(Stroke. 1995;26:1231-1233.)
© 1995 American Heart Association, Inc.
Articles |
Plaque Ulceration and Lumen Thrombus Are the Main Sources of Cerebral Microemboli in High-grade Internal Carotid Artery Stenosis
From the Department of Neurology (M. Sitzer, M. Siebler, H.S.), Department of Pathology (W.M., W.H.), Department of Vascular Surgery and Renal Transplantation (H.-W.K.), and Institute of General Psychology (L.J.), Heinrich-Heine-University, Düsseldorf, Germany.
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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Background and Purpose Previous work has shown that rates of cerebral microemboli downstream of high-grade internal carotid artery stenosis are higher in recently symptomatic compared with asymptomatic patients. In addition, microembolic rates decline after carotid endarterectomy. We conducted a prospective investigation of 40 consecutive asymptomatic or recently symptomatic patients undergoing carotid endarterectomy for 70% to 95% internal carotid artery stenosis to determine the relationship between microembolic rate and pathoanatomic features of the carotid plaque.
Methods Transcranial Doppler monitoring including automated emboli detection was performed preoperatively to assess the rate of cerebral microemboli of the ipsilateral middle cerebral artery. The corresponding endarterectomy specimens were evaluated histologically with respect to the occurrence of plaque fissuring, intraplaque hemorrhage, plaque ulceration, or intraluminal thrombosis.
Results There were strong associations between plaque ulceration,
intraluminal thrombosis, and downstream cerebral microemboli
(P
.005, respectively). There were no correlations of
microembolism with plaque fissuring or intraplaque hemorrhage
(P=.82 and P=.28, respectively).
Conclusions We conclude that ulceration and luminal thrombosis of the atheromatous plaque are the main sources of downstream cerebral microemboli in patients with high-grade internal carotid artery stenosis. Our data support the view that these pathoanatomic features may also play a key role in symptom development.
Key Words: carotid artery diseases • carotid endarterectomy • embolism • pathology • ultrasonics
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Noninvasive long-term transcranial Doppler (TCD) ultrasonography of intracranial arterial blood flow velocity spectra can reveal abnormal, high-pitched intensity signals suggesting clinically silent cerebral formed-element embolism.1 2 Several groups have shown that the rate of cerebral microemboli downstream of internal carotid artery (ICA) stenosis is higher in recently symptomatic than in asymptomatic patients3 4 5 6 and that it declines after carotid endarterectomy.7 8 This suggests that cerebral microembolism may reflect a pathogenically relevant process located at the ICA atheroma ("unstable ICA disease"6 ). The main purpose of our study was to investigate the relationship between individual microembolic rates and pathoanatomic features of the corresponding carotid endarterectomy specimens in patients with high-grade ICA stenosis.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Patients
This study prospectively included 40 consecutive inpatients (13 women, 27 men; age range, 41 to 84 years; median, 61 years) enlisted to undergo carotid endarterectomy for extracranial high-grade ICA stenosis (
70% luminal narrowing) as determined by intra-arterial
cerebral angiography also showing a contribution to the blood supply of
the ipsilateral middle cerebral artery via the stenosed ICA. The degree
of ICA stenosis was determined according to the criteria of the North
American Symptomatic Carotid Endarterectomy Trial
(NASCET).9 Also according to NASCET criteria, patients
were defined as symptomatic (n=28) if they had recently (<121 days
before enlistment) experienced transient retinal or cerebral symptoms
or minor ischemic stroke attributable to the high-grade ICA
lesion. Asymptomatic patients were defined as those who had a history
of no (n=10) or only remote (>120 days before enlistment; n=2)
ischemic symptoms. Antiplatelet drugs or oral anticoagulants
had been discontinued for more than 5 days in all patients before TCD
monitoring. Informed consent was obtained from all patients before each
examination.
Transcranial Doppler Monitoring
In all 40 patients, we performed long-term TCD monitoring
(at least two 1-hour recordings on successive days) to measure the rate
of microembolic signals of the middle cerebral artery ipsilateral to
high-grade ICA stenosis. Our technique of TCD monitoring has been
described elsewhere.6 7 10 In brief, a 2-MHz pulsed-wave
transducer was used with the Doppler probe fixed to the left or right
temporal region for transcranial insonation of the middle cerebral
artery. Axial width of the sample volume was set at 15 mm; the middle
cerebral artery was insonated at a depth of 45 to 55 mm. The TCD
criteria for microembolic events, the interobserver reliability with
the use of these criteria (mean proportion of specific agreement=0.91),
and an automated detection method that uses a neural network have been
reported previously.10 In the present study rates of
cerebral microemboli are based on events concordantly identified as
emboli by both a human observer blind for pathological data (on-line)
and the neural net (off-line).
In the symptomatic patients the time interval between the last ischemic symptom and TCD monitoring was 1 to 118 days (median, 11 days). For all patients the interval between TCD monitoring and carotid endarterectomy was 1 to 21 days (median, 4.5 days).
Pathoanatomic Examination
After longitudinal arteriotomy, the carotid atherosclerotic
plaque was excised en bloc by the vascular surgeon (routine
endarterectomy). The fresh specimen was fixed immediately in 4%
paraformaldehyde solution, and a gross photograph was taken on which
areas of particular interest were marked by a pathologist for
consecutive sectioning. After decalcification, the whole specimen was
transversely sectioned into 2-mm-thick slices starting proximally.
After the slices were embedded in paraffin, three or four 5-µm
sections were obtained from each slice and stained with
hematoxylin-eosin and van Gieson's stain.
The following four pathoanatomic features were assessed during gross
morphological and histological examinations performed independently by
two pathologists blind for clinical data and microembolic rates. We
defined plaque fissuring as vertical or oblique plaque surface
disruption of no more than 1000 µm in width, of varying depth, and
without large intimal defects. Interobserver reliability for detecting
so-defined plaque fissuring was 
=0.74 for the present sample
(see below for statistical analysis). We defined intraplaque
hemorrhage as bleeding within the plaque of greater than 1500 µm in
largest diameter. Interobserver reliability for detecting intraplaque
hemorrhage was =0.92 for the present sample. We defined plaque
ulceration as intimal defect larger than 1000 µm in width, exposing
the necrotic core of the atheromatous plaque.
Interobserver reliability for detecting plaque ulceration was =0.75
for the present sample. We defined lumen thrombus as thrombotic
material of more than 300 µm maximum thickness adherent to the plaque
surface. Interobserver reliability for detecting lumen thrombus was
=0.78 for the present sample. Sizes of pathological
abnormalities reported in the following were obtained from histological
examination after the specimens were fixed in paraformaldehyde.
Prevalences of these four pathoanatomic features are based on the
consensus achieved between both pathologists at joint reevaluation of
their data previously obtained independently.
Statistical Analysis
With the use of statistics, the reliabilities between both
pathologists for detecting the aforementioned pathoanatomic
abnormalities were calculated from their independent evaluations of the
entire sample (values given above). We evaluated the four pathoanatomic
features with respect to an association with microembolic rate detected
at TCD (four consecutive 
2 tests). For this
purpose, we subdivided the patients into tertiles according to
individual microembolic rates (0/h, n=13; 5/h, n=14; >5/h, n=12). A
significance level of P=.05 was chosen. Because we performed
four statistical comparisons, values of P<.01 (.05/4) were
considered to indicate significant findings (
-adjustment according
to the modified Bonferroni procedure).11 Additionally, the
proportions of asymptomatic or symptomatic patients in the microemboli
tertiles were compared with the use of 2
analyses.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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In the 12 asymptomatic patients, TCD monitoring of the middle cerebral artery ipsilateral to high-grade ICA stenosis revealed 36 microembolic events during a total investigation time of 24 hours. All events occurred in two patients with individual microembolic rates of 8/h and 10/h (Table 1
). In the 28 symptomatic patients,
615 microemboli were detected in the middle cerebral artery distal to
ICA stenosis during a total recording time of 58.5 hours. Here the
individual rates of microemboli per hour ranged from 0 in three
subjects up to 90 in one (Table 1). No concomitant neurological
symptoms were reported or observed. Symptomatic patients had
significantly higher rates of microemboli than asymptomatic patients
(Table 1; P<.001).
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One carotid endarterectomy specimen of a symptomatic patient was excluded from pathoanatomic examination because of severe distortion (individual microembolic rate, 13/h). Among the remaining 39 specimens plaque fissuring was diagnosed in 49% (n=19), intraplaque hemorrhage in 21% (n=8), plaque ulceration in 44% (n=17), and lumen thrombus in 64% (n=25). The mean widths of plaque fissuring and plaque ulceration were 410±190 (SD) µm and 3770±2130 (SD) µm, respectively. The mean diameter of plaque hemorrhage was 2820±940 (SD) µm. In six specimens plaque hemorrhage showed continuity with the vessel lumen.
The relationship between TCD-detected microembolism and the
pathoanatomic findings is shown in Table 2.
Microembolism was strongly associated with plaque ulceration
(P=.005) and lumen thrombus (P=.0003), whereas no
correlation emerged with intraplaque hemorrhage or plaque fissuring.
Because these data suggested a relationship between lumen thrombus and
plaque ulceration, we performed an additional 2
analysis for these pathoanatomic features. The results confirmed
the assumption (Table 3). As already suggested by Tables 1
and 2, lumen thrombus and plaque ulceration were also more frequent
in symptomatic compared with asymptomatic patients (Table 4).
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Our data provide evidence that ICA plaque ulceration and intraluminal thrombosis are the main sources of ipsilateral microembolism of the middle cerebral artery in patients with high-grade ICA stenosis (Table 2
). In addition, there is a strong relationship
between both of these pathoanatomic features (Table 3). Thus, the
histological hallmarks of unstable ICA stenosis as defined in our study
were the same as those described postmortem for unstable coronary heart
disease and acute peripheral thrombo-occlusive
disease.12 13
In contrast, intraplaque hemorrhage and plaque fissuring were not
associated with cerebral microembolism (Table 2). Thus, we conclude
that TCD is the first noninvasive method capable of detecting and
monitoring plaque ulceration and lumen thrombus as the main
pathoanatomic features of unstable ICA stenosis. Although it is
tempting to speculate on possible clinical implications of this
observation, ongoing prospective studies will have to clarify whether
cerebral microembolism can also predict ischemic events in
atherosclerotic ICA disease.
Numerous previous investigations that used carotid endarterectomy
specimens have provided conflicting data on whether lumen thrombus,
plaque ulceration, or intraplaque hemorrhage are associated with a
history of ischemic symptoms in ICA disease.14 15 16 17 18 19 20 21 22 23 24 25
In our relatively small sample, there was an association between plaque
ulceration and lumen thrombus and recent ischemic symptoms
(Table 4). This concurs with preliminary pathoanatomic results of the
NASCET and Asymptomatic Carotid Atherosclerosis Study26
that also suggest that disruption and resultant intraluminal
thrombosis, but not primary intraplaque hematoma, are the key events
leading to symptom development in atherosclerotic ICA disease.
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Acknowledgments |
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This study was supported by grants from the Deutsche Forschungsgemeinschaft (Si 370/4-1) and the Hermann-und-Lilly-Schilling-Stiftung (Dr Steinmetz). We are indebted to B. Frahm, C. Hache, A. Nachtmann, and D. Bendfeldt for expert technical assistance and to Dr G. Rose, PhD, for computing the neural net–based data analysis.
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Footnotes |
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Reprint requests to Dr Helmuth Steinmetz, Department of Neurology, Heinrich-Heine-University, Moorenstraße 5, PO Box 101007, D-40001 Düsseldorf, Germany.
Received February 22, 1995; revision received April 3, 1995; accepted April 4, 1995.
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G. Devuyst, G.A. Darbellay, J.-M. Vesin, V. Kemeny, M. Ritter, D.W. Droste, C. Molina, J. Serena, R. Sztajzel, P. Ruchat, et al. Automatic Classification of HITS Into Artifacts or Solid or Gaseous Emboli by a Wavelet Representation Combined With Dual-Gate TCD Stroke, December 1, 2001; 32(12): 2803 - 2809. [Abstract] [Full Text] [PDF]
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 G. Orlandi, S. Fanucchi, C. Fioretti, G. Acerbi, M. Puglioli, R. Padolecchia, F. Sartucci, and L. Murri Characteristics of Cerebral Microembolism During Carotid Stenting and Angioplasty Alone Arch Neurol, September 1, 2001; 58(9): 1410 - 1413. [Abstract] [Full Text] [PDF]
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K. Kimura, K. Minematsu, M. Koga, R. Arakawa, M. Yasaka, H. Yamagami, K. Nagatsuka, H. Naritomi, and T. Yamaguchi Microembolic Signals and Diffusion-weighted MR Imaging Abnormalities in Acute Ischemic Stroke AJNR Am. J. Neuroradiol., June 1, 2001; 22(6): 1037 - 1042. [Abstract] [Full Text] [PDF]
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S. Jander, M. Sitzer, A. Wendt, M. Schroeter, M. Buchkremer, M. Siebler, W. Muller, W. Sandmann, and G. Stoll Expression of Tissue Factor in High-Grade Carotid Artery Stenosis : Association With Plaque Destabilization Stroke, April 1, 2001; 32(4): 850 - 854. [Abstract] [Full Text] [PDF]
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G. Manca, G. Parenti, R. Bellina, G. Boni, M. Grosso, W. Bernini, C. Palombo, M. Paterni, G. Pelosi, M. Lanza, et al. 111In Platelet Scintigraphy for the Noninvasive Detection of Carotid Plaque Thrombosis Stroke, March 1, 2001; 32(3): 719 - 727. [Abstract] [Full Text] [PDF]
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 P.M. Rothwell The Interrelation between carotid, femoral and coronary artery disease Eur. Heart J., January 1, 2001; 22(1): 11 - 14. [PDF]
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 T. J. Tegos, E. Kalodiki, M. M. Sabetai, and A. N. Nicolaides Stroke: Pathogenesis, Investigations, and Prognosis: Part II of III Angiology, November 1, 2000; 51(11): 885 - 894. [Abstract] [PDF]
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T. Omae, O. Mayzel-Oreg, F. Li, C. H. Sotak, M. Fisher, and E. C. Haley Jr Inapparent Hemodynamic Insufficiency Exacerbates Ischemic Damage in a Rat Microembolic Stroke Model Editorial Comment Stroke, October 1, 2000; 31(10): 2494 - 2499. [Abstract] [Full Text] [PDF]
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 B. Axisa, A. R. Naylor, N. London, P. R. F. Bell, and M. M. Thompson The Influence of Carotid Plaque Morphology on the Development of Cerebral Symptoms Vascular and Endovascular Surgery, July 1, 2000; 34(4): 309 - 318. [Abstract] [PDF]
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P. M. Rothwell, R. Gibson, and C. P. Warlow Interrelation Between Plaque Surface Morphology and Degree of Stenosis on Carotid Angiograms and the Risk of Ischemic Stroke in Patients With Symptomatic Carotid Stenosis Stroke, March 1, 2000; 31(3): 615 - 621. [Abstract] [Full Text] [PDF]
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P. M. Rothwell and C. P. Warlow Low Risk of Ischemic Stroke in Patients With Reduced Internal Carotid Artery Lumen Diameter Distal to Severe Symptomatic Carotid Stenosis : Cerebral Protection Due to Low Poststenotic Flow? Stroke, March 1, 2000; 31(3): 622 - 630. [Abstract] [Full Text] [PDF]
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J. Golledge, R. M. Greenhalgh, and A. H. Davies The Symptomatic Carotid Plaque Stroke, March 1, 2000; 31(3): 774 - 781. [Abstract] [Full Text] [PDF]
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S. Aoki, H. Nakajima, H. Kumagai, and T. Araki Dynamic Contrast-Enhanced MR Angiography and MR Imaging of the Carotid Artery: High-Resolution Sequences in Different Acquisition Planes AJNR Am. J. Neuroradiol., February 1, 2000; 21(2): 381 - 385. [Abstract] [Full Text]
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J. Molloy and H. S. Markus Asymptomatic Embolization Predicts Stroke and TIA Risk in Patients With Carotid Artery Stenosis Stroke, July 1, 1999; 30(7): 1440 - 1443. [Abstract] [Full Text] [PDF]
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R. T.F. Cheung, L. Valton, and V. Larrue Early Ischemic Recurrence and Microembolic Signals Detected by Transcranial Doppler • Response Stroke, June 1, 1999; 30(6): 1290 - 1290. [Full Text] [PDF]
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J. A. C. Arnold, K. B. Modaresi, N. Thomas, P. R. Taylor, and T. S. Padayachee Carotid Plaque Characterization by Duplex Scanning : Observer Error May Undermine Current Clinical Trials Stroke, January 1, 1999; 30(1): 61 - 65. [Abstract] [Full Text] [PDF]
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J. T. Moroney, E. Bagiella, M. C. Paik, R. L. Sacco, and D. W. Desmond Risk Factors for Early Recurrence After Ischemic Stroke : The Role of Stroke Syndrome and Subtype Stroke, October 1, 1998; 29(10): 2118 - 2124. [Abstract] [Full Text] [PDF]
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L. Valton, V. Larrue, A. P. le Traon, P. Massabuau, and G. Geraud Microembolic Signals and Risk of Early Recurrence in Patients With Stroke or Transient Ischemic Attack Stroke, October 1, 1998; 29(10): 2125 - 2128. [Abstract] [Full Text] [PDF]
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M. Cullinane, R. Wainwright, A. Brown, M. Monaghan, and H. S. Markus Asymptomatic Embolization in Subjects With Atrial Fibrillation Not Taking Anticoagulants : A Prospective Study Stroke, September 1, 1998; 29(9): 1810 - 1815. [Abstract] [Full Text] [PDF]
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S. Jander, M. Sitzer, R. Schumann, M. Schroeter, M. Siebler, H. Steinmetz, and G. Stoll Inflammation in High-Grade Carotid Stenosis : A Possible Role for Macrophages and T Cells in Plaque Destabilization Stroke, August 1, 1998; 29(8): 1625 - 1630. [Abstract] [Full Text] [PDF]
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J. Molloy, N. Khan, and H. S. Markus Temporal Variability of Asymptomatic Embolization in Carotid Artery Stenosis and Optimal Recording Protocols Stroke, June 1, 1998; 29(6): 1129 - 1132. [Abstract] [Full Text] [PDF]
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C. A. C. Wijman, V. L. Babikian, I. C. A. Matjucha, B. Koleini, C. Hyde, M. R. Winter, and V. E. Pochay Cerebral Microembolism in Patients With Retinal Ischemia Stroke, June 1, 1998; 29(6): 1139 - 1143. [Abstract] [Full Text] [PDF]
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 C. Specker, A. Perniok, U. Brauckmann, M. Siebler, and M. Schneider Review : Detection of cerebral microemboli in APS-- Introducing a novel investigation method and implications of analogies with carotid artery disease Lupus, January 1, 1998; 7(2_suppl): S75 - S80. [Abstract] [PDF]
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 L Valton, V Larrue, A P. Le Traon, and G Geraud Cerebral microembolism in patients with stroke or transient ischaemic attack as a risk factor for early recurrence J. Neurol. Neurosurg. Psychiatry, December 1, 1997; 63(6): 784 - 787. [Abstract] [Full Text] [PDF]
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H. S. Markus, R. Ackerstaff, V. Babikian, C. Bladin, D. Droste, D. Grosset, C. Levi, D. Russell, M. Siebler, and C. Tegeler Intercenter Agreement in Reading Doppler Embolic Signals : A Multicenter International Study Stroke, July 1, 1997; 28(7): 1307 - 1310. [Abstract] [Full Text]
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V. L. Babikian, C. A. C. Wijman, C. Hyde, N. L. Cantelmo, M. R. Winter, E. Baker, and V. Pochay Cerebral Microembolism and Early Recurrent Cerebral or Retinal Ischemic Events Stroke, July 1, 1997; 28(7): 1314 - 1318. [Abstract] [Full Text]
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P.-T. Ko, S.-K. Lin, Y.-J. Chang, S.-J. Ryu, C.-C. Chu, and S.-K. Lin Carotid Floating Plaques Associated with Multiple Cerebral Embolic Strokes: Case Reports Angiology, March 1, 1997; 48(3): 255 - 261. [Abstract] [PDF]
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H.-C. Koennecke, H. Mast, S. S. Trocio Jr, R. L. Sacco, J. L. P. Thompson, and J. P. Mohr Microemboli in Patients With Vertebrobasilar Ischemia : Association With Vertebrobasilar and Cardiac Lesions Stroke, March 1, 1997; 28(3): 593 - 596. [Abstract] [Full Text]
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M. Silvestrini, E. Troisi, M. Matteis, L. M. Cupini, and C. Caltagirone Transcranial Doppler Assessment of Cerebrovascular Reactivity in Symptomatic and Asymptomatic Severe Carotid Stenosis Stroke, November 1, 1996; 27(11): 1970 - 1973. [Abstract] [Full Text]
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A.M. Forteza, V.L. Babikian, C. Hyde, M. Winter, and V. Pochay Effect of Time and Cerebrovascular Symptoms on the Prevalence of Microembolic Signals in Patients With Cervical Carotid Stenosis Stroke, April 1, 1996; 27(4): 687 - 690. [Abstract] [Full Text]
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M. Siebler, A. Nachtmann, M. Sitzer, G. Rose, A. Kleinschmidt, J. Rademacher, and H. Steinmetz Cerebral Microembolism and the Risk of Ischemia in Asymptomatic High-Grade Internal Carotid Artery Stenosis Stroke, November 1, 1995; 26(11): 2184 - 2186. [Abstract] [Full Text]
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Z. Kaposzta, J. F. Martin, and H. S. Markus Switching off Embolization From Symptomatic Carotid Plaque Using S-Nitrosoglutathione Circulation, March 26, 2002; 105(12): 1480 - 1484. [Abstract] [Full Text] [PDF]
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