Download Neuroendovascular Surgery for Acute Ischemic Stroke: All Patients

GENERAL SCIENTIFIC SESSION 4
GENERAL SCIENTIFIC SESSION 4
Neuroendovascular Surgery for Acute Ischemic
Stroke: All Patients All the Time
Ashish Sonig, MD, MS, MCh*‡
Elad I. Levy, MD, MBA*द
Departments of *Neurosurgery and
§Radiology, Jacobs School of Medicine
and Biomedical Sciences, and ¶Toshiba
Stroke and Vascular Research Center,
University at Buffalo, State University of
New York, Buffalo, New York ‡Department of Neurosurgery, Gates Vascular
Institute at Kaleida Health, Buffalo, New
York
Correspondence:
Elad I. Levy, MD, MBA,
University at Buffalo Neurosurgery,
100 High St, Ste B4,
Buffalo, NY 14203.
E-mail: [email protected]
Copyright © 2016 by the
Congress of Neurological Surgeons.
A
cute stroke is one of the leading causes of
death worldwide; an estimated 85% of
acute strokes are caused by cerebral ischemia, and only 30% to 40% are large-vessel
occlusions amenable to intervention.1,2 An analysis of the long journey of acute stroke management shows the substantial influence of
technology on the safety and efficacy of intraarterial mechanical thrombectomy.
Initial randomized controlled trials (RCTs) of
acute stroke treatment focused on intra-arterial
infusion of thrombolytic agents (Prolyse in Acute
Cerebral Thromboembolism [PROACT] II1 and
the Middle Cerebral Artery Embolism Local
Fibrinolytic Intervention Trial [MELT]3). In the
subsequent years, those trials were followed by
mechanical thrombectomy trials, Interventional
Management of Stroke (IMS) III,4 Synthesis
Expansion: A Randomized Controlled Trial on
Intra-Arterial vs Intravenous Thrombolysis in
Acute Ischemic Stroke (SYNTHESIS Expansion),5 and Mechanical Retrieval and Recanalization of Stroke Clots Using Embolectomy (MR
RESCUE).6 These trials predominantly used
a first-generation thrombectomy device, the
Merci retriever (Stryker, Kalamazoo, Michigan).
The IMS III trial was stopped prematurely
because the results did not show any significant difference in functional outcomes after
thrombectomy plus intravenous recombinant
tissue-type plasminogen activator (tPA) compared with intravenous tPA alone. These
mechanical thrombectomy trials had limitations, primarily that documentation of largevessel occlusion was not obligatory. In
IMS III, 20% of patients randomized to the
endovascular group had no large-vessel occlusion. Clearly, these patients would not benefit
from endovascular therapy.
Technology moved forward, and newer
stent retrievers, the Solitaire (Covidien, Irvine,
California) and the Trevo (Stryker), received
Conformité Européenne approval in 2008 and
2009, respectively. In 2012, they were approved
for use by the US Food and Drug Administration. However, retrievable stents were used in
64 | VOLUME 63 | NUMBER 1 | AUGUST 2016
only a minority of patients in the mechanical
thrombectomy trials. For example, these stents
were used in only 13% of cases in SYNTHESIS
Expansion.5
The year 2015 can be unequivocally called
a watershed moment in the management of acute
stroke secondary to large-vessel occlusion. Five
RCTs favoring mechanical thrombectomy over
medical management with intravenous tPA alone
for large-vessel occlusion in the setting of anterior
circulation stroke were published. These RCTs
(Solitaire With the Intention for Thrombectomy
as Primary Endovascular Treatment [SWIFT
PRIME],7 Multicenter Randomized Clinical
Trial of Endovascular Treatment of Acute
Ischemic Stroke in the Netherlands [MR
CLEAN],8 Extending the Time for Thrombolysis
in Emergency Neurological Deficits–Intra-Arterial
[EXTEND-IA],9 Endovascular Treatment for
Small Core and Anterior Circulation Proximal
Occlusion With Emphasis on Minimizing CT
to Recanalization Times [ESCAPE],10 and
Randomized Trial of Revascularization With
Solitaire FR Device vs Best Medical Therapy in
the Treatment of Acute Stroke Due to Anterior
Circulation Large Vessel Occlusion Presenting
Within Eight Hours of Symptom Onset
[REVASCAT]11) endorsed the superiority of
endovascular treatment over medical management alone. The patients underwent thrombectomy within a time frame of 6 to 12 hours
after symptom onset.7,10
In view of the substantial and conclusive
evidence stemming from these 5 trials, the
American Heart Association/American Stroke
Association guidelines were updated.12 According to the 2015 guidelines update, there is
a Class I (strong) recommendation (Level of
Evidence A) for stent-retriever thrombectomy if
all the following criteria are met: prestroke
modified Rankin Scale (mRS) score of 0 to 1,
acute ischemic stroke receiving intravenous
recombinant tPA within 4.5 hours of onset
according to guidelines from professional medical societies, causative occlusion of the internal
carotid artery (ICA) or proximal middle cerebral
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NEUROENDOVASCULAR SURGERY FOR ACUTE ISCHEMIC STROKE
artery (MCA; M1 segment), age $ 18 years, National Institutes of
Health Stroke Scale (NIHSS) score of $ 6, Alberta Stroke Program
Early CT Score (ASPECTS)13 of $ 6, and treatment can be
initiated (groin puncture) within 6 hours of symptom onset.
The guidelines included IMS III,4 SYNTHESIS Expansion,5
and MR RESCUE6 in their assessment. As mentioned, these
trials preferentially used first-generation embolectomy devices
(predominantly the Merci retriever) for mechanical thrombectomy compared with the stent retrievers used in recent trials
(SWIFT PRIME,7 MR CLEAN,8 EXTEND-IA,9 ESCAPE,10
and REVASCAT11). For thrombectomies in patients with
occlusions of the M2 or M3 portion of the MCA, anterior
cerebral artery, vertebral artery, basilar artery, or posterior cerebral
artery, the guidelines provided a Class IIb, Level of Evidence C
recommendation.12
In the journey of mechanical thrombectomy over the years, it
took 96 to 104,5 years for the Merci stent retriever from its
Conformité Européenne certification in 2002 (US Food and
Drug Administration approval in 2004) to 2012, when
enrollment in different RCTs (IMS III,4 SYNTHESIS Expansion,5 and MR RESCUE6) was completed. Similarly, it took
7 years for the Solitaire and Trevo stent retrievers to find
legitimate application in acute stroke intervention.
This brings us to an important question: Do we need to conduct
RCTs to extend the benefit of this proven technology to other
patients with large-vessel occlusions such as the pediatric population, those with strokes in a different location (ie, the posterior
circulation), and those experiencing the onset of symptoms outside
the therapeutic window (eg, wake-up strokes)? In an attempt to
answer this question, we examine these subsets through a review of
relevant literature and the presentation of illustrative cases.
POSTERIOR CIRCULATION STROKE
Posterior circulation stroke has the highest reported mortality
and morbidity of all strokes.14 With intravenous tPA and intraarterial tPA, recanalization can be achieved in only 50% of
patients, and only 45% to 55% of survivors regain functional
independence.15 It is imperative to find an alternative treatment
approach. Excellent results are found in the literature of mechanical
thrombectomy with modern stent retrievers. The results of
mechanical thrombectomy in the setting of acute vertebrobasilar
occlusion across the globe are summarized in the Table.16-22 In our
single-center series, 75% of patients achieved an mRS score of 0 to
2.22 Similarly, in a multicenter series that included 100 patients
with posterior circulation strokes, good recanalization (Thrombolysis in Cerebral Infarction [TICI] grade 2b or 3) was associated
with favorable outcome.23 In this series, both stent retrieval and
aspiration thrombectomy as primary treatment approaches were
effective in achieving successful recanalization.
Illustrative Case 1
A 34-year-old woman sustained a 30-ft fall. Initially, she developed
neck pain and then left-sided weakness, slurred speech, and left-sided
CLINICAL NEUROSURGERY
facial droop with progressive onset of quadriparesis (NIHSS
score . 20). The patient was intubated at an outside hospital,
and by the time she arrived at the emergency room at our institute,
she was outside the therapeutic window for intravenous tPA
therapy. A computed tomographic (CT) angiogram showed basilar
artery dissection and occlusion. The patient underwent a diagnostic
catheter angiogram that showed basilar and left vertebral artery
dissections (Figure 1A). She subsequently underwent reconstruction
of the basilar artery with 5 Enterprise stents (Codman Neuro,
Raynham, Massachusetts; Figure 1B and 1C), and an Xpert stent
(Abbott Vascular, Santa Clara, California) was deployed to repair
the vertebral artery dissection (Figure 1D-1F). In the first week, the
patient slowly regained trace movements on her left side. She then
continued to improve with overall increased mobility. After 6
months, she became ambulatory with near-normal speech. At the 2year follow-up evaluation, she had an mRS score of 1.
Illustrative Case 2
An 82-year-old woman was referred from an outside hospital
where she was recovering from open reduction and internal fixation
of a right hip fracture. She was unresponsive on examination. Rightsided hemianopia was noticed with left gaze preferences. Palate
elevation was examined and was significant for a left curtain sign and
left tongue deviation. The gag reflex was weak. The corneal reflex was
decreased in the left eye. Strength was 3/5 in both the upper and
lower extremities. The NIHSS score was 21. Her medical history was
significant for atrial fibrillation, status after coronary artery bypass
grafting, type 2 diabetes mellitus, hypertension, hyperlipidemia, and
essential tremor. tPA could not be administered because of her recent
surgery. The patient underwent a CT stroke study (consisting of
noncontrast CT scanning, CT angiography, and CT perfusion
imaging), and an acute basilar artery occlusion was found
(Figure 2A). She then underwent a diagnostic cerebral angiogram
and mechanical thrombectomy with the Solitaire stent retriever
(Figure 2B and 2C). A TICI grade 3 flow was achieved (Figure 2D).
On postprocedural day 1, her NIHSS score was 1. In view of her
recent hip surgery, she was discharged to a rehabilitation facility.
ACUTE ICA OCCLUSION WITH OR WITHOUT
TANDEM LESIONS
Acute ICA occlusion carries significant mortality and morbidity
and is more resistant to recanalization with intravenous tPA than are
MCA occlusions.24 The recanalization rate associated with intravenous tPA for ICA occlusion is similar to the natural history of
these occlusions.25 Recent trials7-11 have shown that intravenous
tPA has a lower recanalization rate compared with stent retrievers in
the setting of large-vessel occlusion. These trials did not study
extracranial ICA occlusions and tandem lesions. In another study,26
50 consecutive patients with complete or near-total occlusion of
the ICA were treated with aspiration, angioplasty, and/or stent
placement in conjunction with retrieval devices. Successful
recanalization (TICI grade . 2) was obtained in 45 of 50 patients
VOLUME 63 | NUMBER 1 | AUGUST 2016 | 65
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SONIG AND LEVY
66 | VOLUME 63 | NUMBER 1 | AUGUST 2016
TABLE 1. Stent Retrievers for Acute Basilar Artery Occlusiona
Series, Year
Stent Retriever Used for Treatment
Mourand et al,21 2014
Baek et al,16 2014
Mohlenbruch et al,19 2014
Dorn et al,17 2012
Espinosa de Rueda et al,18 2013
Mordasini et al,20 2013
Patients,
n
Median NIHSS Score at
Presentation
Occlusion TICI Grade 0 Flow,
% of cases
Intravenous tPA, %
of cases
31
25
24
24
18
14
15
11
24
16
20.4
21
31 (100)
25 (100)
22 (91.7)
NA
16 (88.8)
14 (100)
19 (61)
NA
21 (87.5)
NA
NA
5 (35.7)
12
20
12 (100)
5 (41.5)
Sonig et al,22 2015
Solitaire FR
Solitaireb
Solitaire FR or Revive SE
Solitaire FR
Solitaire AB, Solitaire FR, or Trevo
Solitaire FR in 10 patients, permanent stent/
angioplasty in 4
Solitaire FR-10 cases, Trevo-2 cases
Series, Year
Postprocedural TICI
Grade 2-3 Flow, % of
cases
Time From Symptom
Onset to Groin
Puncture, min
Time From Arterial
Puncture to
Recanalization, min
mRS Score of 0-2 at 90Day or Last Follow-up,
n (%)
Mortality
(mRS Score,
6), n (%)
Perioperative
Intracerebral
Hemorrhage, n (%)
23 (74.2)
24 (96)
21 (87.5)
17 (77.9)
17 (94.4)
14 (100)
11 (91.7)
444 (median)
285 (median)
254 (median)
NA
365.9 (mean)
414 (median)
211.25 (mean), 146
(median)
61 (mean)
30 (median)
77 (median)
NA
75.1 (mean)
47 (median)
49.9 (mean), 44
(median)
11 (35)
12 (48)
8 (33)
NA
9 (50)
4 (28.6)
9 (75) (9 of 10 or 90% at
last follow-up)
10 (32)
3 (12)
7 (29)
11 (47.8)
4 (22.2)
5 (35.7)
2 (16.67)
5 (16)
2 (8)
2 (8)
NA
1 (5)
0
0
Mourand et al,21 2014
Baek et al,16 2014
Mohlenbruch et al,19 2014
Dorn et al,17 2012
Espinosa de Rueda et al,18 2013
Mordasini et al,20 2013
Sonig et al,22 2015
a
mRS, modified Rankin Scale; NA, not available; NIHSS, National Institutes of Health Stroke Scale; TICI, Thrombolysis in Cerebral Infarction; tPA, tissue plasminogen activator. Manufacturers: Revive, Codman,
Raynham, Massachusetts; Solitaire AB and FR, Covidien, Irvine, California; and Trevo, Stryker, Kalamazoo, Michigan.
b
Type of Solitaire device (ie, AB or FR) unknown.
Table reproduced with permission from Sonig A, Krishna C, Natarajan SK, et al. Stent retriever-assisted mechanical thrombectomy for acute basilar artery occlusion: single U.S. institution experience [published
online ahead of print November 28, 2015]. Oper Neurosurg. doi: 10.1227/NEU.0000000000001163.22
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NEUROENDOVASCULAR SURGERY FOR ACUTE ISCHEMIC STROKE
CLINICAL NEUROSURGERY
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SONIG AND LEVY
FIGURE 1. A, catheter angiography images (left, anteroposterior view; right, lateral view) show basilar
artery dissection and thrombus (arrows). In view of the dissection and associated clot burden, the patient
underwent stenting of the basilar artery. B, deployed Enterprise stent (Codman Neuro, Raynham,
Massachusetts; left, arrow) and the remaining basilar occlusion (right). C, left vertebral artery angiographic run after subsequent placement of 4 additional Enterprise stents (arrows), followed by repair of the
left vertebral artery dissection by placement of an Xpert stent (Abbott Vascular, Santa Clara, California; D,
left, before reconstruction; arrow, dissection; right, after reconstruction). E, final injection from the left
vertebral artery. F, follow-up computed tomographic angiogram on postoperative day 7 shows normal flow
through the left vertebral and basilar arteries.
(90%), and good outcome (mRS score , 2) at 6 months was
obtained in 30 of 50 patients (60%).
Similarly, our previously published systematic review27 showed
that endovascular therapy for ICA occlusion results in more
favorable clinical outcomes than intravenous tPA therapy alone.
In our study, we analyzed a total of 969 patients. Favorable
outcomes (mRS score of # 2 or Barthel Index of 90-100) were
significantly more frequent in patients who underwent endovascular treatment than in those treated with intravenous thrombolysis alone (33.6% vs 24.9%; P = .004).
A convoluted situation arises when a tandem occlusion is
encountered along with an ICA occlusion: The extracranial carotid
artery may or may not be completely occluded. In this situation,
placement of an extracranial carotid stent may be necessary to obtain
distal access. This extra step increases the complexity of the
procedure,28 and the addition of antiplatelet medications, required
in conjunction with carotid stent placement, carries an additional
risk of hemorrhage. However, the risks and benefits of the
procedure must be taken into consideration. Intravenous tPA
alone in a such a situation may yield a poor recanalization rate and
functional outcome compared with mechanical thrombectomy and
extracranial carotid stenting.29 In one of the largest case series of
stent implantation for proximal ICA occlusion and intra-arterial
thrombolysis for tandem occlusion, 26 of 35 consecutively treated
patients (74.3%) had a TICI grade of 2b or 3 after intervention.30
Symptomatic intracerebral hemorrhage occurred in only 1 patient.
At the 3-month follow-up, the median NIHSS score was 4.
Illustrative Case 3
A 64-year-old man presented with right leg weakness, difficulty
with word finding, and blurring of vision in the left eye. His NIHSS
score was 15. His medical history was remarkable for type 2 diabetes
mellitus and atrial fibrillation. CT perfusion imaging showed an
increase in time to peak in the left MCA territory with minimal loss
of cerebral blood volume (Figure 3A). CT angiography (Figure 3B
and 3C) showed left ICA dissection, M2 MCA occlusion, and
occlusion at the origin of the left ICA. However, the venous phase
of 4-dimensional CT angiography showed pseudo-occlusion of the
left ICA (Figure 3B). The patient underwent diagnostic angiography (Figure 3D), proceeded by stenting of the left ICA for the
dissection and thrombectomy of the superior and inferior MCA
divisions (Figure 3E-3G). The immediate postprocedural angiogram showed TICI grade 3 flow in the superior and inferior
68 | VOLUME 63 | NUMBER 1 | AUGUST 2016
divisions of the left MCA (Figure 3H). After the procedure, the
patient’s NIHSS score improved to 6. The 3-month follow-up CT
angiogram showed patency of the left ICA and MCA (Figure 3I).
At the last follow-up at 6 months, the patient’s mRS score was 1
and NIHSS score was 2.
WAKE-UP STROKE
Studies have shown that the time of stroke symptom onset is
uncertain for between 8% and 25% of patients who arrive at the
emergency room.31,32 Most such patients are those who were
sleeping and woke up with a neurological deficit. The current
guidelines (Level 1 evidence) advocate mechanical thrombectomy
for large-vessel occlusion within 6 hours of symptom onset.12
Thus, patients with wake-up stroke cannot reap the full benefit of
intervention. In such cases, viable brain tissue can be reliably
identified only through neuroimaging. Recently conducted
RCTs (ie, EXTEND-IA9 and SWIFT PRIME7) used CT
perfusion imaging for the assessment of brain tissue viability.
Another trial, ESCAPE,10 extended the intervention to 12 hours
from symptom onset. The assessment of viability was based on
the ASPECTS on noncontrast brain CT images. In this trial, 49
patients had symptom onset for $ 6 hours before intervention.
The mRS scores at 90 days after intervention for this cohort and
the cohort with time of onset of , 6 hours were not significantly
different (rate ratio, 1.7; 95% confidence interval, 0.7-4.0).
We performed a multicenter retrospective analysis of 52
consecutive patients with wake-up stroke who underwent
mechanical thrombectomy.33 In our study, 46 patients (88%)
were treated with stent retrievers, and 6 (12%) were treated with
primary aspiration thrombectomy alone. TICI grade 2b or 3
recanalization was achieved in 36 patients (69%), and a 90-day
mRS score of 0 to 2 was achieved in 25 patients (48%).
Currently, a randomized trial, Trevo and Medical Management
vs Medical Management Alone in Wake Up and Late Presenting
Strokes (DAWN; NCT02142283), is underway in the United
States. Enrollment depends on the viability of brain tissue identified
with CT perfusion imaging and is extended to patients in whom
treatment is initiated up to 24 hours from the onset of symptoms.
Illustrative Case 4
An 86-year-old woman was found unresponsive in the morning;
her NIHSS score was 12 at the time of presentation to the
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FIGURE 2. A, computed tomographic (CT) angiographic reconstruction shows basilar artery occlusion (arrow). B, diagnostic angiogram, left vertebral artery injection,
shows midbasilar occlusion. C, microcatheter injection (left, anteroposterior projection; right, lateral projection) shows good distal flow in the right posterior cerebral
artery. D, final angiographic run shows Thrombolysis in Cerebral Infarction grade 3 flow after thrombectomy with the Solitaire stent retriever (Covidien, Irvine, California).
emergency room. She had last been seen in normal condition 14
hours earlier. Her medical history was remarkable for hypertension, dyslipidemia, reflux disease, and osteoporosis. CT perfusion
imaging (Figure 4A) showed increased time to peak in the left
MCA territory with preserved cerebral blood volume and
cerebral blood flow. CT angiography showed a left M1 occlusion
(Figure 4B). The patient underwent a diagnostic angiogram and
mechanical thrombectomy, which resulted in TICI grade 3 flow
(Figure 4C). Postthrombectomy magnetic resonance imaging
obtained on postoperative day 1 showed a small left basal ganglia
infarct and a left frontal infarct (Figure 4D). At the time of
CLINICAL NEUROSURGERY
discharge, the patient’s NIHSS score was 3. At the last follow-up
(6 weeks), her mRS score was 2.
ABSENCE OF LEVEL 1 EVIDENCE DOES NOT
MEAN ABSENCE OF CREDIBLE EVIDENCE
With the current evidence in favor of thrombectomy for
anterior circulation stroke, it may be unethical to randomize
patients with posterior circulation stroke, wake-up stroke, or
acute ICA with and without tandem occlusion or the pediatric
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SONIG AND LEVY
FIGURE 3. A, computed tomographic (CT) perfusion imaging shows preserved cerebral blood volume (left) and increased time to peak in the left middle cerebral artery
(MCA) territory (right). B, CT angiographic reconstruction shows left internal carotid artery (ICA) occlusion and left M2 MCA occlusion. In the early phase of
4-dimensional CT angiography (left), the left ICA was not visualized, and occlusions of the inferior (arrowhead) and superior (arrow) divisions of the left MCA were
evident. In the late venous phase of 4-dimensional CT angiography (right), the left ICA was visualized (arrow). C, axial CT angiography of the neck showed
a dissection flap (arrow). D, right common carotid artery injection shows left MCA occlusion (left); early phase of left common carotid artery injection shows left ICA
dissection (right, arrow). The dissection flap was navigated, and an inferior MCA thrombectomy was performed with a Solitaire stent retriever (Covidien, Irvine,
California). E, partially occluded inferior MCA division before (left, black arrow) and after (right, white arrow) thrombectomy. F, Thrombolysis in Cerebral
Infarction (TICI) grade 3 flow in the left superior MCA division after thrombectomy (arrow). G, owing to the tortuosity of the left proximal ICA, a Pipeline
Embolization Device (Covidien) was deployed (left, arrow); subsequent complete reconstruction of the left ICA dissection is seen (right). H, final injection showing
TICI grade 3 flow in the superior and inferior divisions of the left MCA. I, follow-up CT angiogram at 3 months shows normal flow through the left ICA and MCA.
stroke population to receive medical management vs thrombectomy. Moreover, the prevalence of acute ischemic stroke in
the pediatric population is so low34 that an RCT cannot be
conceived.
70 | VOLUME 63 | NUMBER 1 | AUGUST 2016
Current trials have established the safety and efficacy of
mechanical thrombectomy in the setting of acute stroke. The
benefits must be extended to cover various populations, lesion
locations, and extended time frames. There is good reason to
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NEUROENDOVASCULAR SURGERY FOR ACUTE ISCHEMIC STROKE
FIGURE 4. A, computed tomographic (CT) perfusion imaging shows preserved cerebral blood volume (left), increased time to peak (center), and preserved cerebral blood
flow (right). B, CT angiographic reconstruction shows left middle cerebral artery (MCA) occlusion (arrow). The patient was taken for mechanical thrombectomy. C, left
internal carotid artery injection showed a left MCA occlusion (left, arrow); Thrombolysis in Cerebral Infarction grade 3 flow was achieved after thrombectomy with the
Solitaire stent retriever (right; Covidien, Irvine, California). D, postthrombectomy magnetic resonance imaging obtained on postoperative day 1 shows a small left basal
ganglia infarct (left) and a left frontal infarct (right).
think that the pace of change will increase with time as new
technology brings the concept of disruptive innovation to the
forefront. The older Merci retriever technology has largely been
replaced by that of the current generation of stent retrievers.
With time, endovascular intervention for acute stroke will
become more efficacious and safer. RCTs will remain the gold
standard and will help the physician to formulate practice
patterns. However, in situations in which RCTs have unambiguously shown benefit in favor of the extension of certain
device technology in the therapeutic spectrum on the basis of the
results of multicenter retrospective studies, single-arm prospective registries are a very good option.
Disclosures
Dr Levy has shareholder/ownership interests in Intratech Medical Ltd,
Blockade Medical LLC, and NeXtGen Biologics. He serves as a national
principal investigator for the Covidien US SWIFT PRIME trials and receives
honoraria for training and lecturing from that company. He receives compensation from Abbott for carotid training sessions for physicians. He serves as
a consultant to Pulsar and Blockade Medical and on the Acute Ischemic Stroke
Clinical Advisory Board for Stryker and the Advisory Board for NeXtGen
Biologics and MEDX. Dr Sonig has no financial relationships to disclose. No
funding was received directly in conjunction with this work.
CLINICAL NEUROSURGERY
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Acknowledgments
We thank Paul H. Dressel, BFA, for preparation of the illustrations and Debra
J. Zimmer for editorial assistance.
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