial and intracranial ultrasound imaging was suggestive of ICA occlusion, additional MRA or digital subtraction angiography (DSA), or both, were performed to evaluate more precisely the intracranial vascular perfusion. Indications for urgent revascularization were fluctuating or progressing neurologic deficit, stroke in evolution, but also fixed, small neurologic deficits in patients with a large PWI/DWI mismatch. Patients with an impaired level of consciousness were excluded from surgery (Table). Rankin scores at the time of admission were 0 to 2 in eight patients (23%) and 3 to 5 in the other 27 (77%) patients (Fig 3).

  • View full-size image.
  • Fig 1. 

    (a) Perfusion-weighted image 4 hours after onset of stroke symptoms (Rankin 4) and before revascularization displays a perfusion deficit (red and green) of the right hemisphere, which represents “tissue at risk” for further infarction. (b) Perfusion-weighted image taken 1 week after successful revascularization of the right internal carotid artery demonstrates a perfusion deficit in the area of the definitive infarction (green), while the surrounding tissue recovered (blue). The patient remained clinically stable.

  • View full-size image.
  • Fig 2. 

    (a) Diffusion-weighted image 4 hours after onset of stroke symptoms and before revascularization of the right internal carotid artery displays white spots in the middle carotid artery perfusion area region as sign for definitely damaged brain tissue. (b) Diffusion-weighted image 1 week after successful revascularization displays an enlargement of the stroke area, which approximately has the same size as the zone of severe perfusion deficit (red color Fig 1, a), but is smaller than the total zone of impaired perfusion in the preoperative perfusion-weighted image (red and green in Fig 1, a).

Table. Inclusion and exclusion criteria for emergency surgery of acute internal carotid artery occlusion
VariableCriteria
Inclusion
Symptoms• <72 hours, fluctuating deficit, stroke in evolution, small stabile deficit
Admission to our stroke unit• <36 hours
CCT, MRI• Acute ischemic stroke <1/3 of the MCA territory
• PWI/DWI deficit
Ultrasound, DSA, MRA• Acute occlusion limited to the extracranial part of ICA
Contraindications
Symptoms• Impaired level of consciousness
CCT, MRI• Acute ischemic stroke >1/3 of the MCA territory
Ultrasound, DSA, MRA• Intracranial ICA occlusion, additional MCA occlusion
• Occlusion of the carotid T

CCT, Cerebral computed tomography; DSA, digital subtraction angiography; ICA, internal carotid artery; MCA, middle carotid artery; MRA, magnetic resonance angiography; MRI, magnetic resonance imaging.

Inclusion criteria based on imaging were a fresh ischemic brain infarction limited to not more than one-third of the territory perfused by the middle cerebral artery (MCA). Exclusion criteria were intracranial hemorrhage or infarction volume that exceeded more than one-third of the MCA perfusion area (Table). In particular, preoperative cerebral CT was performed in nine patients (26%), MRI combined with DWI and PWI in 15 (43%), and 11 (31%) were examined by both neuroimaging methods.

It should be noted that there is frequently an additional occlusion of the distal ICA, in particular in the supraclinoid segment, resulting from embolization or thrombus propagation. Surgical revascularization can only be achieved if the occlusion is limited to the extracranial ICA; therefore, visualization to confirm patency of the distal vessel is essential before performing surgical revascularization (Fig 4). Accordingly, 26 patients (74%) were evaluated by using MRA and 22 patients (63%) by a DSA alone or by both angiographic methods. Apart from ipsilateral ICA occlusion, angiography demonstrated contralateral ICA chronic occlusion in seven patients (20%). Our inclusion criterion for urgent revascularization was a fresh occlusion of the extracranial ICA. Patients with a suspected ICA occlusion older than 3 days, an occlusion of the intracranial ICA or of the ipsilateral MCA, or both, were excluded from urgent revascularization (Table).

  • View full-size image.
  • Fig 4. 

    Duplex subtraction angiography shows (a) an occlusion of the right internal carotid artery, (b) a perfusion of the right middle carotid artery, and (c) a retrograde perfusion of the “siphon.”

Surgery 

Before surgery, six patients (17%) had been treated by systemic recombinant tissue plasminogen activator lysis. Immediately after the diagnostic workup was completed, the patients were transferred to the operating theater. General anesthesia was initiated, and after exposure of the carotid bifurcation, heparin (2500 IU) was administered intravenously. The common carotid artery and the external carotid artery were cross-clamped, and a longitudinal arteriotomy of the common carotid artery extending into the ICA was performed. Chronic atherosclerotic stenosis as underlying cause for acute occlusion was treated by carotid endarterectomy (CEA). The fresh thrombus, which was present usually above the chronic bifurcation process, was either flushed out by elevating the systemic systolic blood pressure to increase the retrograde blood flow, or in case of insufficient backflow, a 2F balloon catheter was advanced with caution towards the carotid siphon and thrombectomy a was performed.

Still insufficient backflow was an indication for an intraoperative arteriography. A 4F arterial double-lumen irrigation embolectomy catheter was inserted into the distal ICA, the balloon catheter was blocked, and 20 mL of contrast medium was applied with smooth pressure to visualize the siphon region and the intracranial vessels. After adequate backflow was achieved, the arterial incision was closed with an autogenous patch graft from the great saphenous vein harvested from the ankle. Restoration of ICA blood flow was evaluated intraoperatively by pulsed Doppler sonography. In four patients, patency could not be achieved and the operation was terminated by ligation of the ICA and a thromboendarterectomy of the external carotid artery.

In two patients, ICA occlusion was due to acute dissection. In one patient, the dissecting membrane was limited to the carotid bulb and the C2 segment and was treated by removing the dissecting membrane together with the thrombus by a Fogarty maneuver and a typical carotid thromboendarterectomy. In the other patient, the dissected segment was excised and replaced using a venous interposition graft from the groin, and the distal anastomosis had to be performed at the skull base.

Postoperative treatment and follow-up 

After surgery, all patients were monitored in the intermediate or intensive care unit for 24 hours under continuous arterial blood pressure control with a systolic blood pressure between 100 and 140 mm Hg before being transferred back to the stroke unit.

During the postoperative stay and before discharge, all patients underwent a standardized clinical neurologic evaluation and duplex ultrasound (DUS) examination of the supra-aortic vessels to confirm the patency of the ICA. Cerebral CT or MRI (Fig 5) were used to re-evaluate 31 (89%) patients during their postoperative hospitalization, including especially those who had shown deterioration of their clinical status.

Follow-up 

All surviving patients were contacted by telephone. The patients were encouraged to come to our department of neurology for complete neurologic check-up and DUS examination of the neck arteries and a Doppler sonography of the intracranial circulation. Recorded was the patient’s present social and medical history, including general information on current state of health, recurrent ischemic events, hospital stays, change in medication, and newly acquired diseases. Current Rankin scores were determined by using a standardized questionnaire. If patients were not able to come to the hospital, general practitioners, practicing neurologists, and local hospitals and rehabilitation clinics were also contacted for the latest medical records such as Doppler and DUS findings of the cerebral circulation, radiologic reports, and letters of discharge. In case of death, date, the place and cause of death was documented.

Back to Article Outline

Results 

Findings during surgery 

After surgical exposure and opening of the carotid bifurcation, complete ICA occlusion was confirmed in all 35 cases. The cause of acute carotid occlusion was atherosclerotic high-grade bifurcation stenosis in 31 patients (89%), acute carotid dissection in 2 (6%), 1 (3%) with embolism from cardiac source, and 1 (3%) with heparin-induced thrombocytopenia with fresh ICA thrombus. We were able to restore blood flow in 31 of the 35 ICA occlusions (89%) but were not able to reopen the occluded ICA in the other four. The reason for failure was an old fibrotic ICA occlusion in three cases and an ICA occlusion at the siphon level with descending thrombus in another case.

Postoperative results 

The DUS check at discharge confirmed that revascularization had been successful in 30 of 35 ICA occlusions (86%). The failures comprised reocclusion in one patient during the hospital stay, and restoration of blood flow could not be achieved during surgery in 4 patients.

Neuroimaging displayed parenchymal hematoma in two patients (6%), one with mass effect and the other without clinical consequences. Reinfarction developed in two further patients (6%); of these, one patient showed a significant enlargement of his pre-existing infarction and deteriorated, and the other sustained a small embolic reinfarction without clinical consequences. Hemorrhagic transformation of the pre-existing infarction developed in four (11%) patients, but without clinical consequences.

Compared with the preoperative clinical examination, 20 patients (57%) had improved at least 1 point in Rankin scale, 11 patients (31%) remained unchanged, and two patients (6%) had deteriorated. One patient, who had been treated by systemic thrombolysis before surgery, deteriorated owing to an intracranial hemorrhage. Reinfarction developed in another patient. Two patients died in the hospital for a 30-day mortality rate of 6% (Fig 3, Fig 6). We were not able to reopen an occluded ICA in one patient who had already sustained a stroke due to brain infarction of the contralateral hemisphere. Postoperative enlargement of this ipsilateral stroke area with malignant brain edema occurred, and the patient died. Another patient died after a deep vein thrombosis with fulminant pulmonary embolism developed during the hospital stay.

In the subgroup of six patients who had been treated by systemic thrombolysis before surgery, three patients improved clinically after surgery, two patients remained stable, and one patient deteriorated due to postoperative intracranial hemorrhage.

Follow-up data 

We were able to get clinical information for 32 of 33 surviving patients (94%) with a mean follow up of 34.4 ± 23.3 months (range, 1-106 months). Five patients died during follow-up. One patient died 6 weeks after carotid revascularization of the effect of his prior stroke, and 4 patients died of causes unrelated to their cerebrovascular disease: 1 died during aortocoronary bypass surgery, 2 died of lung cancer, and 1 of an unknown cause.

Of 27 surviving patients, 13 (48%) were re-examined in our department of neurology and 11 patients (41%) in another hospital or neurologic institution. Information for three patients (11%) was obtained by a telephone call exclusively.

One of the patients in whom we had not been able to restore ICA patency presented with an ipsilateral transient ischemic attack during follow-up. One patient sustained a stroke of the contralateral hemisphere due to a hypertensive crisis. The remaining 25 patients (93%) did not have any neurologic disorders during follow-up. An asymptomatic restenosis developed in one patient, which was treated by dilatation and stenting.

Five of the 13 patients (38%) who were re-examined in our department of neurology had completely recovered from their stroke and were at Rankin stage 0. Compared with discharge, two further patients (15%) had clinically improved at least 1 point in the Rankin scale, five patients (38%) had remained stable, and one patient (8%) had deteriorated, despite CT scans that did not reveal reinfarction.

Back to Article Outline

Discussion 

Since systemic thrombolysis has proven to be effective in reducing the severity of neurologic deficit and morbidity in acute stroke, there has been increased interest in acute interventions for stroke patients.6, 7, 8, 9 Fibrinolysis alone can be effective for treatment of strokes caused by middle cerebral artery occlusion but has been shown to be ineffective in ICA occlusion, revealing a complete recanalization rate of only 10%.10 The occluded segments of intracranial arteries, such as the MCA, usually contain an embolus or a short length of thrombus in an otherwise patent healthy vessel,11, 12 whereas as shown in our study, acute occlusion of the extracranial ICA is usually due to a tight stenosis of atherosclerotic etiology at the carotid bifurcation and a superimposed thrombus. Therefore, CEA and simultaneous removal of the appositional thrombus have to be combined for restoration of blood flow. A prerequisite for successful surgery is the limitation of the ICA thrombosis to its extracranial portion, because only then can the thrombus be retrieved either by sufficient backflow or by a balloon catheter. Thus, all our patients were examined before surgery by MRA or DSA, or by both methods in selected cases, to confirm patency of the distal ICA (Fig 4).

An additional reason for preoperative angiography is the suspicion of an ICA occlusion, which develops from a tight stenosis of the intracranial portion of the ICA with a thrombus propagating from the skull base towards the bifurcation. In such cases surgery, cannot be successful and even endovascular methods, as recently shown in the Mechanical Embolus Removal in Cerebral Ischemia (MERCI) trial,13 have problems recanalizing these distal ICA occlusions. The participating study groups were able to achieve distal ICA revascularization in only 53% to 63%, with a good clinical outcome in 39% of the revascularized patients and a 90-day mortality of 30%; in the group that was not revascularized, 79% of the patients died.

The success of surgery in acute carotid occlusion partly depends on the duration of the occlusion. The occluding thrombus usually originates from the carotid bifurcation and propagates towards the skull base. The thrombus causes inflammation of the arterial wall, and organization of the thrombus begins within days after arterial occlusion. Paty et al14 reviewed their data from 87 patients who underwent surgical treatment for 90 symptomatic carotid occlusions ≤14 days of symptom onset. They were only able to restore blood flow in 31 of 90 occluded ICAs (34%).14 In contrast, we limited our time for urgent revascularization to 3 days after the very first onset of symptoms and were able to reopen 86% of the ICA occlusions. The time interval for successful recanalization may vary from patient to patient, but in general the success rate will be higher with short intervals.

Early revascularization after acute stroke is important not only to preserve perfusion of viable brain but also to salvage ischemic but not yet infarcted brain. In acute ICA occlusion, neurologic disorder occurs either due to thromboembolism while the occluding thrombus is propagating, or from hypoperfusion of the dependent hemisphere in patients with insufficient collateral blood flow.11 Magnetic resonance imaging with DWI and PWI may help to differentiate between ischemic brain tissue that is definitively and irreversibly damaged (DWI), and “tissue at risk,” hypoperfused but still viable, which may be saved by early revascularization (PWI; Fig 1, Fig 2).15, 16, 17, 18, 19, 20

Neumann-Haefelin et al18 demonstrated that PWI/DWI volume mismatch was significantly larger in stroke patients with severe ICA disease than in patients without extracranial carotid stenosis.18 The authors showed that about 80% of the patients presented with a PWI/DWI mismatch during the first 24 hours after onset of stroke symptoms. Control PWI/DWI scans 1 week later revealed an enlargement of the infarction zone in 75% of the patients if the perfusion time delay compared with the unaffected hemisphere, as demonstrated in the first scans, had been >6 seconds.18 The PWI/DWI volume mismatch on MRI was one of our most important criterion for selecting patients for urgent carotid endarterectomy.

Neurologic examination at discharge showed that more than one-half of our patients with successful revascularization had clinically improved. A prospective multicenter trial randomizing the patients into a conservative medical and a surgical group is now needed to investigate the influence of early ICA revascularization on clinical outcome and its corresponding MRI changes in a larger group of cases.

Summarizing our diagnostic algorithm, we now perform first combined MRI/MRA if carotid occlusion is suspected by Doppler/DUS imaging. An additional angiogram using DSA only becomes necessary if the supraclinoid region cannot be evaluated by MRA alone. Patients with infarctions of more than one-third of the MCA perfusion area, with occlusion of the intracranial ICA or MCA, will be excluded from urgent carotid revascularization. Patients with impaired level of consciousness will be excluded without further invasive vascular imaging studies.

Apart from a possible benefit on clinical outcome in the acute stroke situation, reopening of the ICA occlusion may prevent recurrence of stroke later in life. Chronic carotid occlusion is associated with an increased risk of 18.5% to 26% for later ipsilateral cerebral ischemia.21, 22, 23, 24 Other groups recently focused on hemodynamic failure distal to the ICA occlusion and used positron emission tomography scanning to describe the importance of hemodynamic factors in predicting outcome in these patients.23, 24 The necessity of restoring ICA blood flow is emphasized by our observation that 20% of our patients had a chronic occlusion contralateral to the acutely occluded ICA. After successful reopening of ICA occlusion, we did not observe any ipsilateral cerebral ischemia during a mean follow-up of 34 months.

Acute carotid surgery was abandoned for years because of the risk of postoperative intracranial hemorrhage. However intracerebral hemorrhage after ischemic stroke is commonly observed without invasive treatment if patients are studied with serial CT.25, 26 Okada et al25 found hemorrhagic infarction during the first month after the embolic event in 41% of the patients. The percentage of hemorrhagic infarction in their study was higher in patients aged >70 years compared with younger patients and was also higher in moderate or large infarcts compared with smaller infarcts. Of interest was that no correlation was found between hemorrhage and a previous history of hypertension or blood pressure elevation during the acute stage of stroke.25 Hornig et al26 made a similar observation, detecting hemorrhagic transformation in 43% of the cases. The risk of hemorrhage in their study was correlated with a severe neurologic deficit, disturbances of consciousness, and large infarctions with a mass effect.26 Considering these results, we excluded patients with impaired level of consciousness from consideration for emergency revascularization.

Following the example of others, we differentiated bleeding between hemorrhagic infarction and parenchymal hematoma. Hemorrhagic infarction is petechiae or confluent hemorrhage in the area of ischemic injury; parenchymal bleeding is homogeneous bleeding with circumscribed clot formation or mass effect.28, 29

For many years we routinely perform urgent carotid surgery in patients with transient ischemic attack or amaurosis fugax, but in the present study, we only included patients with frank stroke so that we could evaluate the risk of intracranial bleeding and neurologic impairment. The postoperative neuroimaging of our patients displayed parenchymal hematoma in two patients (6%), one of whom had a mass effect, and a hemorrhagic transformation of the ischemic infarction without clinical impairment in four patients (11%). The frequency of postoperative intracranial hemorrhage in our patients is comparable with the natural course of hemorrhagic transformation of ischemic cerebral infarction.25, 26

Apart from postoperative intracranial hemorrhage, reinfarction developed in two further patients (6%). One patient showed a significant enlargement of his pre-existing infarction and deteriorated, and the other one sustained from a small embolic reinfarction without clinical consequences. A postoperative stroke recurrence rate of 6% seems high compared with results of elective carotid surgery; but in general, acute carotid occlusion seems to be associated with a bad outcome. The German Stroke Study Collaboration recruited 4157 patients prospectively who had experienced an acute ischemic stroke and monitored them to assess recurrent stroke and death up to 1 year after the event. Stroke was caused by acute carotid occlusion in 366 patients. Early recurrent cerebral ischemia ≤72 hours after hospital admission was observed in 7.4% of the patients with carotid occlusion. After 100 days, already 21.2% of these patients had died.27

In the last decade, several surgical work groups published their results of urgent carotid surgery.14, 30, 31, 32, 33, 34 Kasper et al30 reported the outcome of 29 patients with revascularization for acute ICA occlusion ≤8 days of clinical presentation. In contrast to our study in which all patients had experienced a preoperative stroke, preoperative stroke had occurred in only nine (31%) patients, whereas most of the patients complained about transient ischemic attack or amaurosis fugax. Their results were similar to ours, with a successful restoration of ICA blood flow in 83%, 48% of the patients had clinically improved, 45% remained unchanged, 7% had deteriorated, and 1 patient (3%) had died.30

Gay et al32 reported 22 emergency carotid revascularizations ≤24 hours with a 30-day mortality rate of 9.5%. Berthet et al34 tried a surgical revascularization of 12 acute ICA occlusions ≤6 hours of symptoms; one patient died of stroke and another died of reasons unrelated to stroke.34 All of these work groups performed careful preoperative workup and had well-defined inclusion and exclusion criteria.

Nowadays interventional teams are also dealing with acute ICA occlusion, using new devices for mechanical thrombectomy, intra-arterial lysis, dilatation, and stenting.35, 36, 37, 38 The largest series was actually presented by a Taiwanese group, who treated 30 patients with acute cervical ICA occlusion by using endovascular techniques. In contrast with our study, intervention was not performed in acute stroke; the most recent cerebral infarction had to be ≥2 weeks before the intervention. The group was able to restore ICA blood flow in 73%. They observed one fatal brainstem infarction for a 30-day mortality rate of 3%. During a mean follow-up of 16 months, ICA restenosis developed in one patient and two others sustained reocclusion, for a reocclusion or restenosis rate of 14%. We are convinced that it is better to treat cervical ICA occlusion surgically: after clamping of the common carotid artery, the entire thrombus and atherosclerotic material can be removed without flooding blood over the embolic source, which effectively prevents embolism. Endovascular maneuvers could be considered if CEA is not an option, especially in intracranial ICA occlusions, where surgery fails and medical treatment alone has a poor outcome.14, 38, 39, 40, 41

Back to Article Outline

Conclusion 

Our preliminary study has shown that urgent revascularization in selected stroke patients with acute carotid occlusion is both technically feasible and associated with acceptable morbidity and mortality rates when preceded by careful preoperative evaluation. A prospective randomized multicenter trial is needed to confirm the validity of our findings and to assess the relative merits of aggressive vs conservative management in these patients.

Back to Article Outline

Author contributions 


Conception and design: BW, MS, WS

Analysis and interpretation: BW, AS, MS, WS

Data collection: AS, RH, BT, BW

Writing the article: BW

Critical revision of the article: RH, AS, BT, MS, WS

Final approval of the article: RH, AS, BT, MS, WS

Statistical analysis: BW, AS

Obtained funding: Not applicable

Overall responsibility: BW

Back to Article Outline

References 

  1. Wylie EJ, Hein MF, Adams JE. Intracranial hemorrhage following surgical revascularization for treatment of acute strokes. Neurosurg. 1963;21:212–215
  2. Thompson JE, Dale JA, Patman RD. Endarteriectomy of the totally occluded carotid artery for stroke. Arch Surg. 1967;95:791–801
  3. Rob GB. Operation for acute completed stroke due to thrombosis of the internal carotid artery. Surgery. 1969;65:862–865
  4. Bruetman ME, Fields WS, Crawford ES, de Bakey ME. Cerebral hemorrhage in carotid artery surgery. Arch Neurol. 1963;9:458–467
  5. Blaisdell FW, Clauss RH, Galbraith JG, Imparato AM, Wylie EJ. Joint study of extracranial occlusion. JAMA. 1969;209:1889–1895
  6. NINDS rt-PA Stroke Group. Tissue plasminogen activator for acute ischemic stroke. N Engl J Med. 1995;333:1581–1587
  7. The National Institute of Neurological Disorders and stroke rt-PA Stroke Study Group. Tissue plasminogen activator for acute ischemic stroke at one year. N Engl J Med. 1999;340:1781–1787
  8. The ATLANTIS, ECASS, and NINDS rt-PA Study Group Investigators. Association of outcome with early stroke treatment: pooled analysis of ATLANTIS, ECASS, and NINDS rt-PA stroke trials. Lancet. 2004;363:768–774
  9. Straub S, Junghans U, Jovanovic V, Wittsack HJ, Seitz RJ, Siebler M. Systemic thrombolysis with recombinant plasminogen activator and tirofiban in acute middle cerebral artery occlusion. Stroke. 2004;35:705–709
  10. Christou I, Felberg RA, Demchuk AM, Burgin WS, Malkoff M, Grotta JC, et al. Intravenous tissue plasminogen activator and flow improvement in acute ischemic stroke patients with internal carotid artery occlusion. J Neuroimaging. 2002;12:119–123
  11. Qureshi AI. Endovascular revascularization of symptomatic acute extracranial internal carotid artery occlusion. Stroke. 2005;36:2335–2336
  12. Qureshi AI, Luft AR, Sharma M, Guterman LR, Hopkins LN. Prevention and treatment of thromboembolic and ischemic complications associated with endovascular procedures: part I: pathophysiological and pharmacological features. Neurosurgery. 2001;46:1344–1359
  13. Flint AC, Duckwiler GR, Budzik RF, Liebeskind DS, Smith WS MERCI and Multi Merci Writing Committee. Mechanical thrombectomy of intracranial internal carotid occlusion (Pooled results of the MERCI and Multi MERCI part I trials). Stroke. 2007;38:1274–1280
  14. Paty PSK, Adeniyi JA, Mehta M, Darling C, Chang BB, Kreienberg PB, et al. Surgical treatment of internal artery occlusion. J Vasc Surg. 2003;37:785–788
  15. Schwamm LH, Koroshetz WJ, Sorensen G, Wang BS, Copen WA, Budzik R, et al. Time course of lesion development in patients with acute stroke (Serial diffusion- and hemodynamic-weighted magnetic resonance imaging). Stroke. 1998;29:2268–2276
  16. Staroselskaya IA, Chaves C, Siver B, Linfante I, Edelmann RR, Caplan L, et al. Relationship between magnetic resonance arterial patency and perfusion-diffusion mismatch in acute ischemic stroke and its potential clinical use. Arch Neurol. 2001;58:1069–1074
  17. Neumann-Haefelin T, Wittsack HJ, Wenserski F, Siebler M, Seitz RJ, Mödder U, et al. Diffusion- and perfusion-weighted MRI (The DWI/PWI mismatch region in acute stroke). Stroke. 1999;30:1591–1597
  18. Neumann-Haefelin T, Wittsack HJ, Fink GR, Wenserski F, Li T-Q, Seitz RJ, et al. Diffusion- and perfusion-weighed MRI (Influence of severe carotid artery stenosis on the DW/PWI Mismatch in acute stroke). Stroke. 2000;31:1311–1317
  19. Wittsack HJ, Ritzl A, Fink GR, Wenserski F, Siebler M, Seitz RJ, et al. MR imaging in acute stroke: diffusion weighted and perfusion imaging parameters for predicting infarct size. Radiology. 2002;222:397–403
  20. Seitz RJ, Meisel S, Weller P, Junghans U, Wittsach HJ, Siebler M. Initial ischemic event: perfusion weighted MR-imaging and apparant diffusion coefficient for stroke evolution. Radiology. 2005;237:1020–1028
  21. Nicholls SC, Bergelin R, Strandness DE. Neurologic sequelae of unilateral carotid artery occlusion: Immediate and late. J Vasc Surg. 1989;10:542–548
  22. Klijn CJ, Van Buren PA, Kappelle LJ, Tulleken CA, Eikelboom BC, Alagara A, et al. Outcome in patients with symptomatic occlusion of the internal carotid artery. Eur J Vasc Endovasc Surg. 2000;19:579–586
  23. Vernieri F, Pasqualetti P, Passarelli F, Rossini PM, Silvestrini M. Outcome of carotid occlusion is predicted by cerebrovascular reactivity. Stroke. 1999;30:2765–2766
  24. Grupp RL, Powers WJ. Risk of stroke and current indications for cerebral revascularization in patients with carotid occlusion. Neurosurg Clin North Am. 2001;473–487
  25. Okada Y, Yamaguchi T, Minematsu K, Miyashita T, Sawada T, Sadoshima S, et al. Hemorrhagic transformation in cerebral embolism. Stroke. 1989;20:598–603
  26. Hornig CR, Dorndorf W, Agnoli AL. Hemorrhagic transformation in cerebral embolism. Stroke. 1986;17:179–185
  27. Weimar C, Goerler M, Harmas L, Diener HC German Stroke Collaboration. Distribution and outcome of symptomatic strenosis and occlusions in patients with acute cerebral ischemia. Arch Neuol. 2006;63:1287–1291
  28. Pessin MS, del Zoppo GJ, Estol C. Thrombolytic agents in the treatment of stroke. Clin Neuropharmacol. 1990;13:271–289
  29. Jansen O, von Kummer R, Forsting M, Hacke W, Sartor K. Thrombolytic therapy in acute occlusion of the intracranial interna carotid artery bifurcation. AJNR Am J Neuroradiol. 1995;16:1977–1986
  30. Kasper GC, Wladis AR, Lohr JM, Roedersheimer LR, Reed RL, Miller TJ, et al. Carotid thromboendarterectomy for recent occlusion of the internal carotid artery. J Vasc Surg. 2002;33:242–250
  31. Huber R, Muller BT, Seitz RJ, Siebler M, Modder U, Sandmann W. Carotid surgery in acute symptomatic patients. Eur J Vasc Endovasc Surg. 2003;25:60–67
  32. Gay Jl, Curtil A, Buffiere S, Favre JP, Barral X. Urgent carotid artery repair: retrospective study of 21 cases. Ann Vasc Surg. 2002;16:401–406
  33. Sbarigia E, Toni D, Speziale F, Falcou A, Sacchetti ML, Panico MA, et al. Emergency and early carotid endarterectomy in patients with acute ischemic stroke selected with a predefined protocol (A prospective pilot study). Int Angiol. 2003;22:426–430
  34. Berthet JP, Marty-Ane CH, Picard E, Branchereau P, Mary H, Veerapen R, et al. Acute carotid artery thrombosis: description of 12 surgically treated cases. Ann Vasc Surg. 2005;19:11–18
  35. Kao HL, Lin M-S, Wang C-S, Lin Y-H, Lin L-C, Chao C-L, et al. Endovascular recanalization for cervical ICA occlusion is feasible with acceptable midterm clinical results. J Am Coll Cardiol. 2007;49:765–771
  36. Dabitz R, Triebe S, Leppmeier U, Ochs G, Vorwerk D. Percutaneous recanalization of acute internal artery occlusions in patients with severe stroke. Cardiovasc Intervent Radiol. 2007;30:34
  37. Srinivasan A, Goyal M, Stys P, Sharma M, Lum C. Microcatheter navigation and thrombolyis in acute symptomatic cervical internal carotid occlusion. AJNR Am J Neuroradiol. 2006;27:774–779
  38. Choi JH, Bateman BT, Mangla S, Marshall RS, Prabhakaran S, Chong L, et al. Endovascular recanalization therapy in acute ischemic stroke. Stroke. 2006;37:419–420
  39. Rubiera M, Ribo M, Delgado-Mederos R, Santamina E, Delgado P, Montaner J, et al. Tandem internal carotid artery/middle cerebral artery occlusion. Stroke. 2006;37:2301–2305
  40. Smith WS. Technology insight: recanalization with drugs and devices during acute ischemic stroke. Neurology. 2007;3:45–53
  41. Arnold M, Kappeler L, Nedeltchev K, Brekenfeld C, Fischer U, Keserue B, et al. Recanalization and outcome after intra-arterial thrombolysis in middle cerebral artery and internal carotid artery occlusion: does sex matter?. Stroke. 2007;38:1281–1285

 Competition of interest: none.

PII: S0741-5214(07)01785-5

doi:10.1016/j.jvs.2007.11.042

Journal of Vascular Surgery
Volume 47, Issue 4 , Pages 752-759, April 2008

Article Tools

* Image Usage & Resolution