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(Stroke. 1997;28:2563-2567.)
© 1997 American Heart Association, Inc.

Articles

Timing of Carotid Endarterectomy After Stroke

Michael B. Pritz, MD, PhD

From the Section of Neurological Surgery, Indiana University School of Medicine, Indianapolis, Ind.

Correspondence to Michael B. Pritz, MD, PhD, Section of Neurological Surgery, Indiana University School of Medicine, 545 Barnhill Dr, Emerson 139, Indianapolis, IN 46202-5125. E-mail michael-pritz{at}iucc.iupui.edu

	Abstract

Top Abstract Introduction Background Intracerebral Hemorrhage After... Cranial CT and Timing... Reports Favoring Early Carotid... Data Interpretation Stratification of Patients With... References

 
Background Timing of carotid endarterectomy after stroke in a patient with a fixed neurological deficit remains an important but unresolved question. Early surgery has been associated with cerebral hemorrhage and infarct extension. Delayed endarterectomy exposes the patient to recurrent stroke and carotid occlusion. This review investigates the hypothesis that timing of surgery after stroke influences outcome and complications.

Summary of Review This analysis critically evaluates peer-reviewed reports that retrospectively examined outcome after surgery performed "early" and "late" after stroke. The basis for intracerebral hemorrhage after endarterectomy is discussed. Clinical features that influence outcome are investigated.

Conclusions Patients undergoing carotid endarterectomy are considered a heterogeneous group based on the following features: presence of low density on cranial CT, vascular territory of the infarct, brain shift, and level of consciousness. While critical review of these retrospective studies suggests that some patients with an acute stroke can safely undergo endarterectomy shortly after the diagnosis is made, direct answers to these questions of timing of endarterectomy after stroke are best addressed by prospective studies. Nevertheless, the present review provides a basis for decision making in certain patients and for the design of future investigations.

Key Words: carotid endarterectomy • cerebral hemorrhage • surgical treatment

	Introduction

Top Abstract Introduction Background Intracerebral Hemorrhage After... Cranial CT and Timing... Reports Favoring Early Carotid... Data Interpretation Stratification of Patients With... References

 
The benefits of carotid endarterectomy in the prevention of stroke in symptomatic patients with high-grade cervical carotid stenosis have been unequivocally established by recent, randomized, prospective clinical trials.^{1 2 3} However, as the surgical risk increases, the value of endarterectomy decreases. When the chance of stroke during endarterectomy rises to 10% or higher, the benefits of surgery largely disappear.⁴ While the likelihood of complications of endarterectomy can be stratified according to neurological, medical, and radiological factors,⁵ timing of surgery after stroke can also affect outcome. Early surgery for the stenotic but patent cervical internal carotid has been associated with ipsilateral cerebral hemorrhage^{6 7} as well as extension of infarct.⁸ On the other hand, delay in endarterectomy exposes the patient to a 2% to 21% risk of recurrent stroke^{9 10 11 12 13} or the possibility of carotid occlusion.¹⁴ How soon after a recent stroke can carotid endarterectomy be safely performed in a patient with a fixed neurological deficit? This review addresses this topic. Endarterectomy for acute carotid occlusion, crescendo transient ischemic attacks (TIAs), and stroke-in-evolution are separate issues and not discussed further.

	Background

Top Abstract Introduction Background Intracerebral Hemorrhage After... Cranial CT and Timing... Reports Favoring Early Carotid... Data Interpretation Stratification of Patients With... References

 
Cerebral hemorrhage subsequent to reconstruction of a stenotic cervical carotid artery is a well-known, although uncommon, complication of carotid endarterectomy. The initial report described 6 patients with a postoperative hemorrhage from a series of 900 individuals who underwent carotid endarterectomy.⁶ Five of the 6 patients had a recent ischemic episode with a neurological deficit at the time of surgery. In each case, surgery was performed between 2 and 6 hours after angiography. All patients had patent but high-grade cervical carotid stenosis. None of the complications took place immediately after surgery but occurred 3 to 6 days after endarterectomy. All endarterectomized vessels were patent postoperatively. These complications were attributed to restoration of blood flow into a recently ischemic area, which resulted in a hemorrhagic transformation of the infarct. Two suggestions were made. First, patients with recent cerebral infarction should be stabilized for at least 1 to 2 weeks before endarterectomy is undertaken. Second, patients in whom endarterectomy cannot be delayed should wait 24 hours after angiography before vessel reconstruction is performed.⁶

These concerns of early endarterectomy after recent cerebral infarction were reinforced by two additional reports. In one study, 5 patients from a series of 179 individuals who underwent arterial reconstructive procedures were described who developed a cerebral bleed subsequent to carotid endarterectomy.⁷ Two patients had carotid stenosis, while 3 patients had carotid occlusion. In the patients with carotid stenosis, symptoms began after an interval of several hours in one case and after 3 days in the other instance. In both patients at autopsy, the endarterectomized vessel was patent and intracerebral hemorrhage was present. These observations suggested that a critical period follows a cerebral infarction during which restoration of blood flow results in hemorrhage adjacent to the infarct.⁷ Additional support for a delay of at least 2 weeks before carotid endarterectomy came from the Joint Study of Extracranial Arterial Occlusion.¹⁵ Surgical mortality was 5% for those patients with neurological deficits of more than 2 weeks' duration compared with 42% for those with deficits of less than 14 days. Furthermore, patients with acute strokes and altered consciousness who underwent surgery 2 weeks or more after admission fared considerably better than those patients undergoing surgery within 14 days. These findings led to the conclusion that the highest complication rate was observed in patients operated on within 14 days of an acute neurological deficit.¹⁵ However, the number of patients undergoing carotid endarterectomy for a stenotic versus an occluded internal carotid artery was not stated.

These initial observations^{6 7 15} published in the era before the advent of CT suggested that carotid endarterectomy be delayed for at least 1 to 2 weeks after stroke. Others¹⁶ suggested surgery be postponed even further for 5 to 6 weeks. Together these reports^{6 7 15 16} formed the basis for delaying carotid endarterectomy for 4 to 6 weeks after acute stroke. These observations were reinforced by a retrospective report examining the results of endarterectomy after recent stroke in patients undergoing surgery 5 weeks or earlier and more than 5 weeks after cerebral infarction.¹⁷ Five strokes occurred in 27 patients (18.5%) undergoing early surgery, while no patient operated on after 5 weeks had neurological worsening. However, 1 of the 5 patients sustaining a stroke that ultimately led to death occurred in a patient who had an uneventful endarterectomy on the symptomatic vessel and then underwent surgery on the asymptomatic, opposite carotid, from which he suffered complications. Furthermore, no strokes occurred in 9 patients in this same series who underwent surgery in week 1 or 2.¹⁷ Others¹⁸ support this stance of delayed surgery.

	Intracerebral Hemorrhage After Carotid Endarterectomy

Top Abstract Introduction Background Intracerebral Hemorrhage After... Cranial CT and Timing... Reports Favoring Early Carotid... Data Interpretation Stratification of Patients With... References

 
Despite considerable advances in neuroimaging, anesthesia, surgery, and perioperative medical management, intracerebral hemorrhage after carotid endarterectomy still happens. Its occurrence, in large series, ranges from 0.3% to 1.2%.^{19 20 21 22 23} Although postoperative hypertension,^{16 20 22 23} previous cerebral infarction,^{16 20 22 23} and postoperative anticoagulant usage^{22 23} play a role, low preoperative perfusion pressure and postoperative hyperperfusion are the underlying mechanisms.^{22 23 24} The occurrence of an intracerebral hematoma subsequent to endarterectomy is not limited to symptomatic patients but has occurred in asymptomatic individuals who underwent surgery for high- grade carotid stenosis.^{23 25}

Cerebral hyperperfusion is known to occur after uncomplicated carotid endarterectomy. Postoperative ipsilateral hyperperfusion can last as long as 11 days after endarterectomy. During this period, autoregulation is impaired.²² Patients who developed intracerebral hematomas postoperatively shared several features in common. Preoperatively, they had high-grade cervical carotid stenosis and hypoperfusion based on physiological measurements. Postoperatively, hyperperfusion of the hemisphere ipsilateral to the endarterectomized vessel was documented by increased cerebral blood flow.^{22 23} Under these circumstances, it is presumed that resistance vessels of the hypoperfused hemisphere are maximally dilated preoperatively. After carotid endarterectomy has restored a normal carotid bifurcation lumen and normal blood flow, hyperperfusion will occur in the ipsilateral hemisphere until resistance vessels regain their ability to constrict and autoregulation is reestablished.²⁴ It is during this period of hemodynamic impairment that measurement and control of blood pressure are critical^{22 23} since cerebral blood flow varies directly with mean arterial pressure.²⁶ In addition to cerebral blood flow measurements and preoperative high-grade cervical carotid stenosis,^{23 24} hypoperfusion can be documented preoperatively by several means. These include measurement of the internal carotid artery/common carotid artery pressure ratio at surgery,²⁴ an inverted supraorbital flow seen on angiography or documented by Doppler ultrasound,²⁴ poor collateral supply and slow flow in the middle cerebral artery at angiography,²³ and ischemic symptoms associated with orthostatic changes.²³ Direct confirmation of postoperative hyperperfusion is done by cerebral blood flow measurements.^{22 23 24} However, symptoms of ipsilateral headaches and seizures²² in addition to hemorrhage should presume hyperperfusion, which can be indirectly confirmed by transcranial Doppler studies.²⁷

	Cranial CT and Timing of Surgery

Top Abstract Introduction Background Intracerebral Hemorrhage After... Cranial CT and Timing... Reports Favoring Early Carotid... Data Interpretation Stratification of Patients With... References

 
Although MRI of the brain is a more sensitive indicator for acute stroke than CT,²⁸ most studies investigating timing of carotid endarterectomy after acute stroke have used CT. The presence or absence of infarction on CT has been reported to have variable influence on the complications of carotid endarterectomy.

In one study,²⁹ patients undergoing elective carotid endarterectomy with CT evidence of infarction had significantly more new postoperative neurological deficits than patients with normal CT studies. Included in this group were 7 patients operated on within 7 days after stroke who had CT evidence of a new cerebral infarction. New stroke or infarct extension occurred in 2 patients.²⁹ In another report, patients undergoing urgent carotid endarterectomy (within 10 days of presentation but at an indeterminate time after symptoms) without and with CT scan evidence of infarction had vastly different outcomes.³⁰ Only 1 of 17 patients with a normal CT scan suffered a neurological deficit. This case was a reperfusion injury with cerebral hemorrhage in a patient with a fixed, neurological deficit. In patients with abnormal CT scans, 4 of 10 patients suffered postoperative neurological deterioration and 1 patient died. However, this was a heterogeneous group of patients (TIA, reversible ischemic neurological deficit, fluctuating deficit, completed stroke). It is unclear from these data which, if any, of these patients who had a fixed, neurological deficit with a completed stroke suffered neurological decline. Also, this entire group of patients included those with a free-floating thrombus (6 patients) and fresh occlusion (2 patients). On the other hand, no correlation was noted between CT scan abnormalities and neurological complications in patients undergoing delayed, elective carotid endarterectomy.³⁰

	Reports Favoring Early Carotid Endarterectomy After Stroke

Top Abstract Introduction Background Intracerebral Hemorrhage After... Cranial CT and Timing... Reports Favoring Early Carotid... Data Interpretation Stratification of Patients With... References

 
No prospective, randomized study has been undertaken to determine which patients might safely undergo carotid endarterectomy after recent stroke. Furthermore, the exact timing of surgery is also unclear. Nevertheless, several retrospective studies have documented acceptable results in patients undergoing "early" surgery performed less than 4 to 6 weeks after cerebral infarction.

A subgroup of 28 patients who underwent surgery within 2 to 30 days after stroke was identified from a larger series of carotid endarterectomy patients. Each of these patients had a small, fixed deficit and hemodynamically significant (>75%) stenosis. Fifteen (53%) of these patients had an operation within 7 days after stroke. Thirteen (62%) of 21 patients had abnormal CT scans. No patient worsened neurologically after surgery, although 1 patient died of a massive pulmonary embolus on the second postoperative day.³¹

The results of a subset of 110 patients with stroke and normal CT scans were extracted from a heterogeneous group of patients who underwent carotid endarterectomy after cerebral ischemia. Patients had surgery within 14 days of their neurological deficit. No patient had a neurological complication in the same territory as the original stroke within 30 days of surgery.⁹

Another series of 3 patients with stroke underwent surgery 1, 4, and 8 days after the onset of maximal symptoms. All patients had CT scan evidence of recent infarction and angiography that showed high-grade carotid stenosis. None of these patients worsened postoperatively or developed vasomotor paralysis or intracerebral hematoma. Meticulous blood pressure control was maintained perioperatively.³²

In a large series of 363 completed strokes and strokes with unstable neurological status, the lowest mortality (1.6%) was in those patients who had carotid endarterectomy done in the first week, while 3.4% mortality occurred in the second week and 23.3% in the third week or later. In addition, 2.2% of this entire group deteriorated, although stratification according to timing of surgery was not given. The low mortality and morbidity in patients who underwent surgery within the first week were attributed to strict control of blood pressure. The high mortality in patients in whom surgery was performed in the third week or later was associated with recurrent strokes preoperatively. Death in these 14 patients was not due to neurological complications of endarterectomy but to myocardial infarction (7 patients), pulmonary embolus (4 patients), gastrointestinal bleeding (1 patient), associated head injury (1 patient), and brain stem stroke (1 patient).¹⁰

In another series, a subset of 29 patients with a limited and stable stroke had carotid endarterectomy from 9 to 21 days after the onset of symptoms. One patient sustained a postoperative stroke (3%), and 3 patients (10%) suffered postoperative minor TIAs that resolved. Thirty-one patients with a reversible ischemic neurological deficit (defined as a deficit lasting longer than 24 hours, resolving completely within 3 weeks, and having no CT evidence of infarction) underwent carotid endarterectomy from 3 to 21 days. In this group, one postoperative stroke (3%) and one TIA (3%) occurred.³³

Another report analyzed 27 patients who underwent carotid endarterectomy within 30 days after recent stroke. Results were stratified according to neurological status and CT findings. Twenty-two neurologically stable patients with mild deficits and a normal CT and 2 patients with moderate neurological deficits and CT findings of recent infarction experienced no morbidity and no mortality. Two of 3 patients with progressive neurological deficits and CT findings of recent infarction experienced infarct extension. One of these 2 patients died.⁸

In another surgical series, 129 patients with recent stroke were preoperatively divided into two groups: early (<6 weeks, 82 patients) and late (>6 weeks, 47 patients) surgery. No significant difference in outcome was found between patients operated early versus late. No significant difference was observed between patients operated on at 2, 4, 6, or more than 6 weeks after stroke.³⁴

In a retrospective analysis, 100 patients with severe (70% to 99%) angiographically defined carotid stenosis with nondisabling hemispheric stroke at entry into the North American Symptomatic Carotid Endarterectomy Trial were divided into two groups: early and late. Early patients had carotid endarterectomy within 30 days (2 to 30 days) of stroke, while the late group had surgery after 30 days. The postoperative stroke rate was comparable between the two groups. Both strokes in the early group were in patients who had a normal noncontrast CT and an acute carotid thrombus.¹²

Preliminary results of others also support the belief that early surgery can be performed safely. An abstract³⁵ reported a retrospective study of 34 patients who underwent carotid endarterectomy within 30 days of a hemisphere stroke. Neurological deficits were noted in 1 patient contralateral to the endarterectomized carotid. No deaths occurred.³⁵

	Data Interpretation

Top Abstract Introduction Background Intracerebral Hemorrhage After... Cranial CT and Timing... Reports Favoring Early Carotid... Data Interpretation Stratification of Patients With... References

 
In a review of the endarterectomy results in relation to timing after acute stroke, several facts emerge. First, intracerebral hemorrhage after endarterectomy is most likely due to postoperative hyperperfusion and can possibly be reduced by meticulous attention to blood pressure perioperatively. Since an intracerebral bleed after endarterectomy can occur in patients without cerebral infarction undergoing elective carotid endarterectomy,^{23 25} fear of this complication in regard to timing of surgery is not a reason to delay operation. Second, several reports^{8 9 10 12 31 32 33 34 35} have documented satisfactory outcomes in patients undergoing surgery within 6 weeks of recent cerebral infarction. Third, even in the recent series with poor outcomes after early surgery,¹⁷ 9 patients had an uncomplicated carotid endarterectomy in weeks 1 and 2 after stroke. Fourth, patients undergoing carotid endarterectomy with fixed neurological deficits probably represent a heterogeneous group whose risks vary according to clinical and radiological features.⁸

	Stratification of Patients With Acute Stroke

Top Abstract Introduction Background Intracerebral Hemorrhage After... Cranial CT and Timing... Reports Favoring Early Carotid... Data Interpretation Stratification of Patients With... References

 
Patients with a stroke who are candidates for carotid endarterectomy represent a heterogeneous group. Some investigators⁵ have subdivided patients into categories according to medical, radiological, and neurological risk factors and have noted the rate of complications based on these divisions. However, review of the studies discussed previously (Table) suggests that neurological deficit, vascular territory of the stroke, infarct size, degree of shift seen on CT, and level of consciousness are features that also may influence the risk of surgery in regard to timing of endarterectomy.

View this table: [in this window] [in a new window]   Table 1. Studies Reviewed

The type and severity of neurological deficit are important features to characterize stroke patients preoperatively. A variety of sophisticated testing is available to evaluate such patients. However, this parameter has not been used to simplify the stratification of patients for two reasons. First, other factors listed below are believed to be more important in the determination of risk and would indirectly reflect the degree of neurological deficit. Second, any feature that might influence assessment of neurological status or result in variation between observer exams would be eliminated.

Vascular distribution of the stroke, size of CT hypodensity, and degree of brain shift are all parameters that can easily be assessed objectively. Since hypodensity seen on noncontrast CT can represent both infarction as well as edema, a distinction between these two features based on this study alone is difficult. The vascular distribution of the infarct is most likely an important feature. Flow to the hemisphere ipsilateral to the endarterectomized carotid is more direct to the middle cerebral artery under ordinary anatomic conditions than to other territories of the anterior circulation. This would imply that patients with middle cerebral artery stroke may be at greater risk for complications than patients with cerebral infarctions in the distribution of other vascular territories. Although clinical data to directly support this premise are lacking, one recent study investigating hemorrhagic transformation of acute cerebral infarcts indicated the importance of stroke location. This report found that medium and large middle cerebral artery territory strokes accounted for 94% of all hemorrhagic transformations.³⁶ Furthermore, patients with large cerebral infarcts have a greater tendency to develop hemorrhagic transformation than those with smaller strokes.^{37 38} Finally, patients with large cerebral infarctions are more likely to demonstrate shift of neural structures on CT. It is precisely this group of patients who would be expected to have a depressed level of consciousness, presumably as a result of increased intracranial pressure. Lethargic patients with significant shift documented by CT do not commonly undergo carotid endarterectomy, and therefore studies reporting the outcome of such patients are not available. However, extrapolation of data from the Joint Study,¹⁵ which was performed before the advent of CT, points to the importance of level of consciousness in patients undergoing surgery within the first 2 weeks after an acute stroke. Mortality was twice as great in patients with a depressed level of consciousness who had an operation within 13 days compared with those who underwent surgery after an interval of 2 weeks.¹⁵

It is tempting to stratify stroke patients undergoing carotid endarterectomy based on the presence or absence of CT hypodensity, brain shift, vascular territory of the infarct, and level of consciousness. However, since only retrospective, and not prospective, randomized studies are available, such groupings may be premature. Furthermore, other factors such as neurological deficit(s) and MRI features may also prove significant. Nevertheless, review of the studies discussed previously and listed in the Table, despite being retrospective, does allow for some suggestions regarding timing of surgery in patients with a stable neurological deficit and certain clinical and radiological features.

Patients with a stable, acute stroke (neurological deficit lasting >24 hours), a normal CT scan, and a normal level of consciousness can probably undergo carotid endarterectomy shortly after the diagnosis is made and evaluation is complete. In this instance, the risk of stroke would seem to approximate that of patients who have suffered a TIA.^{8 9 12 31 33 34 39} Patients with a low density on CT without significant shift, a stable neurological deficit, and a normal level of consciousness have been reported to safely undergo early surgery with low risk.^{8 12 31 32 35} However, the number of patients is small. Since some studies have indicated that CT evidence of stroke carries an increased risk^{29 30} despite early successful surgery,^{8 12 31 32 35} the risk of complications is probably greater than that of patients with a TIA undergoing carotid endarterectomy. Patients who have brain shift on CT with a normal level of consciousness are probably at an indeterminate increased risk for complications if endarterectomy is performed early after carotid stenosis is identified. Stroke patients who have a depressed level of consciousness presumably due to increased intracranial pressure would likely have a significant shift of neural structures on CT. Extrapolation from the observations of the Joint Study¹⁵ suggests that these individuals would likely be at substantial risk for increased neurological deficits if carotid endarterectomy is performed early.

The risk of early carotid endarterectomy in patients with an acute, stable stroke is likely influenced by factors discussed previously as well as others not considered or yet to be identified. Only prospective randomized trials can adequately address these issues. Nevertheless, this review's analysis of previous reports should provide data for decision making in the timing of carotid endarterectomy in certain patients with an acute stroke and a stable neurological deficit as well as for the design of future studies to address these unanswered questions.

	Acknowledgments

 
I thank M. Houser, C. Tomishima, and L. Green for manuscript preparation and Drs J. Biller, A. Bruno, and M. Malkoff for critical comments.

	Footnotes

 
Reviews of this article were directed by Hermes Kontos, MD.

Received June 13, 1997; revision received August 12, 1997; accepted August 27, 1997.

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				A. P. Gasecki, M. Eliasziw, and M. B. Pritz Timing of Carotid Endarterectomy After Stroke • Response Stroke, December 1, 1998; 29(12): 2667 - 2668. [Full Text] [PDF]

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