Radiographic absence of the posterior communicating arteries and the prediction of cognitive dysfunction after carotid endarterectomy

Clinical article

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Object

Approximately 25% of patients exhibit cognitive dysfunction 24 hours after carotid endarterectomy (CEA). One of the purported mechanisms of early cognitive dysfunction (eCD) is hypoperfusion due to inadequate collateral circulation during cross-clamping of the carotid artery. The authors assessed whether poor collateral circulation within the circle of Willis, as determined by preoperative CT angiography (CTA) or MR angiography (MRA), could predict eCD.

Methods

Patients who underwent CEA after preoperative MRA or CTA imaging and full neuropsychometric evaluation were included in this study (n = 42); 4 patients were excluded due to intraoperative electroencephalographic changes and subsequent shunt placement. Thirty-eight patients were included in the statistical analyses. Patients were stratified according to posterior communicating artery (PCoA) status (radiographic visualization of at least 1 PCoA vs of no PCoAs). Variables with p < 0.20 in univariate analyses were included in a stepwise multivariate logistic regression model to identify predictors of eCD after CEA.

Results

Overall, 23.7% of patients exhibited eCD. In the final multivariate logistic regression model, radiographic absence of both PCoAs was the only independent predictor of eCD (OR 9.64, 95% CI 1.43–64.92, p = 0.02).

Conclusions

The absence of both PCoAs on preoperative radiographic imaging is predictive of eCD after CEA. This finding supports the evidence for an underlying ischemic etiology of eCD. Larger studies are justified to verify the findings of this study. Clinical trial registration no.: NCT00597883 (http://www.clinicaltrials.gov).

Abbreviations used in this paper:BMI = body mass index; CA = carotid artery; CAS = CA stenosis; CBF = cerebral blood flow; CEA = carotid endarterectomy; CTA = CT angiography; DM = diabetes mellitus; eCD = early cognitive dysfunction; EEG = electroencephalography; HTN = hypertension; MI = myocardial infarction; MRA = MR angiography; PCA = posterior cerebral artery; PCoA = posterior communicating artery; PVD = peripheral vascular disease.

Object

Approximately 25% of patients exhibit cognitive dysfunction 24 hours after carotid endarterectomy (CEA). One of the purported mechanisms of early cognitive dysfunction (eCD) is hypoperfusion due to inadequate collateral circulation during cross-clamping of the carotid artery. The authors assessed whether poor collateral circulation within the circle of Willis, as determined by preoperative CT angiography (CTA) or MR angiography (MRA), could predict eCD.

Methods

Patients who underwent CEA after preoperative MRA or CTA imaging and full neuropsychometric evaluation were included in this study (n = 42); 4 patients were excluded due to intraoperative electroencephalographic changes and subsequent shunt placement. Thirty-eight patients were included in the statistical analyses. Patients were stratified according to posterior communicating artery (PCoA) status (radiographic visualization of at least 1 PCoA vs of no PCoAs). Variables with p < 0.20 in univariate analyses were included in a stepwise multivariate logistic regression model to identify predictors of eCD after CEA.

Results

Overall, 23.7% of patients exhibited eCD. In the final multivariate logistic regression model, radiographic absence of both PCoAs was the only independent predictor of eCD (OR 9.64, 95% CI 1.43–64.92, p = 0.02).

Conclusions

The absence of both PCoAs on preoperative radiographic imaging is predictive of eCD after CEA. This finding supports the evidence for an underlying ischemic etiology of eCD. Larger studies are justified to verify the findings of this study. Clinical trial registration no.: NCT00597883 (http://www.clinicaltrials.gov).

Carotid endarterectomy (CEA) is a common surgical procedure performed in patients with highgrade carotid artery stenosis (CAS). The efficacy and safety of this procedure have been demonstrated in large randomized clinical trials. Specifically, for symptomatic patients with 70%–99% CAS, the North American Symptomatic Carotid Endarterectomy Trial revealed a 16.5% 2-year reduction in nonfatal strokes and mortality from all causes with CEA versus best medical management, and a 10.1% 5-year risk reduction in patients with 50%–69% CAS.1,25 Similarly, the European Carotid Surgery Trial demonstrated an 11.6% 3-year risk reduction in symptomatic patients with > 60% stenosis.4,10 In asymptomatic patients, prophylactic CEA has been shown to be superior to best medical management in those patients with > 60% CAS.7,24,30 Importantly, the rate of disabling perioperative stroke is as low as 1%–2%, with perioperative mortality occurring in < 1% of patients undergoing CEA.2,12,15,25 Based on this, the 2011 guidelines from the American Heart Association/American Stroke Association recommend therapeutic CEA in symptomatic patients with CAS > 70% (or > 50% in select patients) and prophylactic CEA in asymptomatic patients with CAS > 60%.6,11,22

Despite the high rate of treatment success and low incidence of perioperative morbidity and mortality, studies have demonstrated subtle neurological injury in the context of early postoperative neurocognitive function in as many as 28% of patients following CEA.8,9,11,12,21,27 The underlying pathophysiology of this early cognitive dysfunction (eCD) is not completely understood, but data from a number of studies suggest that ischemic injury is a contributing factor,3,21,31,32 related to hypoperfusion during intraoperative CA cross-clamping and/or to dislodgment of atheroemboli during vessel dissection and plaque removal.

In this study, our aim was to determine whether preoperative radiographic imaging of the circle of Willis—and in particular, of collateral flow via the posterior communicating arteries (PCoAs)—is predictive of patients at risk for exhibiting eCD following CEA.

Methods

Study Subjects

Forty-two patients undergoing elective CEA at Columbia University Medical Center between January 2004 and December 2012 were eligible for inclusion in this institutional review board–approved study. This study was registered with the ClinicalTrials.gov database (http://www.clinicaltrials.gov), and its registration number is NCT00597883. All patients had undergone preoperative CT angiography (CTA) and/or MR angiography (MRA) as part of their standard preoperative care—there were no radiographic images performed solely for the purpose of this study. All patients had complete neuropsychometric evaluation preoperatively and 24 hours postoperatively. All CEA procedures were performed under general anesthesia with routine monitoring as well as continuous electroencephalographic monitoring to detect cerebral ischemia, as previously described.3,12,13,18,20,21,31 An intraoperative CA shunt was placed in 4 patients with significant electroencephalographic changes consistent with cerebral ischemia, and these patients were subsequently excluded from this study. The remaining 38 patients were included in the statistical analysis.

Preoperative Radiographic Imaging

All radiographic imaging was analyzed retrospectively by 2 medical professionals who were trained by a neuroradiologist to determine the status of the PCoAs. For each patient included in the study, the CTA or MRA image obtained closest to the date of surgery was used. The CTA images were obtained on a 16-slice multidetector CT scanner (LightSpeed RT16, GE Healthcare). The MRA images were obtained on a 3-T MR System (Signa HDxT, GE Healthcare) using 2D/3D time-of-flight pulse sequences.

Neuropsychometric Evaluation and Statistical Analysis

Cognitive function was assessed using a previously described battery of neuropsychometric tests.4,10 These tests were chosen to collectively represent a broad range of cognitive domains—motor, visuospatial, verbal memory, and executive function—in accordance with recommendations from a consensus statement on the assessment of neurobehavioral outcomes after cardiac surgery.7,24,30 All patients were evaluated preoperatively and 24 hours postoperatively with neuropsychometric testing.

Neuropsychometric test data scoring and calculations have been described previously.2,12,15,25 The criteria for eCD are based on difference scores calculated for each test, which are obtained by subtracting the preoperative test performance from the postoperative test performance at 24 hours. Similar to previous studies,6,11,22 a Z-score was generated based on the performance of a surgical reference group composed of 56 patients with lumbar laminectomy or microdiscectomy who were ≥ 60 years of age. The mean difference score of a surgical reference group was subtracted from the difference score for each CEA patient and then divided by the SD of the surgical reference group ([Difference CEA − Mean Difference Reference]/SD Reference). Therefore, each test is evaluated in units of SD of the surgical reference group's change in performance. The domains for patients with CEA were evaluated to account for both focal and global/hemispheric deficits: 1) worse performance by ≥ 2 SDs than in the surgical reference group in ≥ 2 cognitive domains, or 2) worse performance by ≥ 1.5 SDs than in the surgical reference group in all 4 cognitive domains. The neuropsychometric tests, their scoring, and performance calculations are described in greater detail in previous works.8,9,11,12,21,27

Statistical analyses were performed with SAS version 9.3 (SAS Institute, Inc.). Univariate analyses were performed to identify predictors of eCD in all 38 patients. The variables analyzed included factors related to patient characteristics (age, sex, education, body mass index [BMI], smoking history); medical history (statin use, diabetes mellitus [DM], hypertension [HTN], peripheral vascular disease [PVD], prior myocardial infarction [MI]); clinical presentation (presence or absence of ischemic symptoms of stroke or transient ischemic attack); and duration of CA cross-clamping. In addition, the integrity of the circle of Willis, as determined by the radiographic visibility of these collateral vessels on preoperative CTA and/or MRA, was analyzed as a predictor of interest for eCD.

Education (years), BMI (kg/m2), and duration of CA cross-clamping (minutes) were treated as continuous variables; the results of these analyses are expressed as the mean ± SD. Age was dichotomized at 75 years and treated as a categorical variable (> 75 or ≤ 75 years).3,21,31,32 All other factors were also treated categorically, and the results are presented as percentages of patients who satisfy the criteria for that variable. For univariate analyses, Student t-test, Wilcoxon rank-sum test, Fisher exact test, Pearson chi-square test, and simple logistic regression were used where appropriate. All variables with p < 0.20 in the univariate analyses were included in a subsequent multiple logistic regression model to identify independent predictors of eCD.

Results

Preoperative MRA was available for 25 patients and CTA for 17; both MRA and CTA were available for 4 patients. The time between the date of preoperative imaging and the date of CEA was 62.6 ± 142.1 days (mean ± SD). Twenty-three (60.5%) of 38 patients had ≥ 1 PCoA visualized on preoperative imaging; 11 patients had 1 visible PCoA and 12 had 2 visible PCoAs. Neither PCoA was visible in the remaining 15 patients (39.5%). Patients with no radiographically visible PCoAs were more likely to present with ischemic symptoms than patients with ≥ 1 visualized PCoA (80% vs 47.8%, p = 0.05). There were no other statistically significant differences between patients with and without radiographically visible PCoAs (Table 1). The sidedness of CAS relative to the radiographically absent PCoA was not significantly associated with eCD. Furthermore, the radiographic visibility of other collateral vessels assessed, including bilateral A1s and P1s, was not predictive of eCD following CEA.

TABLE 1:

Characteristics in 38 patients who underwent CEA*

CharacteristicAll Patients≥1 Visualized PCoANo Visualized PCoAsp Value
no. of patients382315
age >75 yrs34.2%30.4%40.0%0.54
male sex57.9%56.5%60.0%0.83
yrs of education15.0 ± 2.915.1 ± 3.214.8 ± 2.70.77
BMI, kg/m225.0 ± 3.425.0 ± 3.625.1 ± 3.30.88
smoking history57.9%69.6%40.0%0.07
statin use94.7%100%86.7%0.07
DM5.2%8.7%0%0.24
HTN57.9%69.6%40.0%0.07
PVD23.7%21.7%26.7%0.73
prior MI13.2%8.7%20.0%0.31
symptomatic status60.5%47.8%80.0%0.05
cross-clamp duration, mins44.6 ± 11.646.3 ± 12.442.1 ± 10.20.29

Values are expressed as the mean ± SD or as a percentage, as indicated.

Symptomatic status denotes a history of stroke or transient ischemic attack.

Overall, 23.7% of patients exhibited eCD. A significantly greater percentage of patients with eCD had a history of MI (33.3% vs 6.9%, p = 0.04) than did patients without eCD (Table 2). Additionally, significantly more patients with eCD had no radiographically visible PCoAs than did patients without eCD (77.8% vs 27.6%, p = 0.007). There was no significant difference in the incidence of eCD in patients with 1 or 2 radiographically visualized PCoAs (18.2% vs 0%, p = 0.22).

TABLE 2:

Univariate analyses comparing eCD status*

VariableAll PatientseCDNo eCDp Value
no. of patients38929
age >75 yrs34.2%44.4%31.0%0.46
male sex57.9%66.7%55.2%0.54
yrs of education15.0 ± 2.914.8 ± 2.815.0 ± 3.00.82
BMI, kg/m225.0 ± 3.425.9 ± 3.724.8 ± 3.30.38
smoking history57.9%66.7%55.2%0.54
statin use94.7%88.9%96.6%0.37
DM5.2%0%6.9%0.42
HTN57.9%66.7%55.2%0.54
PVD23.7%44.4%17.2%0.09
prior MI13.2%33.3%6.9%0.04
symptomatic status60.5%66.7%58.6%0.67
cross-clamp duration, mins44.6 ± 11.643.4 ± 10.945.0 ± 11.90.74
no visualized PCoAs39.5%77.8%27.6%0.007

Values are expressed as the mean ± SD or as a percentage, as indicated. To be classified as eCD, cognitive dysfunction was exhibited 24 hours after CEA.

The only variables that met criteria for inclusion in the multivariate regression model were PVD, prior MI, and absence of radiographically visualized PCoAs (Table 3). In the final multivariate model, the absence of radiographically visualized PCoAs on preoperative imaging was the only independent predictor of eCD following CEA (OR 9.64, 95% CI 1.43–64.92; p = 0.02).

TABLE 3:

Stepwise multivariate logistic regression model for patients with eCD*

VariableOR95% CIp Value
1st step
 PVD2.610.15–44.220.51
 prior MI2.730.10–73.900.55
 no visualized PCoAs9.641.43–64.920.02
2nd step
 PVD3.230.11–67.040.43
 prior MI2.190.09–92.780.64
 no visualized PCoAs13.671.86–189.470.02
 symptomatic status0.470.05–3.760.48
3rd step
 PVD3.130.12–55.60.43
 prior MI3.740.13–208.770.46
 no visualized PCoAs56.092.27–4016.880.03
 symptomatic status2.080.06–100.260.67
 interaction btwn no visualized PCoAs & symptomatic status0.080–7.130.28

Variables included in this model met criteria of p < 0.2 via univariate regression analyses presented in Table 2.

A subanalysis was performed and limited to the 17 patients in whom preoperative CTA imaging was available. In this cohort, 23.5% of patients exhibited eCD. All patients with eCD (100%) had no radiographically visualized PCoAs, whereas only 30.8% of patients without eCD had no radiographically visualized PCoAs (p = 0.03).

Discussion

The CEA procedure has been shown to be a safe and effective intervention for patients with high-grade CAS in large randomized controlled trials. Because the incidence of perioperative stroke is exceedingly rare, investigators are studying subtler forms of neurological injury, such as eCD, to increase the neurological safety of this commonly performed procedure. A number of studies have attempted to elucidate the underlying pathophysiology of this eCD,3,12,13,18,20,21,31 because it is exhibited by approximately 25% of patients after CEA. This is the first study to evaluate the adequacy of cerebral collateral circulation as a predictor of eCD after CEA.

In this study, patients were stratified according to the status of the PCoAs on preoperative radiographic imaging. Table 1 demonstrates that these subgroups were comparable with regard to a variety of baseline characteristics, with the exception that significantly more patients with no radiographically visualized PCoAs were symptomatic prior to CEA. In the context of cerebrovascular neuroanatomy, there is a clinically plausible explanation for this finding—patients without radiographically visible PCoAs presumably have less robust collateral circulation and are therefore more likely to be symptomatic in the presence of significant CAS. This explanation is supported by a prior study, in which patients with ≥ 2 ageneses/obstructions within the circle of Willis were significantly more likely to require placement of an intraoperative shunt during CA cross-clamping.23 Importantly, there was no significant difference in the incidence of post-CEA eCD in those patients in whom 1 versus 2 PCoAs were visualized on preoperative imaging. This may be a falsenegative finding attributable to the small sample size of the current study, or alternatively it may indicate that adequate collateral circulation exists in the presence of only 1 PCoA. Larger studies are necessary to further explore this question.

Well-established cardiovascular risk factors (obesity, smoking history, male sex, advanced age) and previous cardiovascular diagnoses (prior MI, PVD, DM, HTN) were not significantly different between patients with and without visualized PCoAs, suggesting that the radiographic absence of the PCoAs is not simply a reflection of diffuse systemic atherosclerotic disease. It is also noteworthy that 6 of the 38 patients included in the current study had fetal origin of 1 posterior cerebral artery (PCA). This fetal PCA was ipsilateral to the side of the CEA procedure in only 1 of the 6 patients. None of the 6 patients with a fetal PCA exhibited eCD.

In the final multivariate regression model, PCoA status was an independent predictor of eCD. Based on the existing evidence that ischemic mechanisms contribute to the manifestation of eCD, we speculate that the absence of PCoAs on preoperative CTA and/or MRA may be a radiographic marker of decreased collateral flow within the circle of Willis. It should be noted that collateral flow was adequate to maintain neuronal electrical activity, as measured by EEG. The ischemic threshold for EEG is approximately 18 ml/100 g/min, which is approximately a 60% reduction from normal baseline cerebral blood flow (CBF)—approximately 50 ml/100 g/min.5 Recently published data demonstrate that patients undergoing CEA monitored with both EEG and transcranial Doppler experience mild ischemia that is strongly associated with eCD.19 The mild ischemia most predictive of eCD is a 28% reduction in CBF; a reduction in CBF of this magnitude goes unnoticed by EEG but probably has a significant effect on the brain tissue and perhaps manifests as eCD. The findings of these recently published data along with the data presented in this study support the hypothesis that mildly ischemic conditions during CA cross-clamping play a significant role in the development of eCD.

In contrast to prior studies of eCD after CEA, our analysis did not identify certain variables that had been previously implicated as predictors of this condition: age > 75 years, DM, and statin use have been previously shown to affect the risk of eCD.11,21 However, none of these variables were significant in the univariate analyses presented here. This discrepancy may be attributable to Type 2 error (that is, false negative) in the present study, or to the nonrandomized selection of patients who underwent preoperative CTA and/or MRA. Interestingly, symptomatic status at the time of presentation was also not found to be predictive of eCD in this cohort, although we previously reported that this variable was indeed a significant predictor of eCD in a larger cohort of patients who underwent CEA. We hypothesize that the failure of the present study to identify symptomatic status as predictive of eCD is also a Type 2 error. We have therefore included the results of additional models to investigate possible confounding and interaction effects (Table 3) between visualized PCoAs and symptomatic status. The imprecision caused by the addition of more predictors in such a small sample probably limits the usefulness of these models. It is interesting to note that the point estimate for the effect of symptomatic status on eCD is directionally different in patients with no visualized PCoAs (OR = 0.17) than it is for patients with ≥ 1 visualized PCoA (OR = 2.08); however, this interaction is not statistically significant (p = 0.27). This would support the possibility that there may be an interactive effect between visualized PCoAs and symptomatic status, but the sample size is too small for it to be seen.

When interpreting the results of this study, it is important to consider the anatomical significance and reliability of PCoA status on MRA and/or CTA. In other words, do these imaging modalities provide a reliable depiction of the underlying cerebrovascular anatomy? It is well established that MRA tends to overestimate the degree of vessel stenosis, whereas CTA may provide an underestimate.26,29 This is a reflection of the distinct techniques used for image acquisition in each of these modalities. More specifically, MRA uses blood flow–dependent 3D gradient echo sequences and postacquisition computer processing to image the cerebral vasculature,16,17,28 whereas CTA relies on the high density of intravenously administered contrast material to distinguish the vascular anatomy from the surrounding tissue. Because MRA imaging is flow-dependent, bidirectional flow will lead to signal loss and the subsequent mischaracterization of a vessel as being occluded,14 when in fact the vector of CBF in one direction is merely degrading the magnitude of the vector in the opposite direction. For this reason, we performed a separate statistical analysis of the subset of patients in whom preoperative CTA imaging was available, which confirmed that the radiographic absence of both PCoAs is still significantly associated with eCD after CEA.

The findings presented here are statistically significant and supported by a reasonable scientific hypothesis. However, it is important to recognize that the clinical significance of eCD after CEA is not clearly established. Thus, whereas the inability to visualize PCoAs on preoperative CTA and/or MRA may have implications for patients with borderline indications for CEA, the relevance to the entirety of the patient population undergoing CEA is less clear.

We recognize the limitations of this study. This is a single-center retrospective study, and preoperative CTA and/or MRA imaging was not available in the vast majority of patients who underwent CEA. As a result, the sample size in the current study is small. In addition, radiographic imaging was not obtained in a prospective, randomized fashion, and so we cannot exclude the possibility of selection bias. Furthermore, CTA and MRA are not the most reliable imaging modalities for evaluating cerebrovascular anatomy; digital subtraction angiography would provide higher-resolution anatomical images, but unfortunately catheter angiography is not routinely performed preoperatively in patients undergoing CEA.

Conclusions

The objective of this study was to determine whether preoperative radiographic evaluation of collateral circulation within the circle of Willis could be used to predict which patients are likely to exhibit eCD after CEA. The data presented here suggest that the absence of radiographically visible PCoAs on preoperative CTA and/ or MRA is an independent predictor of eCD after CEA. This finding supports the evidence for an underlying ischemic etiology of eCD. Larger studies are justified to verify the findings of this study.

Disclosure

Drs. Sussman and McDowell were supported by the Doris Duke Charitable Foundation. Ms. Mergeche and Drs. Heyer and Connolly were supported in part by a National Institute on Aging grant (R01 AG17604-9).

Author contributions to the study and manuscript preparation include the following. Conception and design: Connolly, Sussman, Kellner, Mergeche, McDowell, Heyer. Acquisition of data: Sussman, Kellner. Analysis and interpretation of data: Sussman, Kellner, Mergeche, McDowell, Heyer. Drafting the article: Sussman. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Connolly. Statistical analysis: Sussman, Kellner, Mergeche, Bruce, McDowell. Administrative/technical/material support: Heyer. Study supervision: Connolly, Heyer.

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Article Information

Address correspondence to: E. Sander Connolly, M.D., 710 W. 168th St., Box 72, New York, NY 10032. email: esc5@cumc.columbia.edu.

Please include this information when citing this paper: published online July 4, 2014; DOI: 10.3171/2014.5.JNS131736.

© AANS, except where prohibited by US copyright law.

Headings

References

  • 1

    Barnett HJTaylor DWEliasziw MFox AJFerguson GGHaynes RB: Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. N Engl J Med 339:141514251998

    • Search Google Scholar
    • Export Citation
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