 |
|
Characteristics of Cerebral Microembolism During Carotid Stenting and Angioplasty Alone
Giovanni Orlandi, MD;
Simona Fanucchi, MD;
Cristina Fioretti, MD;
Giovanni Acerbi, MD;
Michele Puglioli, MD;
Riccardo Padolecchia, MD;
Ferdinando Sartucci, MD;
Luigi Murri, MD
Arch Neurol. 2001;58:1410-1413.
ABSTRACT
| |
Background Cerebral microembolism has often been documented by transcranial Doppler
imaging during carotid angioplasty and stenting. However, few data are available
about its characteristics during the 2 different kinds of procedure.
Objectives To compare the incidence of microemboli occurring during angioplasty
alone with that during stenting in the different phases of the procedures
and to relate it to periprocedural cerebrovascular complications.
Patients and Methods Thirty-eight patients underwent 41 procedures (15 angioplasty alone
and 26 stenting) for symptomatic carotid stenoses of 70% or more. Transcranial
Doppler monitoring was performed to detect microemboli in the middle cerebral
artery during 3 phases of the procedure: (1) guidewire crossing, (2) first
dilatation in case of angioplasty alone or stent release with predilatation
if performed, and (3) further dilatation.
Results Microemboli occurred in all cases in phase 1 of the procedure but less
frequently in the arteries treated with stenting when compared with those
treated with angioplasty alone in phase 2 and particularly (P<.02) in phase 3. The mean number of microemboli was highest in
phase 2, predominant (P<.05) during angioplasty
alone, and particularly reduced (P<.02) in phase
3 during the stenting procedures. During 2 (5%) of the 41 procedures, cerebrovascular
complications occurred in phase 1, with the number of microemboli being higher
than mean values.
Conclusions Cerebral microembolism is a very common event, especially during guidewire
crossing and angioplasty alone compared with stenting. Further studies concerning
the prognostic significance of this are advisable.
INTRODUCTION
PERCUTANEOUS transluminal angioplasty and stenting of carotid arteries
represent a promising alternative to endarterectomy for patients with symptomatic
stenosis of 70% or more and a simultaneous high perioperative risk,1, 2 although there is no strong evidence
from clinical trials to show that these procedures are more beneficial than
other surgical or medical treatments.3, 4
Moreover, many periprocedural complications may occur,5
such as ischemic neurological deficits due to distal embolization and hemodynamic
impairment.6 Silent brain embolism has also
been frequently documented on magnetic resonance images obtained before and
after neurointerventional procedures.7
Transcranial Doppler imaging is an useful tool for monitoring and detecting
microemboli in the middle cerebral artery and can reveal a high incidence
of asymptomatic embolization during both carotid angioplasty alone8 and stenting procedures,9
with more than 8 times the rate of microemboli observed during carotid endarterectomy,10 despite low levels of hemodynamic impairment.11
Nevertheless, few data are available regarding differences between periprocedural
microemboli occurring during angioplasty alone and those arising during stenting9; moreover, the role of plaque morphology, which may
be associated with differences both in emboli production12
and in ischemic brain damage,13 is not often
considered.
The aim of this study was to compare a group of patients who underwent
carotid stenting with another group of patients who underwent angioplasty
alone with regard to the occurrence of cerebral microemboli during the different
phases of the 2 procedures and to the relationship between the detection of
microemboli and periprocedural cerebrovascular complications.
PATIENTS AND METHODS
Thirty-eight patients (25 men and 13 women; mean age, 67.8 years; age
range, 54-79 years) recruited between February 1998 and July 2000 underwent
41 procedures for symptomatic internal carotid stenoses (bilateral in 3 cases)
of 70% or more proven by selective angiography and evaluated according to
the criteria of the North American Symptomatic Carotid Endarterectomy Trial.14 All patients presented a high risk (cardiological
in 21 cases and pulmonary in 17) for anesthesia, with contraindications for
endarterectomy, and gave their written informed consent to endovascular treatment.
Fifteen arteries were treated with angioplasty alone and 26 with stent placement.
The aim to obtain 2 groups as homogeneous as possible in plaque morphology
and degree of stenosis determined whether arteries were to be selected for
angioplasty alone or for the stenting procedure. The morphological features
of plaque were determined using a duplex-scanner device (AU5; Esaote Biomedica,
Florence, Italy) according to qualitative criteria15
concerning plaque echogenicity (hypoechoic, isoechoic, or hyperechoic), plaque
texture (homogeneous, heterogeneous, or calcified), and plaque surface (smooth,
irregular, or ulcerated). Table 1
shows the similar distribution of ultrasonographic plaque features and angiographic
mean degree of stenosis in the 2 groups of arteries selected for angioplasty
alone or for stenting.
|
|
|
|
Distribution of Ultrasonographic Plaque Features and Angiographic Degree
of Stenosis in 2 Groups of Arteries
|
|
|
All patients were treated with acetylsalicylic acid (100 mg/d) as a
prevention against stroke recurrence. Mild sedation was achieved with promazine
hydrochloride and intravenous heparin sodium (partial thromboplastin time,
80-100 seconds) was used during the procedure. Moreover, 1 mg of atropine
sulfate was administered intravenously to prevent bradycardia due to carotid
sinus stimulation during the balloon inflation phase. A guiding catheter was
inserted into the common carotid artery, and the stenosis was crossed by a
guidewire (0.014- to 0.020-in coronary guidewires) using road-mapping images.
In the case of angioplasty, balloon catheters (OPTA 5 French or Power-Flex
Plus; Cordis Corp, Miami, Fla) measuring, 5 to 6 mm in diameter were used,
and 2 manual inflations lasting 20 to 30 seconds each were performed. When
we used a stent (Wallstent; Boston Scientific Corp), La Garenne Colombes,
France) (8 x 20, 8 x 30, 10 x 20, and 10 x 30 mm,
fully open), care was taken to cover the entire lesion, and then the stent
was submitted to a single dilatation by a balloon under high pressure. Predilatation
with a 3-mm-diameter balloon catheter was performed before the stent release
in the 5 cases showing the highest degree of stenosis.
A 2-MHz pulse-wave transcranial Doppler device (DWL Elektronische Systeme
Multidop X-TCD7; Sipplingen, Germany) was used in all patients for long-term
insonation of the middle cerebral artery, and monitoring was performed during
the entire procedure. The Doppler probes had a diameter of 1.7 cm and were
fixed to the skull with a head tape placed on the transtemporal acoustic window.
The axial width of the sample volume was set at 10 mm, and the middle cerebral
artery was insonated at a predetermined depth of 45 to 55 mm to obtain optimum
insonation of the vessel. A high-pass filter was set at 100 Hz to eliminate
low-frequency arterial wall vibrations. The ultrasonic power emitted at the
probe surface was 50 to 100 mW/cm2. Intensity was defined as the
power measured in decibels contained in the Doppler spectrum. The algorithm
for signal intensity measurements used the whole screen as a background, and
the scale setting was between -100 and +150 cm/s, corresponding to a
pulse repetition frequency of 6500 Hz. A 64-point fast-Fourier transform,
with a length of 2 milliseconds and an overlap of 60%, was used. The above-mentioned
parameters were chosen according to the recommendations of the International
Consensus Group on Microembolus Detection.16
The transcranial Doppler device used an automated method for detecting high-intensity
transient signals, which were identified as microemboli according to the criteria
of the Ninth International Cerebral Hemodynamic Symposium17:
signal intensity at least 3 dB higher than that of the background blood flow,
signals lasting less than 300 milliseconds, unidirectional signal within the
Doppler velocity spectrum, and association with a characteristic sound known
as a chirp. To improve reproducibility of the data,
an intensity detection threshold higher than 7 dB was chosen for this study.16
Patient behavior and transcranial Doppler recording quality were continuously
observed (on-line) by an investigator (S.F.) who recorded all the events that
could be sources of artifacts. The high-intensity transient signals were recorded
on stereo videotape and analyzed off-line by 2 independent observers (G.O.
and C.F.) who were blind to the clinical data. The  index for interobserver
agreement was 0.91.
Three phases of the procedure were taken into consideration: (1) guidewire
crossing, (2) first dilatation in the case of angioplasty alone or stent release
with predilatation if performed, and (3) further dilatation. The mean number
and mean intensity of the microemboli were evaluated during each phase of
the procedure in the angioplasty-alone group and in the stenting group. During
the passage of the angiographic contrast medium, a wide and high increase
in signal intensity, confusing microemboli detection, was always observed
in the middle cerebral artery; hence, this phase of the procedure was excluded
from data analysis. Moreover, the occurrence of amaurosis fugax, transient
ischemic attack, or stroke was considered a periprocedural cerebrovascular
complication.
Data analysis was performed using 2-way  2 analysis (the
percentage of procedures with microemboli was compared between angioplasty
alone and stenting) and the t test (the mean number
and mean intensity of microemboli were compared between angioplasty alone
and stenting). The level of significance was set at P<.05.
RESULTS
Microemboli occurred in all cases in phase 1 of the procedure. On the
contrary, arteries treated with stenting showed a lower incidence of microemboli
than those treated with angioplasty alone in phase 2 (96% vs 100%) and particularly
(P<.02) in phase 3 (54% vs 87%) of the procedure
(Figure 1).
|
|
|
|
Figure 1. Microemboli detected in the middle
cerebral artery on the same side as the carotid arteries submitted to angioplasty
and stenting during guidewire crossing (phase 1), first dilatation or stent
release with predilatation if performed (phase 2), and further dilatation
(phase 3): percentage of procedures with microemboli (A) and mean ±
SD number of microemboli (B). Single asterisk indicates P<.05;
dagger, P<.02.
|
|
|
The mean ± SD number of microemboli detected in phase 1 in arteries
treated with angioplasty alone (13.5 ± 4.3) showed no difference from
that seen in artieries treated with stenting (14.3 ± 5.2). On the contrary,
the number of microemboli was highest in phase 2, with a significant (P<.05) prevalence in the arteries treated with angioplasty
alone (22 ± 3.0) compared with those treated with stenting (19.1 ±
4.1). The number of microemboli decreased in phase 3 of the procedure and
was particularly lower (P<.02) in the arteries
treated with stenting (10.4 ± 5.2) than in those treated with angioplasty
alone (18.6 ± 4.6) (Figure 1).
There was no significant difference in the intensity of microemboli between
angioplasty alone and stenting during all phases of the procedure.
During 2 (5%) of the 41 procedures performed, cerebrovascular periprocedural
complications (transient ischemic attack in one case treated with angioplasty
alone and stroke in another treated with stenting) arose in phase 1. Both
cases demonstrated a number of microemboli that was much higher than the mean
values for this parameter during the same phase of the procedure, whereas
a similar distribution was observed regarding the intensity of microemboli
(Figure 2). The occurrence of microemboli
was asymptomatic in all other cases. During the dilatation, 3 patients who
were treated with angioplasty alone developed minor periprocedural complications,
consisting of transient bradycardia and sudden arterial hypotension. An angiographic
control, performed at the end of the procedures, documented a residual degree
of stenosis that was less than 30% in all cases.
|
|
|
|
Figure 2. Number and intensity of microemboli
during guidewire crossing in 2 cases with periprocedural cerebrovascular complications:
comparison with mean values. TIA indicates transient ischemic attack.
|
|
|
COMMENT
The occurrence of microemboli appears to be a very common event during
all phases of angioplasty and stenting procedures, especially in patients
treated with angioplasty alone. Mechanical factors, such as trauma on the
plaque surface when the guidewire crosses the stenosis and during the first
dilatation, may account for the high incidence of microemboli detaching from
the atherosclerotic lesion. On the contrary, the progressive decrease in the
number of patients showing microemboli during further dilatation might be
attributed to plaque squashing induced by stenosis dilatation, which makes
the plaque surface less crumbly and also reduces friction by means of the
blood flow velocity being restored to normal. Our findings agree with those
of Markus et al,8 who observed multiple embolic
signals immediately after balloon inflation in 9 of 10 patients treated with
angioplasty alone. Likewise, McCleary et al18
reported embolic signals in 9 of 9 patients during carotid stenting. Plaque
entrapment by the stent after its release might also justify the fact that
fewer patients in the group treated with stenting manifested microemboli during
further dilatation than did the patients in the group treated with angioplasty
alone. Similarly, Benichou and Bergeron9 reported
a prevalence of periprocedural microemboli in 19 cases during angioplasty,
compared with 13 cases detected during stenting. Plaque entrapment by the
stent, likewise a close-mesh net, might also account for the mean number of
microemboli observed both during and after stent release being lower than
that detected during the dilatations in the angioplasty-alone group. Differences
in the morphological features of plaque may be associated with differences
in embolization rate12, 13, 14, 15, 16, 17, 18, 19;
nevertheless, we selected the procedures so that the ultrasonographic plaque
features would be similar in both the angioplasty group and the stenting group.
Therefore, the incidence of microemboli cannot be attributed to differences
in plaque features in the 2 groups, but rather to the 2 different procedures.
With regard to the mean values of microemboli intensity, no substantial difference
was observed between the angioplasty group and the stenting group. However,
this parameter seems to have no clear significance, since it might depend
both on the volume and on the nature of the microemboli,20, 21
and the detection system used cannot supply this type of morphological characterization.
The occurrence of microemboli was found to be symptomatic in only 2
patients (5%) who had cerebrovascular complications related to carotid artery
under endovascular treatment, and both problems arose during guidewire crossing.
This could be related to the high number of microemboli; however, other factors
such as hemodynamic insufficiency accompanying the detachment of emboli may
be involved in ischemic damage, probably because of a reduced microemboli
clearance.22, 23 In this respect,
magnetic resonance studies have confirmed that brain embolization is more
frequent than the apparent neurological complication rate.7
Moreover, Rapp et al24 observed recently that
even small (<200 µm) plaque fragments may later cause neuronal ischemia,
and neuropsychological sequelae have been reported as a consequence of cerebral
microembolism during carotid angioplasty.25
Further studies are required to clarify whether a high number of microemboli
may be the harbinger of cerebrovascular complications.
In view of these findings, it appears that stent placement is safer
than angioplasty alone and that any attempt to avoid the production of microemboli
or their consequences, such as the improvement of neurointerventional methods
or the use of neuroprotective agents, might be advisable.
AUTHOR INFORMATION
Accepted for publication April 23, 2001.
From the Department of Neuroscience (Drs Orlandi, Fanucchi, Fioretti,
Acerbi, Sartucci, and Murri) and the Unit of Neuroradiology (Drs Puglioli
and Padolecchia), University of Pisa, Pisa, Italy.
Corresponding author and reprints: Giovanni Orlandi, MD, Department
of Neuroscience, Clinic of Neurology, Via Roma 67, 56100 Pisa, Italy (e-mail:
g.orlandi{at}neuro.med.unipi.it).
REFERENCES
| |
1. Bergeron P, Becquemin JP, Jausseran JM, et al. Percutaneous stenting of the internal carotid artery: the European
CAST I Study: Carotid Artery Stent Trial. J Endovasc Surg. 1999;6:155-159.
FULL TEXT
|
ISI
| PUBMED
2. Griewing B, Brassel F, von Smekal U, Al Ahmar MT, Kessler C. Carotid artery stenting in patients at surgical high risk: clinical
and ultrasound findings. Cerebrovasc Dis. 2000;10:44-48.
FULL TEXT
|
ISI
| PUBMED
3. Crawley F, Brown MM. Percutaneous transluminal angioplasty and stenting for carotid artery
stenosis. Cochrane Database Syst Rev. 2000;(2):CD000515.
4. Phatouros CC, Higashida RT, Malek AM, et al. Carotid artery stent placement for atherosclerotic disease: rationale,
technique and current status. Radiology. 2000;217:26-41.
FREE FULL TEXT
5. Dorros G. Complications associated with extracranial carotid artery interventions. J Endovasc Surg. 1996;3:166-170.
FULL TEXT
|
ISI
| PUBMED
6. Qureshi AI, Luft AR, Janardhan V, et al. Identification of patients at risk for periprocedural neurological
deficits associated with carotid angioplasty and stenting. Stroke. 2000;31:376-382.
FREE FULL TEXT
7. Bendszus M, Koltzenburg M, Burger R, Warmuth-Metz M, Hofmann E, Solymosi L. Silent embolism in diagnostic cerebral angiography and neurointerventional
procedures: a prospective study. Lancet. 1999;354:1594-1597.
FULL TEXT
|
ISI
| PUBMED
8. Markus HS, Clifton A, Buckenham T, Brown MM. Carotid angioplasty detection of embolic signals during and after the
procedure. Stroke. 1994;25:2403-2406.
ABSTRACT
9. Benichou H, Bergeron P. Carotid angioplasty and stenting: will periprocedural transcranial
Doppler monitoring be important? J Endovasc Surg. 1996;3:217-223.
FULL TEXT
|
ISI
| PUBMED
10. Jordan WD Jr, Voellinger DC, Doblar DD, Plyushcheva NP, Fisher WS, McDwell HA. Microemboli detected by transcranial Doppler monitoring in patients
during carotid angioplasty versus carotid endarterectomy. Cardiovasc Surg. 1999;7:33-38.
FULL TEXT
|
ISI
| PUBMED
11. Crawley F, Clifton A, Buckenham T, Loosemore T, Taylor RS, Brown MM. Comparison of hemodynamic cerebral ischemia and microembolic signals
detected during carotid endarterectomy and carotid angioplasty. Stroke. 1997;28:2460-2464.
FREE FULL TEXT
12. Kownator S, Luizy F, Henry M, Amor M, Foliguet B, Chati Z. Relationship between the structure of the plaque and the importance
of embolization during carotid angioplasty [abstract]. J Am Coll Cardiol. 2000;35(suppl A):67.
13. AbuRahma AF, Covelli MA, Robinson PA, Holt SM. The role of carotid duplex ultrasound in evaluating plaque morphology:
potential use in selecting patients for carotid stenting. J Endovasc Surg. 1999;6:59-65.
FULL TEXT
|
ISI
| PUBMED
14. North American Symptomatic Carotid Endarterectomy Trial (NASCET) Steering
Committee. North American Symptomatic Carotid Endarterectomy Trial: methods, patient
characteristics and progress. Stroke. 1991;22:711-720.
FREE FULL TEXT
15. De Bray JM, Baud JM, Dauzat M. Consensus concerning the morphology and the risk of carotid plaques. Cerebrovasc Dis. 1997;7:289-296.
16. Markus HS, Ackerstaff R, Babikian V, et al. Intercenter agreement in reading Doppler embolic signals: a multicenter
international study. Stroke. 1997;28:1307-1310.
FREE FULL TEXT
17. Consensus Committee of the Ninth International Cerebral Hemodynamic
Symposium. Basic identification criteria of Doppler microembolic signals. Stroke. 1995;26:1123.
FREE FULL TEXT
18. McCleary AJ, Nelson M, Dearden NM, Calvey TA, Gough MJ. Cerebral hemodynamics and embolization during carotid angioplasty in
high risk patients. Br J Surg. 1998;85:771-774.
FULL TEXT
|
ISI
| PUBMED
19. Sitzer M, Muller W, Siebler M, et al. Plaque ulceration and lumen thrombus are the main sources of cerebral
microemboli in high-grade internal carotid artery stenosis. Stroke. 1995;26:1231-1233.
FREE FULL TEXT
20. Markus H. Transcranial Doppler detection of circulating cerebral emboli: a review. Stroke. 1993;24:1246-1250.
FREE FULL TEXT
21. Markus HS, Brown MM. Differentiation between different pathological cerebral embolic materials
using transcranial Doppler in vitro model. Stroke. 1993;24:1-5.
FREE FULL TEXT
22. Caplan LR, Hennerici M. Impaired clearance of emboli (washout) in an important link between
hypoperfusion, embolism and ischemic stroke. Arch Neurol. 1998;55:1475-1482.
FREE FULL TEXT
23. Omae T, Mayzel-Oreg O, Li F, Sotak CH, Fisher M. Inapparent hemodynamic insufficiency exacerbates ischemic damage in
a rat microembolic stroke model. Stroke. 2000;31:2494-2498.
FREE FULL TEXT
24. Rapp JH, Pan XM, Sharp FR, et al. Atheroemboli to the brain: size threshold for causing acute neuronal
cell death. J Vasc Surg. 2000;32:68-76.
FULL TEXT
|
ISI
| PUBMED
25. 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.
FREE FULL TEXT
RELATED ARTICLE
Archives of Neurology Reader's Choice: Continuing Medical Education
Arch Neurol. 2001;58(9):1503-1504.
FULL TEXT
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES
|
The Significance of Incomplete Stent Apposition in Patients Undergoing Stenting of Internal Carotid Artery Stenosis
Onizuka et al.
Am. J. Neuroradiol. 2006;27:1505-1507.
ABSTRACT
| FULL TEXT
Spontaneous Improvement of Peristent Ulceration after Carotid Artery Stenting
Kohyama et al.
Am. J. Neuroradiol. 2006;27:151-156.
ABSTRACT
| FULL TEXT
The Amount of Solid Cerebral Microemboli during Carotid Stenting Does Not Relate to the Frequency of Silent Ischemic Lesions
Rosenkranz et al.
Am. J. Neuroradiol. 2006;27:157-161.
ABSTRACT
| FULL TEXT
Silent Cerebral Ischemia Detected With Diffusion-Weighted Imaging in Patients Treated With Protected and Unprotected Carotid Artery Stenting
Cosottini et al.
Stroke 2005;36:2389-2393.
ABSTRACT
| FULL TEXT
Value of US in Selecting Patients for Carotid Angioplasty and Stent Placement * Drs Vos and Ackerstaff respond:
Bluth et al.
Radiology 2005;237:374-375.
FULL TEXT
Impaired Clearance of Microemboli and Cerebrovascular Symptoms During Carotid Stenting Procedures
Orlandi et al.
Arch Neurol 2005;62:1208-1211.
ABSTRACT
| FULL TEXT
Efficacy of Treatment of Severe Carotid Bifurcation Stenosis By Using Self-Expanding Stents without Deliberate Use of Angioplasty Balloons
Lownie et al.
Am. J. Neuroradiol. 2005;26:1241-1248.
ABSTRACT
| FULL TEXT
Focal ischemia of the brain after neuroprotected carotid artery stenting
Schluter et al.
J Am Coll Cardiol 2003;42:1007-1013.
ABSTRACT
| FULL TEXT
Editorial Comment--Carotid Artery Stenting With or Without Protection Devices? Strong Opinions, Poor Evidence!
Eckert and Zeumer
Stroke 2003;34:1941-1943.
FULL TEXT
Controversies in Carotid Stenting
Taylor et al.
VASC ENDOVASCULAR SURG 2003;37:79-87.
ABSTRACT
Current concepts of mechanical cerebral protection during precutaneous carotid intervention
Macdonald and Gaines
Vasc Med 2003;8:25-32.
ABSTRACT
|
