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Incidence and Risk Factors for Diffusion-Weighted Imaging
(+) Lesions After Intracranial Stenting and Its Relationship
With Symptomatic Ischemic Complications
Keun Young Park, MD; Byung Moon Kim, MD; Dong Joon Kim, MD; Dong Ik Kim, MD; Ji Hoe Heo, MD; Hyo Suk Nam, MD; Young Dae Kim, MD; Dongbeom Song, MD Background and Purpose—Little is known about high-signal lesions in magnetic resonance diffusion-weighted imaging
(DWI [+]) after stenting for intracranial atherosclerotic stenosis. This study aimed to evaluate the incidence, distribution, risk factors, and clinical implications of DWI (+) after intracranial stenting.
Methods—A total of 123 patients (male:female=88:35, mean age, 64.1 years) with symptomatic intracranial atherosclerotic
stenosis (mean stenosis, 76.1±7.7%) underwent both stenting and poststenting DWI. The incidence, distribution (embolic-alone versus stenosis-associated perforator/mixed), and risk factors of DWI (+) and its relationship with symptomatic ischemic complications (SIC, including stroke or transient ischemic attack) were retrospectively evaluated.
Results—Forty-three patients (35.0%) had DWI (+). Middle cerebral artery, smaller distal parent artery, and treatment-
related dissection were independent risk factors for DWI (+) (P<0.05). SIC occurred in 4 patients (3.3%), all of whom had DWI (+). Of the patients with DWI (+), neither the number nor the volume of DWI (+) differed significantly between SIC and asymptomatic patients: median number/patient, 3.5 (range, 2–11) versus 2.0 (range, 1–11) and median volume/patient, 329.8 mm3 (range, 76–883.5 mm3) versus 119.5 mm3 (range, 32.5–873.0 mm3). However, SIC occurred more frequently in the stenosis-associated perforator/mixed type (3/11, 27.3%) than in the embolic-alone type (1/32, 3.1%; P<0.05).
Conclusions—The incidence of DWI (+) after intracranial stenting for intracranial atherosclerotic stenosis was 35.0%.
Middle cerebral artery, smaller distal parent artery, and treatment-related dissection were independent risk factors for
DWI (+). SIC occurred more frequently in the stenosis-associated perforator/mixed type than in the embolic-alone
type. (Stroke. 2014;45:3298-3303.)
Key Words: diffusion magnetic resonance imaging ◼ intracranial atherosclerosis ◼ stents ◼ stroke
Diffusion-weighted MRI (MR-DWI) is sensitive to clini- factors of DWI (+) after intracranial stenting and its relation- cally silent infarctions and overt ischemia because it can ship to symptomatic ischemic complications (SIC).
accurately detect small ischemic lesions within 40 minutes, and for ≥5 days after the onset of ischemic stroke.1,2 Therefore, Patients and Methods
MR-DWI positive lesions (DWI [+]) could be used for proce- Patients who underwent both intracranial stenting for symptomatic dure outcome monitoring in cerebral angiography, revascular- ICAS and poststenting MR-DWI between May 2001 and June 2013 ization of cervical internal carotid artery stenosis, coiling for were identified from a prospectively maintained neurointerventional intracranial aneurysm, coronary angiography and intervention, database. Inclusion criteria for intracranial stenting were symptomatic ICAS ≥70%, symptomatic ICAS ≥60% and refractory to antiplatelet and cardiac surgery.3–14 Intracranial atherosclerotic stenosis medication, or asymptomatic with progressive worsening of stenosis (ICAS) is responsible for 9% to 37% of ischemic stroke, with >80% on follow-up angiography despite dual antiplatelet medication. even higher rates seen in Asian populations.15,16 Intracranial Exclusion criteria were suspicion of vasculitis or Moyamoya disease stenting has been suggested as an adjuvant or a rescue treat- and parent artery anatomy that made it too dangerous to navigate to a ment modality for patients who are refractory to medical man- more distal arterial branch or to deliver the stent to the target lesion. For each patient, the need for and feasibility of intracranial stenting agement.17–19 Nonetheless, there has been only one small case were determined after discussion between interventional neuroradiol- series investigating DWI (+) after intracranial stenting.4 In ogists and stroke neurologists. For this study, additional exclusion cri- this study, we evaluated the incidence, distribution, and risk teria were as follows: (1) patients who underwent balloon angioplasty Received May 26, 2014; final revision received August 30, 2014; accepted September 4, 2014.
From the Departments of Neurosurgery (K.Y.P.), Radiology (B.M.K., D.J.K., D.I.K.), and Neurology (J.H.H., H.S.N., Y.D.K., D.S.), Severance Hospital, Yonsei University College of Medicine, Seoul, South Korea.
The online-only Data Supplement is av
Correspondence to Byung Moon Kim, MD, PhD, Department of Radiology, Severance Hospital, Yonsei University College of Medicine, 50–1 Yonsei-ro, Seodaemun-gu, 120–752, Seoul, South K 2014 American Heart Association, Inc.
Stroke is available at http://stroke.ahajournals.org

Park et al DWI (+) Lesion After Intracranial Stenting 3299
alone, (2) patients who underwent emergent stenting as part of intra- at least twice: within 30 days before and within 24 hours after intra- arterial recanalization therapy for acute stroke, and (3) patients who cranial stenting. MR-DWI was also performed if any new neurological did not have pre- or poststenting MR-DWI.
symptom developed. Pre- and poststenting MR-DWI were analyzed by independent neuroradiologists who had not participated in the treatment. DWI (+) was defined as any newly developed high-signal intensity le-sion in the relevant brain region after intracranial stenting. The relevant All patients received dual antiplatelet premedication (aspirin 100 mg brain region was defined as brain parenchyma downstream of the guid- and clopidogrel 75 mg daily) for ≥5 days before the procedure. All ing catheter, as previously reported.9 First, DWI (+) was assessed in each intracranial stenting was performed under local anesthesia. A bolus patient. If present, then respective DWI (+) size, number, and volume of heparin 3000 IU was administered intravenously immediately after were analyzed for each patient. The total volume of DWI (+) was calcu- placement of a 6F shuttle guiding sheath (Cook, Bloomington, IN) lated as the sum of the area of DWI (+) on each slice multiplied by slice or a 6F Envoy guiding catheter (Cordis, Miami Lakes, FL) into the thickness. In addition, the distribution of DWI (+) was stratified into cervical internal carotid artery or vertebral artery. Thereafter, 1000 2 types: embolic-alone and stenosis-associated perforator/mixed type. IU/h was administered. After completion of the procedure, heparin Embolic-alone type was defined as DWI (+) distributed in the cortical was stopped, but not reversed.
and subcortical region distal to the target stenosis (Figure 1). Stenosis- Balloon-expandable coronary stents (Driver, Medtronic, associated perforator/mixed type was defined as ≥1 DWI (+) located Minneapolis, MN; FlexMaster, JOMED, Rangendingen, Germany; in the territory of the perforator which was closely related to the target Vision, Guidant, St. Paul, MN) were used before the introduction of stenosis regardless of the presence of distal embolic lesions (Figure 2).
the Wingspan stent in March 2010. However, the Wingspan stent has Each patient's neurological status was assessed by board-certified been used exclusively since its introduction. Wingspan stenting was neurologists immediately after stenting and daily during admission performed using a previously reported procedure.18 Prestenting balloon for the development of any new or worsening neurological deficits. angioplasty always preceded Wingspan stenting using the Gateway Clinical outcomes were evaluated at discharge, at 1 month, and at balloon. Whether or not to perform prestenting balloon angioplasty 3-month intervals thereafter. Periprocedural SIC was defined as the during balloon-expandable stent (BES) insertion was decided based on occurrence of any type of stroke or transient ischemic attack during operator discretion. When performing prestenting balloon angioplasty admission. All technical and clinical periprocedural complications before BES insertion, the smallest balloon (1.5–2.0 mm) available was were prospectively registered into the neurointerventional and neuro- used for the purpose of allowing the stent to pass through the lesion logical database and were retrospectively evaluated.
easily. Otherwise, there were no remarkable differences between BES and Wingspan stent procedure and postprocedural management.
MRI and Clinical Assessment
Statistical analysis was performed using IBM SPSS statistics version 20.0 (IBM Corp, Armonk, NY). Continuous variables with a normal Except for patients with symptomatic intracranial hemorrhage, MR-DWI (field of view, 23 cm×23 cm; matrix, 128×128; b-factor, 0 and 1000; slice thickness, 3–5 mm with no gap) was obtained in all patients Figure 2. A 68-year-old woman presenting with perforator/mixed
type infarctions. A, Prestenting diffusion-weighted MRI (MR-DWI)
Figure 1. A 58-year-old man presenting with embolic infarctions.
showed acute perforator-type infarction in the left lateral len- A, Prestenting diffusion-weighted MRI (MR-DWI) showed acute
ticulostriate artery territory and 2 small embolic infarctions in the infarctions in the left occipital and temporal lobes. B, Catheter
left temporoparietal lobes (not shown). B, Catheter angiogram
angiograms showed a severe degree of stenosis in the left intra- showed a severe degree of stenosis at the left middle cerebral cranial vertebral artery which supplies the entire posterior circula- artery M1 portion with decreased perfusion in the left middle tion because of chronic occlusion of the right vertebral artery (not cerebral artery territory. C, Poststenting angiogram revealed a
shown). C, Poststenting angiogram showed only a minimal resid-
mild degree of residual stenosis with no angiographic abnor- ual stenosis without any angiographic abnormality. D, Poststent-
mality. D, Poststenting MR-DWI showed a mixed type of new
ing MR-DWI showed acute embolic infarction in the right middle stenosis-associated perforator infarct and embolic lesions in the cerebellar peduncle and cerebellar hemisphere (not shown).
left frontal cortex.
3300 Stroke November 2014
distribution were presented as means±SD. Continuous variables without a normal distribution were presented as medians and rang- MR-DWI has been used to monitor cerebral embolism after es. Categorical variables were presented as percentages. Statistical analysis was performed to characterize the association between various cardiac and neurovascular procedures.3–14 Recently, DWI (+) and possible risk factors. Statistical analysis was also per- DWI (+) has been identified as a possible marker of SIC risk formed to determine the relationship between number of DWI (+) and factors postaneurysm coiling and carotid revascularization.5,7,9 the distribution of DWI (+) and SIC. A χ2 test or Fisher exact test were However, to our knowledge, there is only one small case study performed for categorical variables as appropriate. An independent t test or the Mann–Whitney U test were used for continuous variables of DWI (+) after intracranial angioplasty with or without as appropriate. The univariate cutoff for inclusion in logistic regres- stenting for ICAS.4 In that study, DWI (+) was detected in 8 sion was P<0.20. All tests were 2-tailed. α was set at P<0.05 with a (47.1%) of the 16 patients who underwent angioplasty with 95% confidence interval.
(n=10) or without stenting (n=7). DWI (+) appeared more fre-quently after balloon angioplasty followed by stent placement than after balloon angioplasty alone or primary stent place- Patient and Target ICAS Characteristics
ment. Length of stenosis was also significantly correlated with A total of 134 patients underwent intracranial stenting. One DWI (+). However, that study seemed too small to identify hundred twenty-three patients (88 men and 35 women with risk factors associated with DWI (+).
a mean age of 64.1±9.1 years) were included in this study. In this study, the incidence of DWI (+) was 35.0%, which Eleven patients were excluded: 9 who underwent intracranial was lower than the previous case study. Middle cerebral stenting performed as a part of intra-arterial therapy for acute artery location of the target stenosis, smaller distal parent stroke and 2 patients because poststenting MR-DWI was not artery, and treatment-related dissection were independent obtained as a result of hemorrhagic complications. Of the 2 risk factors for DWI (+) (Table 1). These independent risk patients who had poststenting hemorrhagic complication, one factors may be associated with the difficulty of the stent- had intraparenchymal hemorrhage because of hyperperfusion ing procedure. It is likely more difficult to deliver a stent to syndrome and the other had subarachnoid hemorrhage prob- target stenoses in the middle cerebral artery than in other ably because of microguidewire perforation. One hundred locations (internal carotid artery, vertebral artery, or basilar sixteen (94.3%) of the 123 patients were symptomatic. The artery). This may also be true for smaller distal parent arter- location of target ICAS was the internal carotid artery in 44 ies. Furthermore, because dissection itself can cause overt (35.8%), vertebral artery in 43 (35.0%), middle cerebral artery infarction, it is not surprising that treatment-related dissection in 20 (16.3%), and basilar artery in 16 patients (13.0%). The significantly increased the rate of DWI (+). Greater age is a mean degree and length of target ICAS were 76.1±7.7% and previously documented risk factor for DWI (+) after coiling 9.4±3.4 mm (Table 1).
of intracranial aneurysm or carotid artery stenting.9,20 This suggests that greater baseline atherosclerosis and vascular Morbidity and Mortality of Elective Stenting
tortuosity in older patients may increase microembolisms dur- Except for emergent stenting as a part of intra-arterial ing the stenting procedure.9,21 In this study, greater age was a therapy for acute stroke, a total of 125 patients underwent significant risk factor for DWI (+) in univariate analysis but intracranial stenting. Treatment-related symptomatic compli- was not significant in multivariate analysis, probably because cations occurred in 6 patients, 4 ischemic and 2 hemorrhagic. of low statistical power. The Wingspan stent was also a risk Treatment-related morbidity and mortality were 4.0% (5 of factor in univariate analysis and showed a trend for DWI (+) 125) and 0.8% (1 of 125), respectively.
in the multivariate analysis. In the recent study assessing DWI (+) after carotid artery stenting, more porous open- MR-DWI and SIC
cell stents showed a significantly higher rate of DWI MR-DWI (+) was observed in 43 (35.0%) of 123 patients. The (+) than closed-cell design stents.7 The Wingspan has total number of DWI (+) was 162 (median 3 per patient, range an open-cell design and is composed of thinner struts 1–11 per patient). The median dimension of DWI (+) was 4.0 than the coronary BES. This may increase the rate of mm (range, 1.6–16.4 mm). The median total volume of DWI distal microemboli during or after stenting. Wingspan (+) per patient was 119.5 mm3 (range, 32.5–883.5 mm3). The stent was a significant risk factor for embolic-only type distribution of DWI (+) was embolic-alone in 32 and stenosis- DWI (+) on univariate analysis but did not remain significant associated perforator/mixed type in 11 patients. After adjusting in the logistic regression analysis (Table I in the online-only for age, smoking status, length of target stenosis, prestenting Data Supplement). Also, there was no significant difference angioplasty, and stent type, middle cerebral artery location of in the distribution of DWI (+) between Wingspan and BES the target stenosis, smaller distal parent artery, and treatment- (Table II in the online-only Data Supplement). It might be related dissection were independent risk factors for DWI (+) because of low statistical power.
(Table 1). SIC occurred in 4 (3.3%) of the 123 patients, all of Importantly, the rate of SIC in this study was 3.3%, all of whom showed DWI (+) (Table 2). There was no significant whom showed DWI (+). However, there was no significant risk risk factor for SIC. Of the 43 patients with DWI (+), there was factor for SIC. This was likely because of the low incidence no difference in the number or in the total volume of DWI of SIC in this data set. Acute in-stent thrombosis occurred in (+) between SIC and asymptomatic patients. However, SIC 13.8% of our cases. The reported rates of in-stent thrombosis occurred more frequently in the perforator/mixed type than in after Wingspan stenting in the previous 2 studies were 10.8% the embolic-alone type (Table 3).
and 14.6%, respectively.18,22 If not detected, acute in-stent Park et al DWI (+) Lesion After Intracranial Stenting 3301
Table 1. Risk Factors for MR-DWI (+) Lesions After Intracranial Stenting
P Value (OR, 95% CI) Diabetes mellitus Time from the last symptom to stenting 0.009 (10.443, 1.817–60.032) Vertebral artery Length of stenosis 0.049 (2.124, 1.004–4.490) 0.020 (7.766, 1.379–443.728) In-stent thrombosis BES indicates balloon-expandable coronary stent; CAOD, coronary artery occlusive disease; CI, confidence interval; DP the parent artery distal to the target stenosis; DP , diameter of the parent artery proximal to the target stenosis; ICA, internal carotid artery; MCA, middle cerebral artery; OR, odds ratio; P , P value in the univariate analysis; and P , P value in the logistic regression analysis.
*Fisher exact test.
3302 Stroke November 2014
Table 2. Characteristics and Outcomes of 4 Patients With
(SAMMPRIS) trial, smoking was protective against isch- Periprocedural Symptomatic Ischemic Complications
emic stroke poststenting. Also, in our study, smoking seemed to show a protective effect against DWI (+) poststenting Discharge Final mRS Pre-MR Stent Type Post-MR (Table 1). Bang et al26 reported that current smoking was independently and negatively correlated to poor long-term outcome after atherosclerotic stroke. Although there are still VA Stroke Embolic many controversies, several possible mechanisms were sug- gested: (1) effects of nicotine on angiogenesis or hemostasis, F MCA Stroke Mixed Wingspan (2) chronic obstruction resulting in increased tissue threshold BA indicates basilar artery; BES, balloon-expandable coronary stent; F, or ischemic preconditioning and enhancing collateral flows to female; Loc, location of the target stenosis; M, male; MCA, middle cerebral the ischemic penumbra, and (3) short-acting increase in blood artery; MR, magnetic resonance; mRS, modified Rankin scale score; Sx, type pressure as a compensatory mechanism enhancing perfusion of presenting symptom; TIA, transient ischemic attack; and VA, vertebral artery.
to the ischemic penumbra.27 Of the patients with DWI (+), there was no difference in thrombosis can cause a severe infarction. Fortunately, acute the number or the total volume of DWI (+) between SIC and in-stent thrombosis in our study and the previous 2 reports asymptomatic patients. However, SIC occurred more fre- could be resolved by intra-arterial or intravenous glycoprotein quently in stenosis-associated perforator/mixed type than in IIb/IIIa inhibitor infusion with or without small amount of a embolic-alone type. This result seemed to correspond with fibrinolytic agent. As a result, there was no case of a neurolog-ical sequelae in the 3 case series including this study.
post hoc analyses of a recent randomized controlled trial on rate of in-stent thrombosis after Wingspan stenting seemed stenting versus aggressive medical therapy for intracranial to be higher than that after stenting for coiling. It is likely arterial stenosis.28–30 In those analyses, most symptomatic peri- because Wingspan stent was applied to ICAS, an entirely dif- procedural ischemic strokes were perforator territory infarc- ferent neurovascular disease from aneurysm.
tions (71.4%) in close proximity to the target stenosis. Unlike 22 In addition, the cause of acute in-stent thrombosis may be related to resistance carotid artery stenting, where DWI (+) was exclusively caused to antiplatelet drugs. Aspirin and clopidogrel resistance occurs by distal emboli from carotid atheromatous plaques or aortic in an ≈17% of patients undergoing coronary stent placement.23 arches, DWI (+) after intracranial stenting can occur because Procedure-related thromboembolic events in coil emboliza- of distal emboli, perforator compromise from the snowplow tion occurred more frequently in nonresponder to antiplatelet effect of plaques during angioplasty, or both. Patients with premedication.24 In our study and the previous 2 reports, anti- prestenting perforator infarction closely related to target ste- platelet drug resistance test was not performed routinely, and nosis showed a higher perforator stroke rate after elective therefore, adjustment or change of antiplatelet premedication stenting.31 Therefore, in line with previous studies, our results for nonresponder was not done. It might affect the rates of suggest that ICAS presenting with adjacent perforator isch- in-stent thrombosis and intracranial hemorrhage in our study. emia may contraindicate intracranial stenting.
Recently, Alexander et al25 reported a proceeding in which, This study has the several limitations inherent in the ret- with adjustment or change of antiplatelet premedication for rospective nature. In addition, another limitation is that nonresponders or hyperresponder, no case of acute in-stent MR-DWI was not obtained between diagnostic angiography thrombosis or intraparenchymal hemorrhage occurred after and the stenting procedure in all patients. Therefore, silent Wingspan stenting in 154 patients. This result suggests that embolism during diagnostic angiography or from the target antiplatelet resistance test and adjustment of mediation for lesion between prestenting and poststenting MR might have nonresponder or hyperresponder should be performed before increased the rate of DWI (+). To decrease the influence of such silent embolism on our results, only obvious new lesions In Stenting and Aggressive Medical Management for in brain parenchyma downstream from the location of the Preventing Recurrent Stroke in Intracranial Stenosis guiding catheter during the stenting procedure were assessed. Pre- and poststenting cognitive functions were not assessed in this study so that the relationship between cognitive function Table 3. Relationship Between DWI (+) and Symptomatic
and silent DWI (+) could not be evaluated. It may be another limitation of this study. Silent DWI (+) may affect cognitive Symptomatic Ischemic function decline.32 However, another studies failed to show Complications, n (%) the correlation between silent DWI (+) and cognitive function change.33,34 Therefore, it should be addressed in the further Numbers, median (range) prospective study.
Volume, median (range), mm3 329.8 (76–883.5) 119.5 (32.5–873.0) 0.280*Distribution, n (%) The incidence of DWI (+) after intracranial stenting was Perforator or mixed 35.0%. Middle cerebral artery, smaller distal parent artery, and treatment-related dissection were independent risk factors DWI indicates diffusion-weighted imaging.
*Mann–Whitney U test.
for DWI (+). Of the patients with DWI (+), there was no dif- †Fisher exact test.
ference in the number or in the volume of DWI (+) between Park et al DWI (+) Lesion After Intracranial Stenting 3303
SIC and asymptomatic patients. However, SIC occurred more 15. Qureshi AI, Feldmann E, Gomez CR, Johnston SC, Kasner SE, Quick frequently in the perforator/mixed type than in the embolic- DC, et al. Intracranial atherosclerotic disease: an update. Ann Neurol. 2009;66:730–738.
16. Wong KS, Huang YN, Gao S, Lam WW, Chan YL, Kay R. Intracranial stenosis in Chinese patients with acute stroke. Neurology. Sources of Funding
17. Jiang WJ, Yu W, Du B, Gao F, Cui LY. Outcome of patients with ≥70% This study was supported by a faculty research grant of Yonsei symptomatic intracranial stenosis after Wingspan stenting. Stroke. University College of Medicine for 6-2014-0071.
18. Shin YS, Kim BM, Suh SH, Jeon P, Kim DJ, Kim DI, et al. Wingspan stenting for intracranial atherosclerotic stenosis: clinical outcomes and risk factors for in-stent restenosis. Neurosurgery. 2013;72:596–604.
19. Alurkar A, Karanam LS, Oak S, Nayak S, Sorte S. Role of balloon- expandable stents in intracranial atherosclerotic disease in a series of 182 20. Russjan A, Goebell E, Havemeister S, Thomalla G, Cheng B, Beck C, 1. Lutsep HL, Albers GW, DeCrespigny A, Kamat GN, Marks MP, Moseley et al. Predictors of periprocedural brain lesions associated with carotid ME. Clinical utility of diffusion-weighted magnetic resonance imaging stenting. Cerebrovasc Dis. 2012;33:30–36.
in the assessment of ischemic stroke. Ann Neurol. 1997;41:574–580.
21. Albayram S, Selcuk H, Kara B, Bozdag E, Uzma O, Kocer N, et al. 2. Schlaug G, Siewert B, Benfield A, Edelman RR, Warach S. Time course Thromboembolic events associated with balloon-assisted coil embo- of the apparent diffusion coefficient (ADC) abnormality in human lization: evaluation with diffusion-weighted MR imaging. AJNR Am J stroke. Neurology. 1997;49:113–119.
3. Kato K, Tomura N, Takahashi S, Sakuma I, Watarai J. Ischemic lesions 22. Lawson MF, Fautheree GL, Waters MF, Decker DA, Mocco JD, Hoh B. related to cerebral angiography: evaluation by diffusion weighted MR Acute intraprocedural thrombus formation during Wingspan intracranial 4. Tsumoto T, Terada T, Tsuura M, Matsumoto H, Masuo O, Yamaga H, stent placement for intracranial atherosclerotic disease. Neurosurgery. et al. Diffusion-weighted imaging abnormalities after percutaneous 2010;67(ons suppl 1):ons 166–ons170.
transluminal angioplasty and stenting for intracranial atherosclerotic dis- 23. Grossmann R, Sokolova O, Schnurr A, Bonz A, Porsche C, Obergfell ease. AJNR Am J Neuroradiol. 2005;26:385–389.
A, et al. Variable extent of clopidogrel responsiveness in patients after 5. Bendszus M, Stoll G. Silent cerebral ischaemia: hidden fingerprints of coronary stenting. Thromb Haemost. 2004;92:1201–1206.
invasive medical procedures. Lancet Neurol. 2006;5:364–372.
24. Kang HS, Kwon BJ, Kim JE, Han MH. Preinterventional clopidogrel 6. Forbes KP, Shill HA, Britt PM, Zabramski JM, Spetzler RF, Heiserman response variability for coil embolization of intracranial aneurysms: JE. Assessment of silent embolism from carotid endarterectomy by use of clinical implications. AJNR Am J Neuroradiol. 2010;31:1206–1210.
diffusion-weighted imaging: work in progress. AJNR Am J Neuroradiol. 25. Alexander M, Nuno M, Alexander J, Agutos C, Yu W. Intracranial stent- ing for atherosclerotic disease with aggressive anti-platelet therapy 7. Park KY, Kim DI, Kim BM, Nam HS, Kim YD, Heo JH, et al. Incidence management: a consecutive series of 154 patients. J Neurointerv Surg. of embolism associated with carotid artery stenting: open-cell versus closed-cell stents. J Neurosurg. 2013;119:642–647.
26. Bang OY, Park HY, Lee PH, Kim GM, Chung CS, Lee KH. Improved 8. Rordorf G, Bellon RJ, Budzik RE Jr, Farkas J, Reinking GF, Pergolizzi outcome after atherosclerotic stroke in male smoker. J Neurol Sci. RS, et al. Silent thromboembolic events associated with the treatment of unruptured cerebral aneurysms by use of Guglielmi detachable coils: 27. Bang OY. Possible mechanisms and controversies of protective effects of prospective study applying diffusion-weighted imaging. AJNR Am J risk factors against stroke severity. J Neurol Sci. 2008;267:188–189.
28. Chimowitz MI, Lynn MJ, Derdeyn CP, Turan TN, Fiorella D, Lane 9. Kang DH, Kim BM, Kim DJ, Suh SH, Kim DI, Kim YS, et al. MR-DWI- BF, et al; SAMMPRIS Trial Investigators. Stenting versus aggres- positive lesions and symptomatic ischemic complications after coiling of sive medical therapy for intracranial arterial stenosis. N Engl J Med. unruptured intracranial aneurysms. Stroke. 2013;44:789–791.
10. Omran H, Schmidt H, Hackenbroch M, Illien S, Bernhardt P, von der 29. Fiorella D, Derdeyn CP, Lynn MJ, Barnwell SL, Hoh BL, Levy EI, Recke G, et al. Silent and apparent cerebral embolism after retrograde et al; SAMMPRIS Trial Investigators. Detailed analysis of periproce- catheterisation of the aortic valve in valvular stenosis: a prospective, ran- dural strokes in patients undergoing intracranial stenting in Stenting and domised study. Lancet. 2003;361:1241–1246.
Aggressive Medical Management for Preventing Recurrent Stroke in 11. Restrepo L, Wityk RJ, Grega MA, Borowicz L Jr, Barker PB, Jacobs Intracranial Stenosis (SAMMPRIS). Stroke. 2012;43:2682–2688.
MA, et al. Diffusion- and perfusion-weighted magnetic resonance imag- 30. Derdeyn CP, Fiorella D, Lynn MJ, Rumboldt Z, Cloft HJ, Gibson D, ing of the brain before and after coronary artery bypass grafting surgery. et al. Mechanisms of stroke after intracranial angioplasty and stenting in the SAMMPPRIS trial. Neurosurgery. 2013;2:777–795 12. Stolz E, Gerriets T, Kluge A, Klövekorn WP, Kaps M, Bachmann G. 31. Jiang WJ, Srivastava T, Gao F, Du B, Dong KH, Xu XT. Perforator stroke Diffusion-weighted magnetic resonance imaging and neurobiochemical after elective stenting of symptomatic intracranial stenosis. Neurology. markers after aortic valve replacement: implications for future neuropro- tective trials? Stroke. 2004;35:888–892.
32. Huang KL, Ho MY, Chang CH, Ryu SJ, Wong HF, Hsieh IC, et al. 13. Wityk RJ, Goldsborough MA, Hillis A, Beauchamp N, Barker PB, Impact of silent ischemic lesions on cognition following carotid artery Borowicz LM Jr, et al. Diffusion- and perfusion-weighted brain mag- stenting. Eur Neurol. 2011;66:351–358.
netic resonance imaging in patients with neurologic complications after 33. Wasser K, Pilgram-Pastor SM, Schnaudigel S, Stojanovic T, Schmidt H, cardiac surgery. Arch Neurol. 2001;58:571–576.
Knauf J, et al. New brain lesions after carotid revascularization are not 14. Büsing KA, Schulte-Sasse C, Flüchter S, Süselbeck T, Haase KK, Neff associated with cognitive performance. J Vasc Surg. 2011;53:61–70.
W, et al. Cerebral infarction: incidence and risk factors after diagnos- 34. Kang DH, Hwang YH, Kim YS, Bae GY, Lee SJ. Cognitive outcome and tic and interventional cardiac catheterization–prospective evaluation at clinically silent thromboembolic events after coiling of asymptomatic diffusion-weighted MR imaging. Radiology. 2005;235:177–183.
unruptured intracranial aneurysms. Neurosurgery. 2013;72:638–645.

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