Published online before print August 21, 2008, doi: 10.1161/STROKEAHA.108.518357
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(Stroke. 2008;39:3116.)
© 2008 American Heart Association, Inc.
Comments, Opinions, and Reviews |
The Role of Carotid Artery Stenting and Carotid Endarterectomy in Cognitive Performance
A Systematic Review
From the Division of Vascular and Endovascular Surgery (P.D.R., M.L., P.C.) and the Stroke Unit (V.C., M.P.), University of Perugia, Ospedale S. Maria della Misericordia, Perugia, Italy; and the Department of Neurology (L.D.), Stroke Unit, University of Lille, Lille, France.
Correspondence to Piergiorgio Cao, MD, FRCS, University of Perugia, Vascular and Endovascular Surgery, Ospedale S. Maria della Misericordia, Loc. S. Andrea delle Fratte, 06156 Perugia, Italy. E-mail pcao{at}unipg.it
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Abstract |
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Background and Purpose— Change in cognition is being increasingly recognized as an important outcome measure; however, the role of carotid revascularization on this issue remains to be determined. It is still under debate whether carotid artery stenting and carotid endarterectomy have the same influence on neuropsychological functions.
Summary of Review— This article systematically reviews recent literature in an attempt to clarify this issue. A total of 32 papers reporting on neurocognition after carotid endarterectomy (n=25), carotid artery stenting (n=4), or carotid artery stenting versus carotid endarterectomy (n=3) were identified. The studies were different for many methodological factors, eg, sample size, type of patients and control group, statistical measure, type of test, timing of assessment, and so on. There was a lack of consensus in defining the improvement or impairment after either carotid artery stenting or carotid endarterectomy. Furthermore, there were nonuneqivocal results regarding the same domain of assessment (memory, visuomotor, attention). Based on available evidence, it is probable that carotid endarterectomy as well as carotid artery stenting do not change neuropsychological function "per se."
Conclusions— Assessment of cognition after carotid revascularization is probably influenced by many confounding factors such as learning effect, type of test, type of patients, and control group, which are often minimized in their importance. The role of carotid revascularization is to prevent stroke in patients with severe carotid stenosis as highlighted by previous large randomized trials. Although an effect of carotid revascularization on cognition could be missed as a consequence of underpowered studies included in this review, at this time, no prediction can be done regarding its repercussions on higher intellectual functions. Larger studies appropriately designed and powered to assess cognition after carotid revascularization might change this view.
Key Words: angioplasty and stenting • carotid endarterectomy • carotid stenosis • cognition • stenting • systematic review
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Introduction |
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Change in cognition is one of the most threatening diseases of recent years. With the progressive aging of the population, the burden of dementia disorders has become even more challenging. Cerebrovascular disease plays a main role in the development of dementia as reported by the stroke–dementia association.1,2 Carotid endarterectomy (CEA) in patients with severe carotid stenosis reduces stroke risk.3,4 However, the influence of CEA, if any, on silent cerebral ischemia and cognition is less defined. A possible link between improved cognitive function and better cerebral perfusion has been hypothesized, whereas subclinical microembolic cerebral patterns occurring during revascularization may worsen neuropsychological function.5 This effect on cognition has further challenged the role of carotid artery stenting (CAS) in carotid stenosis. In addition to the questionable safety of CAS in preventing stroke, higher frequency of microembolism in CAS compared with CEA has been observed by transcranial Doppler (TCD) and diffusion-weighted MR brain imaging.6
Previous reviews on cognition after carotid revascularization, mainly reporting on studies published before 1990, have provided uncertain results regarding the potential benefit of CEA.7–10 Although the validity of cognitive tests persists over time, patient characteristics, brain pharmacological support, and surgical skills have improved over the past 2 decades. Furthermore, very little information has been obtained on these functions after CAS. To investigate the effect of cerebral revascularization on cognition, we performed a systematic review of recent articles on neuropsychological testing after CAS and/or CEA.
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Methods |
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A search strategy was designed to identify all relevant studies on cognitive testing in carotid revascularization. This search was restricted to papers published between January 1990 and May 2007. Studies were initially identified from the Medline/PubMed database, EMBASE, and the Cochrane Database using the search terms "cognitive function," "carotid endarterectomy," "carotid angioplasty," "carotid stenting," "carotid revascularization," "neuropsychological outcome," and "cognitive tests." Additional papers were identified from reference lists of retrieved articles, abstract lists of recent scientific meetings, and Internet-based sources (www.tctmd.com, www.cxvascular.com) of information.
Studies were included if they reported on cognitive tests comparing pre- and postoperative performances in CAS and/or CEA with numbers of examined population and results of cognitive evaluation and enrolled at least 10 cases.
Studies were excluded when reporting: (1) quality of life without neuropsychological assessment or cognitive assessment limited to the anesthesia waning phase; (2) cognitive function in nonsurgical patients, patients with intracranial stenosis or without postoperative assessment; and (3) on case reports and review articles without personal data.
Papers from the same authors were not excluded when reporting additional information as different tests, measurements, and populations.
Two researchers (P.D.R. and V.C.) separately screened the reference list to identify relevant reports. A data extraction form was specifically developed to record study population, control group, analysis, cognitive tests (type and domain), assessment timing, and outcomes. Data were checked for quality independently by the 2 researchers.
Because a battery of cognitive tests specifically addressing the issues related to carotid stenosis and revascularization has not been yet devised, we attempted to simplify the results by: (1) grouping studies in 3 categories according to whether they were reporting on CEA alone, CAS alone, or CAS and CEA together; and (2) assembling study results according to the 3 most commonly investigated cognitive domains: (a) memory, (b) executive function, and (c) attention and language. Although some tests may examine combined categories, most of them were designed to examine individual domains. We combined tests into these 3 major domains to make classification easier and for better access for physicians, because a direct comparison of studies is problematic in view of the disparate measurements of neuropsychological functions.
Global assessment, depression, and dementia scores were not specifically analyzed.
Due to the heterogeneity in definition, method, timing of assessment, and type of tests and to avoid misleading results from differences in measurements, data from this systematic review could not be combined in a formal meta-analysis. This was in accordance with the QUality Of Reporting Of Meta-analyses (QUOROM) recommendations (www.consort-statement.org/QUOROM.pdf).
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Results |
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Search Results
Forty-five potentially relevant articles were identified, 32 of which satisfied the inclusion criteria. Studies were excluded when dealing with pharmacology recovery after anesthesia (n=2),11,12 lacking postoperative assessment (n=1),13 case reports (n=2),14,15 review articles (n=4),7–10 or ongoing trials without available results (n=3). One study was considered a duplicate16 of another included study17 (Figure).
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The 32 included studies, published between 1990 and 2007, are listed in Tables 1 and 2
.5,17–47 Twenty-five reported on cognitive outcome after CEA,5,17–26,28–42 4 after CAS,43–46 and 3 after CEA versus CAS.18,27,47 Overall, 16 used one or more control groups varying from healthy subjects to patients affected by different diseases.18–21,25,27–29,30,33,34,38,41,42,44,46,47
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Ten focused exclusively on symptomatic5,17,21,28,33,35,43,45,27,47 and one on asymptomatic patients.19 Time of cognitive assessment varied from 24 hours to 8 years after revascularization and 4 reported at 1 year or later (3 and 8 years). In 13 of 31, neurological assessment was repeated more than once.
A range of tests (from 3 to 18) investigating several domains was used in each study. In addition to cognition, 3 studies also reported on quality of life25,36,42 and 17 on depression, anxiety, and dementia.
The methodological quality of the included studies was rated as "fair" in all except 3, all published before 2000 and graded as "poor"5,18,37 on a formal assessment checklist (one published only as an abstract18). All studies were published in peer-reviewed journals. Authors used specific methodology (repeated calculations, statistical correction for practice, control group, inclusion criteria, threshold for significance) to try to overcome chance effects and straighten the reliability of results. However, a sample size was not a priori calculated to power the study in any.
The definition of improvement or impairment varied significantly among the included studies and different statistical measurements were used to quantify score changes; changes of 1 or 2 SD or a probability value <0.05 using variance tests could be accepted for significance.
Neuropsychological Outcome After Carotid Endarterectomy
The main characteristics of the 25 reports on CEA are shown in Table 1
.5,17–26,28–42 The study population varied from 22 to 189. To compare cognitive outcome, 12 studies used single or multiple control groups varying from healthy people (n=7),19,25,29,33,34,41,42 to patients with vascular risk factors (n=1),19 to those with peripheral disease (n=2),20,25 those undergoing orthopedic surgery (n=3),21,30,38 or those undergoing urologic surgery (n=1).28 One study analyzed cognitive outcome exclusively in asymptomatic19 and 5 in symptomatic carotid stenosis.5,21,28,33,35 Comparing post-CEA assessment with preoperative condition with a control group, 6 reported no substantial changes after CEA,20,23,30,33,40,42 5 highlighted impairment,5,19,24,31,38 and 4 improvement,21,22,35,41 although not all psychological tests were consistently changed. In the remaining, percentages of improvement varied among different domains. Improvement was reported to be higher at later evaluations.21,28
Neuropsychological Outcome After Carotid Artery Stenting
The main characteristics of the 4 studies reporting cognitive tests after CAS are shown in Table 2.43–46 Populations ranged from 10 to 100. Two were controlled studies.44,46 In the Moftakhar paper, along with CAS, intracranial carotid and vertebral stenosis procedures were also included and reported separately.45 In all 4 studies, a stent was applied to perform CAS; however, only the 2 most recent43,46 used cerebral protection (CPD). One,44 which did not use CPD, showed no significant changes in cognition, whereas the other 3 showed improvement in most of the tests regardless of the use of CPD. A transient impairment in the Boston Naming Test reversing at 2 weeks was found in another study.46 Improvement was detected particularly in memory tests43,46 and in older patients.43
Neuropsychological Outcome After Carotid Endarterectomy and Carotid Artery Stenting
The 3 studies directly comparing CAS versus CEA were all performed within 2 randomized, controlled trials, either the CAVATAS18,27 or the SPACE.47 However, because only a small subgroup of the overall randomized population in both trials was analyzed for cognitive assessment, the sample to assess neurocognition could be unbalanced(Table 2). In the first 2 studies,18,27 analyzing a subgroup of patients within CAVATAS, all procedures except one were performed by angioplasty alone, whereas in the SPACE subgroup,47 a stent was systematically used. No use of CPD was reported. All these studies were unable to find any significant difference in cognition between the 2 populations after revascularization,18,27,47 although patients undergoing CAS performed worse on a single visuomotor test in the study by Crawley et al.27
Although microembolism was higher during CAS, no association between TCD-detected microembolism and cognitive impairment was reported.27 Similarly, no significant changes in the S100β protein values were noted in patients undergoing CAS versus those undergoing CEA in the subgroup of the SPACE trial.47
Neuropsychological Outcomes According to Domain
Changes reported within the 3 major domains are shown in Tables 3, 4, and 5.
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Almost all of the studies reported on memory function (Table 3). A variety of tests were used to assess short, immediate, or delayed recall. In half of the CAS studies, there was improvement in verbal memory. The results from CEA were not homogeneous. Five studies19,20,32,38,42 suggested a decline in cognitive performance, whereas 9 found the greatest improvement in tests on memory, either in the early or the later postoperative assessments.22,25,26,28,34–37,41
Tests for the attention domain are reported in Table 4, the Trail Making Test being one of the most commonly used (14 studies).19,20,23,27,30–32,38,40,41,44,46,47 Grunwald used the Number Collection Test as a substitute for the Trail Making Test.43
Trail tests measuring problem-solving, attention, motor control, and set-shifting were used to assess psychomotor speed (Part A), sustained attention (Part B), or to encompass a number of frontal lobe aspects. We analyzed these tests within the attention domain (although they explore other cognitive functions) to compare the results from different studies in the same type of test. Overall, no significant changes were detected in 6 studies using Trail tests.20,27,30,40,44,47 From the 3 CAS studies using these tests, 2 showed improvement,43,46 whereas the remaining had unchanged results.44 In CEA studies, the results were improved in 4 of 10.22,25,32,41 Attention tests tended to improve at the later assessment time19,20,28 (Table 4).
Language is one of the most complex cognitive fields to be investigated. We analyzed the side and dominance of the treated carotid, when available, to assess the possible laterality effect of neuropsychological dysfunction on language (Table 4). Language tests did not change significantly. Similarly, in analyzing the laterality effect, only 4 of the 7 available studies examining this effect17,21,26,30,34,37,39 found impairment related to the side.17,26,34,37
The largest degree of overlap with other domains occurred in the Executive Function, in which tests investigating visuomotor and visual–constructive ability were included. The most commonly used were Rey Osterrieth, Complex Figure, and Grooved Pegboard, the former mainly used for the nondominant hemisphere, whereas the latter included varieties for the dominant and nondominant hemisphere assessment. Other details and tests are reported in Table 5.
Only one of the 4 CAS studies analyzed this domain and reported unchanged results.46 Another study comparing CAS versus CEA found that the Grooved Pegboard was the only impaired test in the CAS population after the procedure.27
Other Findings
Many studies have incorporated brain imaging into the assessment of neuropsychological function to establish possible correlations with cerebrovascular flow, cerebral reserve, and microembolism.
The effect of microembolism by diffusion-weighted MRI31,43 tended to exclude any correlation, whereas TCD studies either suggested5,28,36 or failed to find any possible impairment.27
A correlation between flow modification by single photon emission CT and cognitive improvement after revascularization has been shown, especially in patients with reduced cerebral reserve.29,34,39
There were overall 5 studies analyzing CAS without use of CPD.21,27,47,44,45 In all except one (which showed improved results),45 no changes in cognition could be found after CAS. On the other side, of the 2 studies reporting on CAS with CPD,43,46 both showed improvements.
The confounding effect of other variables (education, gender, age, symptoms, redo, and so on) on cognition has been reported; older patients appear to improve after CAS43 and worsen after CEA.35,38,40
Two other studies reported improvement in patients with clinical mild cerebral impairment.22,28
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Discussion |
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This review shows that CAS as well as CEA does not clearly affect neurocognition. Cognitive impairment and improvement are both detectable after CAS or CEA. The conflicting results are attributable to differences in several methodological (nonpowered study, type of test, statistic measure, follow-up schedule, presence of a control group) and patient-related variables (older, diabetic, symptomatic patients).
Conversely, previous review articles on cognition after CEA published before 2000 reported an improvement in neuropsychological outcome.7–9 Lunn et al found improvement in cognitive function after CEA in 16 of the 28 studies analyzed.9 This was even more evident in the studies published before 1984.9
In the present review, only 4 of the 25 CEA studies published after 1990 showed clear improvement in cognitive function after surgery; in the remaining, no change, impairment, or contradictory results were detected in the different tests. However, we cannot definitely exclude an effect of carotid revascularization on cognition because results were derived from many small studies probably underpowered to demonstrate a true difference in outcome. Type II errors could have influenced these negative results. Although half of the included studies analyzed more than 50 cases, an a priori calculation of the study power was not given in any, possibly providing underpowered results.
Lessons learned from previous reviews and publications on cognition after carotid revascularization might have improved the quality of the most recent experience on this topic. Indeed, a number of methodological biases appropriately raised by previous authors analyzing cognitive studies after CEA7–9 might be, at least in part, encompassed in these more recent experiences published after 1990, which are reported here.
The learning effect in patients re-evaluated at short interval schedules was probably a major and often disregarded flaw affecting a number of earlier studies favorable for an improvement in neurocognition after carotid revascularization. However, the majority of investigators in the present review have tried to control the fact that subjects improve their cognitive score with practice by adding a control group,18,20–29,30,33,34,38,41,42,44,46,47 by using reassessment after a minimum of 3 months17–27,31,35,36,39–42,44,45 or by correcting for practical effect in statistical evaluation.44 Nevertheless, important limitations still remain even in the recent experiences, as evidenced previously. As a further step, the standardization of tests designed for vascular cognitive assessment could lead to a more accurate and reliable data collection on this topic.10
To our knowledge, this is the first systematic review analyzing cognitive function after CAS. Nevertheless, only 7 studies analyzed this procedure, 3 of which in comparison with CEA.21,27,43–47 Surprisingly, approximately half of the CAS studies reported improvement in cognitive function, especially in memory tests,43,46 contradicting previous reports suggesting a potential cognitive damage from CAS due to microembolism.48–51 However, due to the small numbers and lack of controls in 2 of the CAS studies, conclusions should be drawn cautiously.
It is generally accepted that CAS carries a higher cerebral embolic risk. Subclinical microembolic events, revealed by imaging, might negatively affect cognitive performance. Indeed, cognitive decline has been associated with silent microembolic cerebral injury in other clinical settings such as cardiac catheterization and surgical procedures.48,49 In the present review, no clear evidence of higher cognitive impairment was detected after CAS. Even if no direct comparison between CAS and CEA was available in large populations, in the 3 studies comparing CAS with CEA,21,27,47 no differences in cognitive performance were found despite a higher rate of microembolism in the CAS group.27 This apparent discrepancy may be explained by the disparate composition of microembolisms; gaseous embolisms are less hazardous than particulate ones and lead to less serious clinical consequences.50,51
Diffusion-weighted MRI31,43 or some TCD27 studies tended to exclude any correlation, whereas other TCD experiences suggested a possible impairment.5,28,36
To this regard, the 2 studies in which CAS was performed with CPD43,46 both showed improvements in cognition after CAS. Of the other 5 studies analyzing CAS without CPD,21,27,47,44 all but one45 showed unchanged cognition. However, differences in sample size, time of assessment, and type of test among these small studies could have affected the differences.
In addition to embolism,5,28,36 another 2 mechanisms for cognitive impairment during carotid revascularization have been suggested. Intraprocedural changes in cerebral blood flow due to clamping or ballooning might correlate with neuropsychological impairment.14 Other studies have shown benefit from improved perfusion after carotid revascularization, particularly in patients with reduced cerebral reserve.22,29,34,39 However, cognitive deterioration might also occur in the context of cerebral hyperperfusion.14 From this literature review, it appears that there are more data supporting an effect from flow variation than from microembolism on cognitive performance after carotid revascularization. Three studies analyzing flow modification by single photon emission CT found a correlation between flow modification and cognitive improvement in patients with reduced cerebral reserve.29,34,39 The effect of microembolism was extensively analyzed but contradictorily defined.
Many investigators are working to discover what exactly occurs in the brain "behind the scenes" during and after carotid revascularization. Based on available evidence, it is likely that CEA as well as CAS does not affect neuropsychological function per se. Cognitive function is influenced by more than one confounding factors (learning effect, type of test, type of patients and control subjects) that are frequently minimized or disregarded.
This review presents limitations. Studies might not be adequately powered to assess a true effect of revascularization of cognition and conclusions should be interpreted with caution due to a possible Type II error. A direct comparison among the studies was problematic in view of the diversity in measuring neuropsychological function. We analyzed tests assessing specific cognitive domains (ie, attention and language, executive function including visuomotor skill, and memory). This categorization, however, is not used universally because no standardization and overlap for domains exists. Global assessment, depression, and dementia scores were not evaluated.
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Conclusions |
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Whether and to what extent the neurocognitive functions of patients is affected by CAS or CEA remains unclear.
Patients with carotid stenosis and their relatives are strongly interested in knowing whether carotid revascularization may affect neuropsychological functions. This is particularly true for asymptomatic patients for whom the role of revascularization is still under debate, and the change in cognitive functions may play a role in assessing the risk/benefit ratio of the treatment choice. As revealed in this review, there are no data indicating a cognitive change after CAS or CEA in patients who do not experience stroke complications, even if new silent embolic lesions, especially after CAS, were detected on cerebral imaging. However, larger studies appropriately designed and properly powered to assess cognition after carotid revascularization might also change this opinion.
Carotid revascularization is the best proven measure for stroke prevention in patients with large-vessel disease. Physicians, neurologists, and vascular surgeons should thoroughly inform their patients on the expected outcomes after carotid revascularization on the basis of data from randomized trials without any false expectations in cognition.
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Acknowledgments |
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We thank Francesca Zannetti and Eileen Mahoney for editing assistance.
Disclosures
None.
Received February 22, 2008; accepted March 14, 2008.
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References |
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1. Hachinski V, Munoz DG. Cerebrovascular pathology in Alzheimer’s disease: cause, effect or epiphenomenon? Ann NY Acad Sci. 1997; 826: 1–6.[CrossRef][Medline] [Order article via Infotrieve]
2. Rockwood K, Wentzel C, Hachinski V, Hogan DB, MacKnight C, McDowell I. Prevalence and outcomes of vascular cognitive impairment. Vascular Cognitive Impairment Investigators of the Canadian Study of Health and Aging. Neurology. 2000; 54: 447–451.
3. North American Symptomatic Carotid Endarterectomy Trial Collaboration. Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med. 1991; 325: 445–453.[Abstract]
4. MRC Asymptomatic Carotid Surgery Trial (ACST) Collaborative Group. Prevention of disabling and fatal strokes by successful carotid endarterectomy in patients without recent neurological symptoms: randomised controlled trial. Lancet. 2004; 363: 1491–1502.[CrossRef][Medline] [Order article via Infotrieve]
5. Gaunt ME, Martin PJ, Smith JL, Rimmer T, Cherryman G, Ratliff DA, Bell PRF, Naylor R. Clinical relevance of intraoperative embolization detected by transcranial Doppler ultrasonography during carotid endarterectomy: a prospective study of 100 patients. Br J Surg. 1994; 81: 1435–1439.[Medline] [Order article via Infotrieve]
6. Lacroix V, Hammer F, Astarci P, Duprez T, Grandin C, Cosnard G, Peeters A, Verhelst R. Ischemic cerebral lesions after carotid surgery and carotid stenting. Eur J Vasc Endovasc Surg. 2007; 33: 430–435.[CrossRef][Medline] [Order article via Infotrieve]
7. Irvine CD, Gardner FV, Davies AH, Lamont PM. Cognitive testing in patients undergoing carotid endarterectomy. Eur J Vasc Endovasc Surg. 1998; 15: 195–204.[CrossRef][Medline] [Order article via Infotrieve]
8. Rao R. The role of carotid stenosis in vascular cognitive impairment. Eur Neurol. 2001; 46: 63–69.[CrossRef][Medline] [Order article via Infotrieve]
9. Lunn S, Crawley F, Harrison MJG, Brown MM, Newman SP. Impact of carotid endarterectomy upon cognitive functioning. A systematic review of the literature. Cerebrovasc Dis. 1999; 9: 74–81.[Medline] [Order article via Infotrieve]
10. Lal BK. Cognitive function after carotid artery revascularization. Vasc Endovascular Surg. 2007; 41: 5–13.
11. Kostopanagiotou G, Markantonis SL, Polydorou M, Pandazi A, Kottis G. Recovery and cognitive function after fentanyl or remifentanil administration for carotid endarterectomy. J Clin Anesth. 2005; 17: 16–20.[CrossRef][Medline] [Order article via Infotrieve]
12. Wilhelm W, Schlaich N, Harrer J, Kleinschmidt S, Müller M, Larsen R. Recovery and neurological examination after remifentanil–desflurane or fentanyl–desflurane anaesthesia for carotid artery surgery. Br J Anaesth. 2001; 96: 41–49.
13. Bossema ER, Brand N, Moll FL, Ackerstaff RGA, de Haan EHF, van Doornen LJP. Cognitive functions in carotid artery disease before endarterectomy. J Clin Exp Neuropsychol. 2006; 28: 357–369.[CrossRef][Medline] [Order article via Infotrieve]
14. Ogasawara K, Inoue T, Kobayashi M, Fukuda T, Komoribayashi N, Saitoh H, Yamadate K, Ogawa A. Cognitive impairment associated with intraoperative and postoperative hypoperfusion without neurologic deficits in a patient undergoing carotid endarterectomy. Surg Neurol. 2006; 65: 577–581.[CrossRef][Medline] [Order article via Infotrieve]
15. Lee TM, Ho DS, Chan CC. Preliminary neuropsychological outcomes of angioplasty and stenting of extra cranial cerebral arteries. Percept Mot Skills. 1999; 88: 267–270.[CrossRef][Medline] [Order article via Infotrieve]
16. Bo M, Massaia M, Speme S, Cappa G, Strumia K, Cerrato P, Ponzio F, Molaschi M. Cognitive function after carotid endarterectomy: greater risk of decline in symptomatic patients with left internal carotid artery disease. J Stroke Cerebrovasc Dis. 2005; 14: 221–228.[CrossRef][Medline] [Order article via Infotrieve]
17. Bo M, Massaia M, Speme S, Cappa G, Strumia K, Cerrato P, Ponzio F, Poli L. Risk of cognitive decline in older patients after carotid endarterectomy: an observational study. J Am Geriatr Soc. 2006; 54: 932–936.[CrossRef][Medline] [Order article via Infotrieve]
18. Sivaguru A, Gaines PA, Beard J, Venables GS. Neuropsychological outcome after carotid angioplasty: a randomised control trial [Abstract]. J Neurol Neurosurg Psychiatry. 1999; 66 (suppl): 262.
19. Aharon-Peretz J, Tomer R, Gabrieli I, Aharonov D, Nitecki S, Hoffman A. Cognitive performance following endarterectomy in asymptomatic severe carotid stenosis. Eur J Neurol. 2003; 10: 525–528.[CrossRef][Medline] [Order article via Infotrieve]
20. Aleksic M, Huff W, Hoppmann B, Heckenkamp J, Pukrop R, Brunkwall J. Cognitive function remains unchanged after endarterectomy of unilateral internal carotid artery stenosis under local anaesthesia. Eur J Vasc Endovasc Surg. 2006; 31: 616–621.[CrossRef][Medline] [Order article via Infotrieve]
21. Antonelli Incalzi R, Gemma A, Landi F, Pagano F, Capparella O, Snider F, Manni R, Carbonin P. Neuropsychologic effects of carotid endarterectomy. J Clin Exp Neuropsychol. 1997; 19: 785–794.[Medline] [Order article via Infotrieve]
22. Borroni B, Tiberio G, Bonardelli S, Cottini E, Facheris M, Akkawi N, Pezzini A, Cervi E, Giulini SM, Padovani A. Is mild vascular cognitive impairment reversible? Evidence from a study on the effect of carotid endarterectomy. Neurol Res. 2004; 26: 594–597.[CrossRef][Medline] [Order article via Infotrieve]
23. Bossema ER, Brand N, Moll FL, Ackerstaff RGA, van Doornen LJP. Does carotid endarterectomy improve cognitive functioning? J Vasc Surg. 2005; 41: 775–781.[CrossRef][Medline] [Order article via Infotrieve]
24. Bossema ER, Brand N, Moll FL, Ackerstaff RGA, van Doornen LJP. Perioperative microembolism is not associated with cognitive outcome three months after carotid endarterectomy. Eur J Vasc Endovasc Surg. 2005; 29: 262–268.[CrossRef][Medline] [Order article via Infotrieve]
25. Bossema ER, Brand N, Geenen R, Moll FL, Ackerstaff RGA, van Doornen LJP. Effect of carotid endarterectomy on patient evaluations of cognitive functioning and mental and physical health. Ann Vasc Surg. 2005; 19: 673–677.[CrossRef][Medline] [Order article via Infotrieve]
26. Brand N, Bossema ER, van Ommen M, Moll FL, Ackerstaff RGA. Left or right carotid endarterectomy in patients with atherosclerotic disease: ipsilateral effects on cognition? Brain Cogn. 2004; 54: 117–123.[CrossRef][Medline] [Order article via Infotrieve]
27. Crawley F, Stygall J, Lunn S, Harrison M, Brown MM, Newman S. Comparison of microembolism detected by transcranial Doppler and neuropsychological sequelae of carotid surgery and percutaneous transluminal angioplasty. Stroke. 2000; 31: 1329–1334.
28. Fearn SJ, Hutchinson S, Riding G, Hill-Wilson G, Wesnes K, McCollum CN. Carotid endarterectomy improves cognitive function in patients with exhausted cerebrovascular reserve. Eur J Vasc Endovasc Surg. 2003; 26: 529–536.[CrossRef][Medline] [Order article via Infotrieve]
29. Fukunaga S, Okada Y, Inoue T, Hattori F, Hirata K. Neuropsychological changes in patients with carotid stenosis after carotid endarterectomy. Eur Neurol,. 2006; 55: 145–150.[CrossRef][Medline] [Order article via Infotrieve]
30. Heyer EJ, Sharma R, Rampersad A, Winfree CJ, Mack WJ, Solmon RA, Todd GJ, McCormick PC, McMurtry JG, Quest DO, Stern Y, Lazar RM, Connolly ES. A controlled prospective study of neuropsychological dysfunction following carotid endarterectomy. Arch Neurol. 2002; 59: 217–222.
31. Heyer EJ, Adams DC, Solomon RA, Todd GJ, Quest DO, McMahon DJ, Steneck SD, Choudhri TF, Connolly ES. Neuropsychometric changes in patients after carotid endarterectomy. Stroke. 1998; 29: 1110–1115.
32. Heyer EJ, DeLaPaz R, Halazun HJ, Rampersad A, Zurica J, Sciacca R, Benvenisty AI, Todd GJ, Quest DO, Lavine S, Solomon RA, Connolly ES. Neuropsychological dysfunction in the absence of structural evidence for cerebral ischemia after uncomplicated carotid endarterectomy. Neurosurgery. 2006; 58: 474–480.[Medline] [Order article via Infotrieve]
33. Iddon JL, Sahakian BJ, Kirkpatrick PJ. Uncomplicated carotid endarterectomy is not associated with neuropsychological impairment. Pharmacol Biochem Behav. 1997; 56: 781–787.[CrossRef][Medline] [Order article via Infotrieve]
34. Kishikawa K, Kamouchi M, Okada Y, Inoue T, Ibayashi S, Iida M. Effects of carotid endarterectomy on cerebral blood flow and neuropsychological test performance in patients with high-grade carotid stenosis. J Neurol Sci. 2003; 213: 19–24.[CrossRef][Medline] [Order article via Infotrieve]
35. Lind C, Wimmer A, Magometschnigg H,. Ehrmann L, Havelec L, Reichenauer M, Zeiler K. Einfliisse der Karotisendarterektomie auf verschiedene Hirnleistungsparameter. Langenbecks Arch Chir. 1993; 378: 345–352.[CrossRef][Medline] [Order article via Infotrieve]
36. Lloyd AJ, Hayes PD, London NJM, Bell PRF, Naylor AR. Does carotid endarterectomy lead to a decline in cognitive function or health related quality of life? J Clin Exp Neuropsychol. 2004; 26: 817–825.[CrossRef][Medline] [Order article via Infotrieve]
37. Mononen H, Lepojärvi M, Kallanranta T. Early neuropsychological outcome after carotid endarterectomy. Eur Neurol. 1990; 30: 328–333.[Medline] [Order article via Infotrieve]
38. Mocco J, Wilson DA, Komotar RJ, Zurica J, Mack WJ, Halazun HJ, Hatami R, Sciacca RR, Connolly ES, Heyer EJ. Predictors of neurocognitive decline after carotid endarterectomy. Neurosurgery. 2006; 58: 844–850.[CrossRef][Medline] [Order article via Infotrieve]
39. Ogasawara K, Yamadate K, Kobayashi M, Endo H, Fukuda T, Yoshida K, Terasaki K, Inoue T, Ogawa A. Postoperative cerebral hyperperfusion associated with impaired cognitive function in patients undergoing carotid endarterectomy. J Neurosurg. 2005; 102: 38–44.[Medline] [Order article via Infotrieve]
40. Pearson S, Maddern G, Fitridge R. Cognitive performance in patients after carotid endarterectomy. J Vasc Surg. 2003; 38: 1248–1253.[CrossRef][Medline] [Order article via Infotrieve]
41. Sinforiani E, Curci R, Fancellu R, Facchinetti P, Mille T, Bono G. Neuropsychological changes after carotid endarterectomy. Funct Neurol. 2001; 16: 329–336.[Medline] [Order article via Infotrieve]
42. Sirkka A, Salenius JP, Portin R, Nummenmaa T. Quality of life and cognitive performance after carotid endarterectomy during long-term follow-up. Acta Neurol Scand. 1992; 85: 58–62.[Medline] [Order article via Infotrieve]
43. Grunwald IQ, Supprian T, Politi M, Struffert T, Falkai P, Krick C, Backens M, Reith W. Cognitive changes after carotid artery stenting. Neuroradiology. 2006; 48: 319–323.[CrossRef][Medline] [Order article via Infotrieve]
44. Leherner J, Willfort A, Milekush I, Guttmann G, Minar E, Ahmadi R, Lalouschek W, Deecke L, Lang W. Neuropsychological outcome 6 months after unilateral carotid stenting. J Clin Exp Neuropsychol. 2005; 27: 859–866.[CrossRef][Medline] [Order article via Infotrieve]
45. Moftakhar R, Turk AS, Niemann DB, Hussain S, Rajpal S, Cook T, Geraghty M, Aagaard-Kienitz B, Turski PA, Newman GC. Effects of carotid or vertebrobasilar stent placement on cerebral perfusion and cognition. AJNR Am J Neuroradiol. 2005; 26: 1772–1780.
46. Xu G, Liu X, Meyer JS, Yin Q, Zhang R. Cognitive performance after carotid angioplasty and stenting with brain protection devices. Neurol Res. 2007; 29: 251–255.[CrossRef][Medline] [Order article via Infotrieve]
47. Witt K, Borsch K, Daniels C, Walluscheck K, Alfke K, Jansen O, Czech N, Deuschl G, Stingele R. Neuropsychological consequences of endarterectomy and endovascular angioplasty with stent placement for treatment of symptomatic carotid stenosis. A prospective randomized study. J Neurol. 2007; 254: 1524–1532.[CrossRef][Medline] [Order article via Infotrieve]
48. Braekken SK, Reinvang I, Russell D, Brucher R, Svennevig JL. Association between intraoperative cerebral microembolic signals and postoperative neuropsychological deficit: comparison between patients with cardiac valve replacement and patients with coronary artery bypass grafting. J Neurol Neurosurg Psychiatry. 1998; 65: 573–576.
49. Sylivris S, Levi C, Matalanis G, Rosalion A, Buxton BF, Mitchell A, Fitt G, Harberts DB, Saling MM, Tonkin AM. Pattern and significance of cerebral microemboli during coronary artery bypass grafting. Ann Thorac Surg. 1998; 66: 1674–1678.
50. Rosenkranz M, Fiehler J, Niesen W, Waiblinger C, Eckert B, Wittkugel O, Kucinski T, Röther J, Zeumer H, Weiller C, Sliwk U. The amount of solid cerebral microemboli during carotid stenting does not relate to the frequency of silent ischemic lesions. AJNR Am J Neuroradiol. 2006; 27: 157–161.
51. Vermeer SE, Prins ND, den Heijer T, Hofman A, Koudstaal PJ, Breteler MMB. Silent brain infarcts and the risk of dementia and cognitive decline. N Engl J Med. 2003; 348: 1215–1222.
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