Volume 21, Issue 7 , Pages 983-988, July 2010
One-year Cognitive Outcomes Associated with Carotid Artery Stent Placement
Article Outline
Purpose
To assess relatively long-term (ie, 1 year) neurocognitive outcomes of patients undergoing carotid artery stent (CAS) placement with cerebral protection.
Materials and Methods
Sixty-two patients (19 symptomatic; mean age, 73 years) with significant carotid stenosis (≥ 70% for symptomatic patients, ≥ 80% for asymptomatic patients) underwent CAS placement with embolic protection. Cognitive function was assessed prospectively with use of a battery of standardized tests administered at baseline (1–5 days before CAS endovascular therapy) and at 3, 6, and 12 months after CAS placement. Diffusion-weighted imaging (DWI) was performed before the procedure and within 24 hours after CAS placement.
Results
Results of statistical modeling across occasions of measurement indicated significant main effects of occasion for the Dementia Rating Scale (DRS)–2 concept formation (P < .001), memory (P = .029), and total scores (P = .001); the DRS-2 total age- and education-corrected Mayo Older Americans Normative Studies score (P < .001); and the North American Adult Reading Test IQ score (P = .003). The vast majority of patients showed improvement or no change relative to baseline DRS-2 total scores at all time points. No significant relationship between DWI outcomes and cognition scores over time was found. Age influenced improvement on cognitive tests, whereas baseline symptom status did not.
Conclusions
Revascularization with a carotid stent and neuroprotection, at a minimum, left cognitive function unchanged in patients receiving a CAS, and in many instances improved it. The preliminary findings of this prospective pilot study should be confirmed with a larger, controlled trial.
Abbreviations: 3MS, Modified Mini-Mental State Examination, BDI, Beck Depression Inventory, CAS, carotid artery stent, CEA, carotid endarterectomy, DRS, Dementia Rating Scale, DWI, diffusion-weighted imaging, LES, Learning Efficiency Sum, LOT, Learning Over Trials, MOANS, Mayo Older Americans Normative Studies, NAART, North American Adult Reading Test, PRS, Percent Retention Sum, RAVLT, Rey Auditory Verbal Learning Test
STROKE is the third most common cause of death in the United States (1). In addition to mortality, physical and cognitive morbidity associated with stroke make it the leading cause of adult disability in the United States (2). Approximately 75% of strokes occur in the distribution of the carotid arteries, with carotid occlusive and stenotic disease being a common cause. Carotid stenosis has been shown to significantly impact cognitive performance, even in the absence of stroke, possibly as a result of chronic ischemia associated with hypoperfusion (3, 4, 5).
Revascularization of carotid stenosis may improve cognitive function by restoring cerebral hemodynamics. Carotid endarterectomy (CEA) has been the “gold standard” for carotid revascularization. Recently, carotid artery stent (CAS) placement has emerged as a newer, less invasive, catheter-based alternative. Accurate assessment of the benefit of revascularization on cognitive performance is confounded by perioperative events that occur during CEA or CAS placement. For example, during CEA, hypoperfusion arising from extended carotid cross-clamping has been shown to lead to cognitive dysfunction (6). Embolic dislodgement during CEA and CAS may also lead to microembolic ischemia and cognitive decline; most centers now use cerebral protection devices during CAS procedures, the use of which appears to reduce thromboembolic complications (7).
Revascularization may have adverse and beneficial effects on neurologic outcomes, making quantification of a net effect challenging, as illustrated by three recent systematic reviews of neurocognition after CEA or CAS (8, 9, 10). All three reviews showed mixed results of improvement, no change, or decline after the procedure, but methodologic differences among the studies, including a lack of consensus on standardized tests, and different approaches to analysis of results make it difficult to compare across studies or draw accurate conclusions.
The focus of the current study is to assess relatively long-term (ie, 1 year) neurocognitive outcomes and their relationship to microembolic events of patients undergoing CAS with use of a cerebral protection device. We hypothesized that CAS with neuroprotection would result in stable neurocognitive function with no decline relative to the patient's baseline function. We also employed diffusion-weighted imaging (DWI), a valuable technique for identifying macroscopic, perioperative ischemic events that may adversely impact cognitive performance. We hypothesized that new DWI abnormalities would identify cerebral macroscopic incidents in cases in which neurocognitive function declined.
Materials and Methods
Patients
This prospective study was approved by the Food and Drug Administration as a Category B Investigational Device Exemption study, and had institutional review board approval and surveillance. Patients were recruited from the Providence Medical Center radiology department. Institutional review board–approved consent was obtained from each patient before enrollment. Patients between 18 and 90 years of age undergoing treatment for significant carotid stenosis were eligible. Symptomatic and asymptomatic patients had stenoses of at least 70% and 80%, respectively, to be eligible. Patients were ineligible if they had childbearing potential, were in other clinical trials, had evolving stroke or intracranial hemorrhage, or were allergic to critical medications. They could not have severe dementia, active bleeding or previous ipsilateral stroke with significant deficit, previous intracranial hemorrhage or brain surgery, or any other condition that would interfere with antiplatelet therapy. All patients were treated with aspirin and clopidogrel bisulfate (Plavix; Bristol-Myers Squibb/Sanofi-Aventis, Bridgewater, New Jersey) before and after the procedure. The first language of all patients was English.
CAS Placement
Technical details of the stent implantation procedure (femoral route, Seldinger technique) were described previously (11). The Rx Acculink carotid stent system and Rx Accunet embolic protection system (Abbott Vascular, Santa Clara, California) were used in all patients.
DWI
Magnetic resonance (MR) imaging diffusion sequences were performed on a 1.5-T scanner (GE Medical Systems, Milwaukee, Wisconsin) with standard DWI sequences. DWI was completed after diagnostic angiography and before CAS placement to ensure that any potential diffusion-weighted abnormalities were attributable to the carotid stent procedure and not to any preexisting condition, including spontaneous embolic events or potentially embolic events from the diagnostic angiography. DWI was repeated within 24 hours after CAS placement for comparison with the preprocedure study. Baseline and postprocedure results were compared and scored as positive or negative. Any new diffusion-weighted abnormalities caused the entire study to be scored as positive; unchanged study results were scored as negative. All studies were read by independent, board-certified neuroradiologists blinded to the neurocognitive status and outcomes of the patients. DWI abnormalities after CAS placement were recorded by an independent neuroradiologist. The vascular distribution of abnormalities was noted within the ipsilateral, contralateral, and vertebrobasilar distributions. Any noted contralateral abnormalities were evaluated for differences between treated and untreated vessels and related vasculature.
Neurocognitive Testing
Cognitive function was assessed using a battery of standardized tests administered at baseline (1–5 days before CAS and after diagnostic angiography) and at 3, 6, and 12 months after CAS placement. The battery included five well-validated measures proven to be reliable indicators of cognitive change (12), which are detailed in the subsequent paragraphs. All tests were administered by a neuropsychologist or a trained psychometrician.
The Dementia Rating Scale (DRS) (13) and its revision, DRS-2 (14), provides a standardized, quantitative, and multifaceted assessment of cognitive function in neurologically impaired populations. In addition to a global score, the DRS-2 is comprised of subscales of memory, attention, initiation/perseveration, construction, and concept formation. For comparative and diagnostic purposes, the DRS-2 has been incorporated into the Mayo Older Americans Normative Studies (MOANS) data bank. The MOANS data (15) represent one of the largest normative data sets available in the assessment of cognition in aging Americans. The Rey Auditory Verbal Learning Test (RAVLT) is a repeat-trials list-learning test that assesses immediate attention/memory, long-term retention, and the effects of interference on long-term memory (16). The RAVLT has been incorporated into the MOANS data bank; normative values from the MOANS data were used for this study. The Trail Making Test–B assesses speed of visual search, attention, and mental flexibility. It has age- and education-adjusted normalized scores available for clinical interpretation (17). The North American Adult Reading Test (NAART) (18) has been used in several CAS (19) and endarterectomy studies (8, 20) to estimate premorbid verbal intelligence. The Beck Depression Inventory (BDI) (21) and its revision, BDI-II, are used to detect depression, which is known to negatively impact most aspects of cognitive function (12), and to assess depression severity; there is a large database of aging population norms available for clinical interpretation. Mini Mental State Exam–modified, a brief screening measure of general cognitive status that has been used to assess risk in CAS studies (22). Mini Mental State Exam–modified was the only measure administered at all assessment time points. Its use within 1 week of CAS placement was intended to monitor the acute postsurgery phase.
Statistical Analysis
Independent variables were formed by assigning patients to one of two groups based on each of the following: degree of carotid stenosis at the time of enrollment (stenosis < 90% or ≥ 90% according to North American Symptomatic Carotid Endarterectomy Trial measuring technique), presence or absence of new DWI abnormalities in the post-CAS image, test attention (baseline DRS-2 attention subscale score ≤ 12 or > 12), IQ (≤ 108 or > 108 on baseline NAART score), and age (< 80 or ≥ 80 years). A trichotomous variable was formed based on the baseline DRS-2 total raw score: patients were divided into those scoring lower than 120, 120–130, and more than 130.
Neuropsychologic test data was entered into an Excel spreadsheet (Microsoft, Redmond, Washington) and transferred to SPSS for statistical analysis (version 16; SPSS, Chicago, Illinois). As the study design was within-patient repeated measures, each patient acted as their own control with performance on subsequent tests being compared with pretreatment performance.
Significant neuropsychologic performance change was defined as a change in posttreatment performance of at least 1 SD unit from the pretreatment score in accordance with general test construction theory (12) and other carotid stenosis or cardiac research groups (20). A power analysis completed on our study population indicated that a change score of 0.5 SD units could be detected (assuming an α value of P < .05 and an interoccasion correlation of 0.30) with a power of 95%. Therefore, we were confident we could satisfy the proposed definition of clinically meaningful change in test scores. After entry into the database, variables were visually examined in histograms and mean, SD, and skewness coefficients were computed.
To examine the effects of stent placement, data obtained across study periods were statistically tested using hierarchical (ie, multilevel) linear modeling. Change was assessed by entering the occasion of measurement into the model equation by itself and, in separate analyses, while controlling for preprocedure stenosis (cutoff of 90%), DWI results, age (cutoff of 80 years), attention subscale score (cutoff of 12) and IQ (cutoff of 108).
Results
Data were available for 62 eligible individuals who received a CAS (Table 1). Nineteen (31%) were symptomatic (previous ipsilateral transient ischemic attack, cerebral vascular accident, or amaurosis fugax).
Table 1. Patient Characteristics at Study Entry (N = 62)
| Characteristic | Value |
|---|---|
| Age (y) | 73 ±9 |
| Sex (%) | |
| Male | 42±68 |
| Female | 20±32 |
| Education (%) | |
| Less than high school | 14±23 |
| High school | 29±47 |
| More than high school | 19±31 |
| Smoking behavior (%) | |
| Never | 14±23 |
| Current | 15±24 |
| Past | 33±53 |
| Self report (%) | |
| Transient ischemic attack | 18±29 |
| Stroke | 16±26 |
| From medical record (%) | |
| Previous endarterectomy | 26±42 |
| Previous amaurosis | 8±13 |
| History of diabetes | 21±34 |
| History of peripheral artery disease | 19±31 |
| History of coronary artery disease | 37±60 |
| Stenosis > 90% (%) | 24±39 |
| Symptomatic (%) | 19±31 |
Table 2 contains a summary of test score means and SDs for each neurocognitive test at all occasions of measurement: baseline (ie, before CAS placement) and at 3, 6, and 12 months after stent placement. Results of statistical modeling across occasions indicated significant main effects of occasion for DRS-2 concept formation scores, DRS-2 memory scores, DRS-2 total scores, DRS-2 total age- and education-corrected MOANS scaled scores, and NAART IQ scores (Table 3). BDI-II scores showed a significant change over occasion, but when covariates were included in the model equation, the occasion effect was no longer significant. The analysis of the RAVLT recognition memory MOANS scores yielded probability levels lower than 0.10 before and after covariates were added.
Table 2. Neuropsychologic Variables Before and After Treatment
| Variable | Before CAS (N = 62) | After CAS Placement | ||
|---|---|---|---|---|
| 3 Months (n = 51) | 6 Months (n = 48) | 12 Months (n = 51) | ||
| DRS-2 attention AMSS | 11.4±2.0 | 11.6±1.7 | 11.5±1.8 | 11.9±1.7 |
| DRS-2 init/pres AMSS | 8.0±3.8 | 8.7±3.2 | 8.9±3.5 | 8.5±3.2 |
| DRS-2 construction AMSS | 9.4±1.6 | 9.5±1.4 | 9.8±1.1 | 9.8±1.2 |
| DRS-2 concept form AMSS | 8.9±2.6 | 10.0±2.4 | 10.2±2.6 | 10.8±2.2 |
| DRS-2 memory AMSS | 9.3±3.0 | 9.7±3.0 | 10.6±2.5 | 10.9±2.6 |
| DRS-2 total AMSS | 8.2±3.3 | 9.7±3.4 | 10.0±3.7 | 10.6±3.4 |
| DRS-2 AEMSS | 8.0±3.6 | 9.3±3.6 | 9.9±3.9 | 10.6±3.5 |
| BDI-II raw | 9.9±8.5 | 8.4±7.0 | 8.5±6.4 | 7.3±7.0 |
| NAART errors | 105±10 | 106±10 | 107±11 | 108±10 |
| 3MS raw | 89.7±8.4 | 91.4±6.5 | 91.9±5.9 | 92.2±6.9 |
| MMS raw | 26.7±2.6 | 27.5±1.7 | 27.3±2.2 | 27.6±2.1 |
| Trails B scaled | 5.8±2.8 | 6.1±2.7 | 6.2±2.9 | 6.2±2.6 |
| RAVLT trial I MOANS SS | 9.3±2.8 | 10.2±2.6 | 9.9±2.6 | 10.0±3.1 |
| RAVLT LOT MOANS SS | 9.9±2.8 | 9.7±2.6 | 9.8±2.6 | 10.7±3.4 |
| RAVLT trial B MOANS SS | 10.3±2.5 | 11.2±3.0 | 11.1±2.0 | 10.5±2.9 |
| RAVLT trial VI MOANS SS | 9.2±3.2 | 9.4±3.1 | 9.2±3.2 | 10.1±3.2 |
| RAVLT 30 delay MOANS SS | 9.9±3.1 | 10.2±2.8 | 10.0±2.5 | 10.4±2.8 |
| RAVLT recog MOANS SS | 10.0±2.8 | 9.9±2.6 | 10.9±2.3 | 10.5±2.3 |
| RAVLT STPR MOANS SS | 9.0±3.2 | 9.6±2.8 | 9.3±3.6 | 9.8±3.1 |
| RAVLT LTPR MOANS SS | 9.9±3.0 | 10.5±2.7 | 10.2±2.3 | 10.1±2.8 |
| LES Mayo | 91.9±15.4 | 94.4±15.5 | 93.8±15.9 | 97.4±16.1 |
| DRS Mayo | 94.5±16.8 | 96.5±16.6 | 95.3±16.0 | 99.4±16.3 |
| PRS Mayo | 96.3±17.8 | 99.5±15.7 | 97.8±17.0 | 98.5±16.6 |
Table 3. Results of Tests of the Main Effect of Occasion
| Outcome | Random Regression Model P Values: Change vs. Occasion | |
|---|---|---|
| No Covariates | With Covariates⁎ | |
| DRS-2 concept formation (AMSS) | <.001 | <.001 |
| DRS-2 memory (AMSS) | .002 | .029 |
| DRS-2 total (AMSS) | <.001 | .001 |
| DRS-2 AEMSS | <.001 | <.001 |
| RAVLT recognition (MOANS) | .079 | .094 |
| NAART errors | .003 | .003 |
| BDI-II (raw) | .043 | .097 |
⁎Covariates included measures of MRI diffusion, symptom status, and carotid artery stenosis prior to stent placement exceeded 90%, attention scores on the DRS-2 exceeded 12, NAART scores exceeded 108, and age exceeded 80 years. |
The number and percentage of patients whose condition improved, stabilized, or declined from baseline by 3, 6, and 12 months after CAS placement on the DRS-2 total score are shown in Table 4. At all time points, the vast majority of patients showed an improvement or stabilization relative to baseline. When the sample was divided into groups according to baseline DRS-2 total scores (ie, < 120, 120–130, and > 130), each of the three groups showed an improvement during the 1-year follow-up period, although only the middle group's improvement was significant (Figure).
Table 4. DRS-2 Total Score Changes versus Baseline
| Outcome⁎ | 3 Months (n = 51) | 6 Months (n = 48) | 12 Months (n = 51) |
|---|---|---|---|
| Improved | 8(16) | 10(21) | 11(22) |
| Stabilized | 42(82) | 34(71) | 40(78) |
| Declined | 1(2) | 4(8) | 0 |
| Total | 51(100) | 48(100) | 51(100) |
⁎“Improved” indicates a change in total score of more than +3, “stabilized” indicates a change between +3 and −3, and “declined” indicates a change of more than −3. The total score is standardized and has an SD of 3, hence “improved” is an upward change of 1 SD. |
Figure.
DRS-2 total score means plotted against the occasion of measurement by baseline cognitive score group. AMSS = age-corrected MOANS scaled score.
When patients were classified by age into two groups (cutoff of 80 years) and the age group by occasion interaction term was examined, change over time in performance on the DRS-2 construction, RAVLT trial VI, 30-second delay, and recognition MOANS scores, as well as the DRS (Mayo) and Trials B (scaled) scores, were influenced by age before and after adjustment with covariates (Table 5).
Table 5. Probability Levels for Cutoff at Age 80 Years by Occasion Interaction Term
| Outcome | Random Regression Model: P Values for Cutoff Age 80 years (Occasion × Age) | |
|---|---|---|
| No Covariates | With Covariates | |
| DRS-2 construction (AMSS) | .044 | .046 |
| RAVLT trial VI (MOANS) | .019 | .021 |
| RAVLT 30 delay (MOANS) | .020 | .019 |
| RAVLT recognition (MOANS) | .027 | .042 |
| DRS (Mayo) | .008 | .008 |
| Trails B (scaled) | .049 | .044 |
DWI data were available on all but two patients who were excluded from MR imaging by protocol as a result of the presence of pacemakers. There were 13 patients who had diffusion MR imaging changes that varied from one small (2–3 mm) diffusion abnormality to several small diffusion abnormalities. One patient had a small nonhemorrhagic stroke. No significant relationship was detected between MR diffusion status and change in cognition scores at any time point after correction by covariates. The same was true for baseline symptom status: after correction by covariates, the baseline symptom status was not related to the change in cognition scores.
The following outcome variables were not found to be significantly influenced by time of assessment, age, MR diffusion status, or whether the patient was symptomatic: DRS-2 attention scale, RAVLT trial I, RAVLT LOT, RAVLT LTPR, LES, PRS, 3MS.
Discussion
The most striking observation from the present study is that revascularization with a carotid stent and neuroprotection, at a minimum, left cognitive function unchanged, and in many instances improved it. The results are in keeping with previous reports of cognitive improvement after CAS placement (23, 24, 25, 26, 27) and offer the longest follow-up and most comprehensive neurocognitive evaluation yet reported to our knowledge. It is noteworthy that two of these previous reports monitored cerebral perfusion by intracranial angiography (23, 27) and found that improved neurocognitive function was associated with increased cerebral perfusion after stent implantation. Although we did not monitor cerebral perfusion in the current pilot study, its measurement would be a logical addition to a follow-up study.
A secondary hypothesis was that decreases in neurocognitive function would be associated with macroscopic incidents evident on DWI. However, no significant change or decrease in cognitive function in patients with or without DWI abnormalities on MR imaging was observed. A recent study (28) reported decreased cognitive function before and after the procedure in 23 patients who received a CAS compared with a control group. The authors speculated that cognitive dysfunction 1 day after stent placement represented true cerebral injury (28). Although we did not measure cognition immediately after stent placement, DWI was performed before and within 24 hours after CAS placement. None of the DWI abnormalities were associated with significant change or decrease in cognitive function at any of the time points measured (3, 6, and 12 months after CAS placement). Therefore, in our small sample, neurocognitive changes could not be attributed to macroscopic incidents evident on DWI.
The findings that (i) pretreatment symptom status did not predict the post–CAS placement change in cognition scores and (ii) asymptomatic patients showed an improvement in cognitive performance after CAS placement suggest that asymptomatic patients are not truly asymptomatic, but experience neurocognitive compromise, possibly as a result of carotid stenosis or decrease in cerebral perfusion. The “asymptomatic” patient who was previously believed to have limited cognitive compromise associated with carotid stenosis may, in fact, be experiencing adverse cognitive consequence. A previously published population-based case-controlled study (4) reported that reduced cognitive performance was associated with carotid stenosis in asymptomatic patients. Interestingly, cognitive impairment was not associated with MR imaging–detectable lesions in this study. In the past, decreased stroke risk from treatment of carotid stenosis has been used as the only medical indication to treat these patients (29, 30). Now it is possible to entertain the notion of treating a significantly narrowed carotid artery to improve neurocognitive brain function regardless of whether the patient has had previous symptoms. Prophylactic CAS placement in asymptomatic patients is not supported by data in the current study; however, the findings are hypothesis-generating and bear further investigation in a controlled study of an expanded population.
The data also suggest that the younger patient group (ie, those aged < 80 years) appears to possess greater cognitive reserve that the brain can access when flow is normalized, whereas the window of opportunity to access the reserve appears to diminish with age, as indicated by the finding that cognition in older patients improved less after CAS placement. This is an important concept in view of the trend toward a greater population of older adults, many of whom continue to work or desire active lifestyles and who may be limited by cognitive impairment. The association of age and post–CAS placement cognition should be confirmed in a larger, controlled trial.
The DRS-2 is a composite index of cognitive function that provides information on five of seven cognitive domains: attention/concentration, verbal/visual memory, initiation/perseveration, construction, and conceptualization; it reflects the stage of vascular dementia. When the patients were divided into groups according to their baseline DRS-2 scores, only the group that scored in the middle range showed significant improvement during the 1-year follow-up. Although the small sample size in each group precludes definite interpretation, it does appear that patients in the middle group—those with mild vascular dementia—tended to derive the most benefit from the restoration of perfusion. The group scoring in the high range had little room to improve. In the group with the lowest baseline scores, the decrease in cognitive function may have progressed to the point that restoring circulation could not reverse it.
The findings of the present single-center pilot study indicate the need for further research with larger populations and/or comparison with control groups. We have attempted to identify variables predictive of cognitive improvement in the hopes of determining which patients would most likely derive cognitive benefit from stent placement. The decision to treat is dependent on many factors, but maintaining optimal cognitive function in a population with increasing physical and mental demands should be given reasonable priority in the decision-making process.
Acknowledgments
We thank Lynn Dahlstrom for assistance coordinating the clinical trial and Sean Raabe for help with data tabulation. We thank Jane Bailly for contributions to manuscript development.
References
- Heart disease and stroke statistics—2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 2009;119:480–486
- . Prevalence of disabilities and associated health conditions among adults—United States, 1999. MMWR Morb Mortal Wkly Rep. 2001;50:120–125
- Cognitive impairment and decline are associated with carotid artery disease in patients without clinically evident cerebrovascular disease. Ann Intern Med. 2004;140:237–247
- . Reduced neuropsychological test performance in asymptomatic carotid stenosis: the Tromso Study. Neurology. 2004;62:695–701
- . Chronic ischemia and neurocognition. Neuroimaging Clin N Am. 2007;17:313–324
- Neuropsychological dysfunction in the absence of structural evidence for cerebral ischemia after uncomplicated carotid endarterectomy. Neurosurgery. 2006;58:474–480
- . Cerebral protection devices for use during carotid artery angioplasty with stenting: a health technology assessment. Int J Technol Assess Health Care. 2006;22:119–129
- . Impact of carotid endarterectomy upon cognitive functioning: a systematic review of the literature. Cerebrovasc Dis. 1999;9:74–81
- . Long-term results of 442 consecutive, standardized carotid endarterectomy procedures in standard-risk and high-risk patients. J Vasc Surg. 2007;46:876–882
- . Cognitive outcomes after carotid revascularization: the role of cerebral emboli and hypoperfusion. Neurosurgery. 2008;62:385–395
- Carotid artery stenting is associated with increased complications in octogenarians: 30-day stroke and death rates in the CREST lead-in phase. J Vasc Surg. 2004;40:1106–1111
- . Neuropsychological assessment. 3rd ed.. New York: Oxford University Press; 1995;
- . Dementia Rating Scale (DRS): professional manual. Odessa, FL: Psychological Assessment Resources; 1988;
- . Dementia Rating Scale-2 (DRS-2). Lutz, FL: Psychological Assessment Resources; 2001;
- Mayo's Older Americans Normative Studies: category fluency norms. J Clin Exp Neuropsychol. 1998;20:194–200
- . Rey Auditory and Verbal Learning Test: a handbook. Los Angeles: Western Psychological Services; 1996;
- . Comprehensive norms for an expanded Halstead-Reitan battery: demographic corrections, research findings, and clinical applications. Odessa, FL: Psychological Assessment Resources; 1991;
- . North American Adult Reading Test: age norms, reliability, and validity. J Clin Exp Neuropsychol. 2002;24:1123–1137
- . Percutaneous transluminal angioplasty and stenting for carotid artery stenosis. Cochrane Database Syst Rev. 2000;CD000515
- . Comparison of microembolism detected by transcranial Doppler and neuropsychological sequelae of carotid surgery and percutaneous transluminal angioplasty. Stroke. 2000;31:1329–1334
- . An inventory for measuring depression. Arch Gen Psychiatry. 1961;4:561–571
- . Low mini-mental status predicts mortality in asymptomatic carotid arterial stenosis. Asymptomatic Carotid Atherosclerosis Study investigators Neurology. 2000;55:30–34
- Effects of carotid or vertebrobasilar stent placement on cerebral perfusion and cognition. AJNR Am J Neuroradiol. 2005;26:1772–1780
- Cognitive changes after carotid artery stenting. Neuroradiology. 2006;48:319–323
- . Cognitive performance after carotid angioplasty and stenting with brain protection devices. Neurol Res. 2007;29:251–255
- Effect of carotid artery stenting on cognitive function in patients with carotid artery stenosis: preliminary results. AJNR Am J Neuroradiol. 2008;29:265–268
- Improvement of neurocognitive function after protected carotid artery stenting. Cathet Cardiovasc Interv. 2008;71:114–119
- Incidence of moderate to severe cognitive dysfunction in patients treated with carotid artery stenting. Neurosurgery. 2009;65:325–329
- . Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med. 1991;325:445–453
- . Endarterectomy for asymptomatic carotid artery stenosis. JAMA. 1995;273:1421–1428
None of the authors have identified a conflict of interest.
From the SIR 2006 Annual Meeting.
PII: S1051-0443(10)00318-0
doi:10.1016/j.jvir.2010.03.011
© 2010 SIR. Published by Elsevier Inc. All rights reserved.
Volume 21, Issue 7 , Pages 983-988, July 2010
