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- •Neurosonology and Neuroimaging of Stroke
- •Foreword
- •Foreword
- •Table of Contents
- •Physics of Flow
- •Flow Pattern and Flow Velocity
- •Ultrasound Principles
- •Doppler Effect
- •Doppler Shift and Flow Velocity
- •List of Abbreviations
- •Introduction
- •Part A Principles and Rules
- •1 Flow and Ultrasound Basics
- •Flow Dynamics
- •Ultrasound Systems
- •Ultrasound Transducer
- •Imaging Modalities, Parameters, and Settings
- •2 Vascular Anatomy and Structure of Ultrasound Examination
- •General Arterial Anatomy
- •Extracranial Arterial Anatomy
- •Intracranial Arterial Anatomy
- •General Structure of Arterial Ultrasound Examination
- •Special Arterial Anatomy and Ultrasound Anatomy
- •Extracranial Arteries
- •Intracranial Arteries
- •General Venous Anatomy
- •Intracranial Venous Anatomy
- •Extracranial Venous Anatomy
- •General Structure of Venous Ultrasound Examination
- •Special Venous Anatomy and Ultrasound Anatomy
- •Intracranial Veins and Sinuses
- •Extracranial Veins
- •3 Intracranial Hemodynamics and Functional Tests
- •Autoregulation
- •Testing of Autoregulation
- •Neurovascular Coupling
- •Testing of Neurovascular Coupling
- •Metabolic Coupling
- •Other Tests to Assess Differences Between the Right and Left Sides as Markers of Impaired Collateral Function
- •Parameters of Cerebral Hemodynamics
- •Cerebral Blood Flow Velocity
- •Resistance Indices
- •Cerebral Blood Flow
- •Cerebral Circulation Time
- •Cerebral Blood Volume
- •4 Pathogenesis of Stroke
- •Arterial Ischemia
- •Classification of Arterial Stroke
- •Microembolic Signals
- •Spontaneous Microemboli
- •Detection of Microemboli in Patent Foramen Ovale
- •Venous Ischemia
- •5 Vascular Pathology
- •Vessel Wall Pathology
- •Elongations
- •Intima-media Thickness
- •Atherosclerotic Plaques
- •Dissection
- •Fibromuscular Dysplasia
- •Vasculitis
- •Stenoses and Occlusions
- •Ultrasound Criteria of Stenoses
- •Ultrasound Criteria of Occlusions
- •Extracranial Pathology
- •Extracranial Anterior Circulation
- •Extracranial Posterior Circulation
- •Intracranial Pathology
- •Intracranial Anterior Circulation
- •Intracranial Posterior Circulation
- •Collateral Pathways
- •Intracranial Collateral Pathways
- •Intracranial Collateral Pathways in ICA Occlusive Processes
- •Intracranial Collateral Pathways in VA Occlusive Processes
- •Extracranial Collateral Pathways
- •Clinical Relevance of Collateral Pathways
- •6 Angiographic Techniques in Neuroradiology
- •Digital Subtraction Angiography
- •Historical Development
- •Technical Aspects
- •Strengths and Disadvantages
- •Magnetic Resonance Angiography
- •Historical Development
- •Technical Aspects
- •Strengths and Disadvantages
- •Computed Tomographic Angiography
- •Historical Development
- •Technical Aspects
- •Strengths and Disadvantages
- •Current Algorithm at the Charité University Hospital
- •Stroke
- •Intracranial Aneurysm
- •Vasculitis
- •Cerebral Venous Thrombosis
- •Peri-therapeutic Imaging
- •Initial Neurosonologic Findings
- •Conventional Angiography
- •Clinical Course
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Question to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 1)
- •Clinical Course
- •Neurosonologic Findings (Day 20)
- •Final Diagnosis
- •Discussion
- •Part B: Case Histories
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings
- •Clinical Course
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings
- •Conventional Angiography
- •Clinical Course
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 1)
- •Conventional Angiography (Day 2)
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 2)
- •Clinical Course
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Clinical Course (1)
- •Question to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings
- •Cerebral CT
- •Clinical Course (2)
- •Final Diagnosis
- •Discussion
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Clinical Course (1)
- •Question to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 42)
- •Neuroradiologic Findings
- •Clinical Course (2)
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 1)
- •Conventional Angiography (Day 2)
- •Clinical Course
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Clinical Course (1)
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings
- •Clinical Course (2)
- •Follow-up Neurosonologic Findings (1 Hour)
- •Clinical Course (3)
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 1)
- •Clinical Course (1)
- •Questions to Answer by Ultrasound Techniques
- •Follow-up Neurosonologic Findings (Day 2)
- •Clinical Course (2)
- •Follow-up Neurosonologic Findings (Day 7)
- •Clinical Course (3)
- •Follow-up Neurosonologic Findings (6 Months)
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings
- •Conventional Angiography
- •Clinical Course
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Question to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 1)
- •Clinical Course (1)
- •Conventional Angiography (Day 5)
- •Clinical Course (2)
- •Follow-up Neurosonologic Findings (5 Years)
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings
- •Clinical Course
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Initial Neurosonologic Findings
- •Conventional Angiography
- •Clinical Course (1)
- •Follow-up Neurosonologic Findings (2Months)
- •Clinical Course (2)
- •Follow-up Neurosonologic Findings (5Months)
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 1)
- •Clinical Course (1)
- •Follow-up Neurosonologic Findings (6 weeks)
- •Clinical Course (2)
- •Final Diagnosis
- •Discussion
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 1)
- •Conventional Angiography (Day 3)
- •Clinical Course
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings
- •Conventional Angiography
- •Clinical Course (1)
- •Follow-up Neurosonologic Findings (3 Months)
- •Clinical Course (2)
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings
- •Conventional Angiography
- •Clinical Course
- •Final Diagnosis
- •Discussion
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 1)
- •Evaluation of Collateral Function
- •Conventional Angiography
- •Clinical Course (1)
- •Follow-up Neurosonologic Findings (Day 20)
- •Clinical Course (2)
- •Final Diagnosis
- •Discussion
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Clinical Course (1)
- •Follow-up Neuroradiologic Findings (Day 3)
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 3)
- •Conventional Angiography (Day 4)
- •Clinical Course (2)
- •Final Diagnosis
- •Discussion
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 1)
- •Clinical Course (1)
- •Questions to Answer by Ultrasound Techniques
- •Neurosonologic Findings (Day 10)
- •Neuroradiologic Findings (Day 11)
- •Clinical Course (2)
- •Final Diagnosis
- •Discussion
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings
- •Conventional Angiography
- •Clinical Course (1)
- •Question to Answer by Ultrasound Techniques (6 Months)
- •Neurosonologic Findings (6 Months)
- •Clinical Course (2)
- •Questions to Answer by Ultrasound Techniques (8 Months)
- •Neurosonologic Findings (8 Months)
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Clinical Course (1)
- •MRI and MR Angiography (10:00 Hours)
- •Questions to Answer by Ultrasound Techniques
- •Neurosonologic Findings (12:00 Hours)
- •Conventional Angiography (16:00 Hours)
- •Clinical Course (2)
- •Questions to Answer by Ultrasound Techniques
- •Follow-up Neurosonologic Findings (6 Months)
- •Clinical Course (3)
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 2)
- •Conventional Angiography (Day 4)
- •Clinical Course (1)
- •Clinical Course (2) and Follow-up Neuroradiologic Findings
- •Follow-up Neurosonologic Findings (10 Months)
- •Clinical Course (3)
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Conventional Angiography
- •Clinical Course (1)
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 1)
- •Clinical Course
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings
- •Conventional Angiography
- •Clinical Course
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 1)
- •Conventional Angiography (Day 2)
- •Clinical Course (1)
- •Follow-up Neurosonologic Findings (4 Weeks)
- •Clinical Course (2)
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 1)
- •CT Angiography (CTA) (Day 1)
- •Clinical Course (1)
- •Question to Answer by Ultrasound Techniques
- •Follow-up Neurosonologic Findings (Day 90)
- •Question to Answer by Ultrasound Techniques
- •Follow-up Neurosonologic Findings (Day 180)
- •Clinical Course (2)
- •Final Diagnosis
- •Discussion
- •Clinical Presentation
- •Initial Neuroradiologic Findings (Day 1)
- •Suspected Diagnosis
- •Questions to Answer by Ultrasound Techniques
- •Initial Neurosonologic Findings (Day 20)
- •Conventional Angiography (Day 22)
- •Clinical Course (1)
- •Questions to Answer by Ultrasound Techniques
- •Follow-up Neurosonologic Findings (Day 29)
- •Follow-up Neurosonologic Findings (3 Months)
- •Final Diagnosis
- •Discussion
- •References
- •Index

Case 8 Bilateral Intracranial V4 Vertebral Artery Stenosis
166
creased flow velocities in both V4-VA segments, reaching a
peak systolic flow velocity of 175cm/s (insonation depth:
61 mm) on the left side and 169 cm/s (insonation depth:
67 mm) on the right. The BA had a normal flow pattern
(Figs.B8.8–B8.10).
Degree of Neurosonologic Difficulty: Low
Conclusion
Bilateral left-pronounced intracranial VA stenoses. Restenosis of the left VA after balloon dilatation. No evidence of
reocclusion or stenosis of the BA.
Fig. B8.1 DSA, left VA injection, posteroanterior view. Left VA-V4
stenosis (arrowhead) and BA occlusion starting at the midbasilar
region (arrow), (courtesy of Dr. Faiss, Asklepios FachklinikumTeupitz,
Teu pitz , Ge rman y).
Fig. B8.3 Unenhanced CT, axial plane. Circumscribed right cerebellar infarction within the SCA territory (arrow), (courtesy of Dr. Faiss,
Asklepios Fachklinikum Teupitz, Teupitz, Germany).
Fig. B8.2 DSA, left VA injection, posteroanterior view. Complete
recanalization of the BA after intraarterial thrombolysis. Diminished
left V4-VA stenosis after balloon dilatation (arrows), (courtesy of Dr.
Faiss, Asklepios Fachklinikum Teupitz, Teupitz, Germany).
Fig. B8.4 Extracranial duplex, longitudinal plane. Left V2-VA diameter: 4.5 mm.

Initial Neurosonologic Findings (Day 42)
167
Degree of Neurosonologic Difficulty: Low
Fig. B8.5 Extracranial duplex, longitudinal plane. Right V2-VA diam-
eter: 3.2 mm.
Fig. B8.7 Extracranial duplex, longitudinal plane. Doppler spectrum
analysis of the right V2-VA with mildly increased pulsatility (flow
velocity: 72/14 cm/s).
Fig. B8.6 Extracranial duplex, longitudinal plane. Doppler spectrum
analysis of the left V2-VA with increased pulsatility (flow velocity: 46/
11 cm/s). Note the mild retrograde flow component indicating relevant distal obstruction.
Fig. B8.8 TCCS (transforaminal approach). Turbulent and increased
flow in the left V4-VA (flow velocity: 175/79 cm/s).
Fig. B8.9 TCCS (transforaminal approach). Turbulent and increased
flow in the right V4-VA (flow velocity: 169/70 cm/s).
Fig. B8.10 TCCS (transforaminal approach). Normal flow in the BA.

Case 8 Bilateral Intracranial V4 Vertebral Artery Stenosis
168
Degree of Neurosonologic Difficulty: Low
Fig. B8.11 CTA, coronal MIP: 4 weeks after thrombolysis and left-
sided balloon dilatation: Persisting bilateral intracranial VA stenosis
with massive local calcification hindering graduation of stenoses
(arrowheads). Note that there is a signal loss in the right distal
V4-VA which is caused by an elongated vessel course and not by a
distal vessel occlusion.
Neuroradiologic Findings
MRIcouldnotbeperformedbecausethepatientexperienced severe claustrophobia. Cerebral CT did not show any
new ischemic lesion. CTA confirmed the bilateral intracranial VA stenoses with severe calcification in this area
(Fig. B8.11).
Clinical Course (2)
During the next few days the patient experienced further
recurrent episodes of vertigo and nausea which were
closely related to episodes of low blood pressure. Clopidogrel was added as a second antiplatelet agent and attempts were made to keep the blood pressure within the
upper normal range. Interventional treatment with stent
placement was discussed but refused by the patient. During 3 years of follow-up, no new ischemic event occurred
and the neurosonologic findings remained unchanged.
Final Diagnosis
Successful intraarterial thrombolysis in distal BA occlusion, probably caused by artery-to-artery embolism from
bilateral calcified intracranial VA stenoses. Suspected additional hemodynamic transient ischemic attacks (TIAs)
originating from the vertebrobasilar circulation.
Discussion
Clinical Aspects
Here we report of a 56-year-old man with bilateral intracranial VA stenoses. An artery-to-artery embolism originated from one of these stenoses and subsequently led to a
distal BA occlusion. Intraarterial thrombolysis was successfully performed and only a small right-sided cerebellar
infarct within the SCA territory remained. The case represents a special pathologic constellation within the vertebrobasilar territory because of the bilaterally affected V4VA segments.
According to reports of several stroke databases, ischemic events of the posterior circulation account for approximately 20 % of strokes (Bogousslavsky et al. 1988,
Moulin et al. 1997, Vemmos et al. 2000). The New England
Medical Center Posterior Circulation Registry is the largest
database comprising prospectively collected data of 407
patients (Caplan et al. 2004). Of these, 59 % had a stroke,
24 % TIA followed by stroke and 16 % sustained a TIA with
subsequent stroke. Ischemic strokes of the posterior circulation was caused by embolic events in 40 % of cases
when considering the single most likely mechanism. Of
these, 60 % were thought to be of cardioembolic origin.
Artery-to-artery embolic events originating from the posterior circulation accounted for 35 % and a mixed cause in
the remaining 5 % of cases. Large artery occlusive lesions
causing stroke (32 %), vessel branch occlusion (14 %), migraine (3 %) and others (10 %) were the next relevant
causes (Caplan et al. 2004).
Stenoses of the posterior circulation are predominantly
found at the VA origin followed by the BA and intracranial
VA. Within the intracranial VA they are most frequently
found in the distal segments, near the origin of the posterior inferior cerebellar artery (PICA). Bilateral stenoses, as
in our case, are not rare (Bogousslavsky et al. 1988, Caplan
1983, Muller-Kuppers et al. 1997). The New England Medical Center Posterior Circulation Registry reported clinical
and radiological findings of 42 patients (9.8 %) with bilateral intracranial VA involvement. Of these, 18 had bilateral
stenosis, eight had bilateral occlusion, and 16 had unilateral occlusion and contralateral stenosis. Only six patients
(14%) had isolated bilateral intracranial VA pathology. The
others presented in addition occlusive vascular lesions in
the BA (69 %), the extracranial VA (43 %), and also in the ICA
(26 %). Most of the stenoses were of atherothrombotic
origin (Shin et al. 1999).
In cases of chronic and slowly progressing occlusive
processes, patients with distal VA stenoses develop different collateral pathways. Collateralization may occur from
the anterior circulation via the posterior communicating
artery (PCoA) or the posterior circulation via the cerebellar
arteries, anterior spinal artery, and the leptomeningeal
arteries. However, often this is not sufficient, which may
lead to impaired perfusion in the dependent brain territories. Subsequently, patients present with recurrent ste-

Discussion
169
reotyped TIAs. Vertigo, dysarthria, ataxia, and double vision are the most frequent symptoms which may be
aggravated by orthostasis or antihypertensive therapy
(Caplan 1996). Shin and co-workers (1999) found 81 % of
patients in the group having TIAs had bilateral VA pathology; 38% of the TIAs were isolated events, and the remainderoccurredbeforeoraftermanifestationofstroke.In
most TIAs a hemodynamic cause was suspected (Shin et
al. 1999). As in our case, transient vertigo and ataxia were
the most frequently found clinical symptoms. The main
components of the vestibulocerebellar system, located in
the cerebellum and brain stem, derive their blood supply
from the distal VA via penetrating branches and the PICA
andarequicklyaffectedbyareducedorthogradeperfusion.
If a completed stroke occurs, the infarctpattern depends
on the site of the vascular pathology. Medullary infarctions
or infarcts of the PICA territory are observed if the stenotic
process is located proximal to, or directly at the origin of
the PICA. Ischemia within the BA, SCA, and posterior cerebral artery (PCA) territory occur more often in stenotic
processes distal to the PICA branch. Artery-to-artery embolic events from atheromatous plaques located in the
intracranial VA may also result in distal patterns of infarction. In our patient, a VA-derived thrombus caused a distal
BA occlusion with clinically fluctuating signs of a “top-ofthe-basilar-syndrome” (Caplan 1980, Mehler 1989). In
cases of persisting occlusion this may lead to ischemic
infarctions in upper pons, midbrain, cerebellum within
the SCA territory, thalamus, and the PCA territory. However, the extent may vary, as in our patient who only had a
partial SCA infarction. From this we can assume that
although the occlusion began at the mid-basilar level, it
must have extended to the head of the BA. We can also
conclude that our patient’sclinicalsymptomswereindicative of distal BA involvement, as they were mainly comprised of a mesencephalic dysfunction (transient third
nerve palsy and fluctuation in consciousness). Because of
the fluctuating symptoms, lack of ischemic signs on cerebral CT, and verification of the BA occlusion by DSA, an
intracranial thrombolysis was performed which led to
complete recanalization 6 hours after the onset of his
symptoms. Furthermore, balloon dilatation of the left
high-grade VA stenosis was performed.
In general, the therapeutic options in thromboembolic
occlusionsoftheBAaresimilartothoseintheanterior
circulation. However, only case series addressing treatment of acute BA occlusion have so far been published;
there are no randomized trials. Based on the results of the
NINDS trial (The NINDS rt-PA Stroke Study Group 1995)
some data exist about the intravenous application of
thrombolytic substances in patients with vertebrobasilar
occlusion within a 3 hour margin (Grond et al. 1998) within
the first 7 hours (Montavont et al. 2004) and even up to 12
hours for patients with sudden disturbance of consciousness and tetraparesis and up to 48 hours for patients with
gradually increasing brain stem symptoms (Lindsberg et al
2004). In this larger series including 43 patients with a BA
occlusion receiving systemic rt-PA thrombolysis, 52 %
demonstrated a BA recanalization. The mortality after 3
months was 40 %, and 22 % of patients achieved a good
clinical outcome, being independent in all functions of
daily life (Lindsberg et al. 2004). Improved recanalization
rates and clinical outcomes were also reported for intraarterial thrombolysis when compared with medical therapy with an antiplatelet agent. Intraarterial thrombolysis
is to date the most accepted therapy in BA occlusion. A
recent metaanalysis compared the results of intravenous
and intraarterial thrombolysis within the posterior circulation. It demonstrated that recanalization rates were significantly better if intraarterial thrombolysis was used
instead of intravenous thrombolysis (65 % vs. 53 %). However, survival rates and clinical outcome did not differ
significantly in the two groups (45 % vs. 50 %), but both
groups had a similar proportion of good clinical outcome
(24 % vs. 22 %) (Lindsberg and Mattle 2006). Independently
of the applied treatment strategy, the proportion of patients with a good clinical outcome was higher if recanalization occurred (38 % vs. 2 %). Contrary to the anterior
circulation, no clear time window for thrombolysis in the
posterior circulation has been established. In patients with
a stuttering course and no early infarct signs, the time
window for intraarterial and systemic thrombolysis may
be extended at least to up to 48 hours after onset of
symptoms (Lindsberg and Mattle 2006).
In addition to the above-mentioned treatment regimens, a new combination of therapies, “bridging therapy,” has been proposed for the posterior circulation. Eckert and coworkers demonstrated that the combination of
intraarterial rt-PA, intravenous abciximab, and, if applicable, a balloon dilatation or stent, placement in 47 patients,
led to similar recanalization rates (72 % vs. 68 %), a better
clinical outcome (34 % vs. 17 %) and a significant lower
mortality (38 % vs. 68 %) than with intravenous rt-PA alone
(Eckertetal.2005).
In our patient balloon dilatation was performed in the
left intracranial VA. A restenosis of the dilated vessel occurred. Restenosis has been reported in approximately
one-third of cases after intracranial stenting (Jiang et al.
2007, SSYLVIA Study Investigators 2004). Stenting seems
nottobesuperiortoballoondilatationwithrespectto
restenosis rates, but stroke rates at follow-up might be
lower after stenting procedures (Eberhardt et al. 2006)
(for further information on intracranial stenting, see also
Case 5, p.149).
Angiologic and Anatomic Aspects
In our case, the transcranial color-coded sonography
(TCCS) assessment of both intracranial V4-VA stenoses
was uncomplicated. The cut-off for a 100 % confident detection of a ≥ 50 % stenosis is ≥ 120 cm/s (Baumgartner et al.
1999). Both VAs in our patient revealed systolic flow velocities of around 170–180cm/s, well above these cut-off
Degree of Neurosonologic Difficulty: Low

Case 8 Bilateral Intracranial V4 Vertebral Artery Stenosis
170
values. There are no published data for a more detailed
grading. In ultrasound examination, a flow profile analysis
of pre- and poststenotic vessel segments can give valuable
additional information. The extracranial VA profiles in our
patient revealed a left-pronounced increased pulsatility,
ontheleftsidewithasmallretrogradeflowcomponent.
The BA itself did not show an obvious poststenotic flow
pattern. Taking this information into account, a stenosis of
beginning hemodynamic relevance, approximately of 80 %
withintheleftV4-VAsegmentandof70%intherightV4VA segment, can be assumed. Ultrasound assessment of
the intracranial VA segment may be limited in uncooper-
Degree of Neurosonologic Difficulty: Low
ative patients or those with a large neck circumference.
Furthermore, V4-VA segment elongations, frequently
found in the elderly might hinder an unequivocal vessel
identification and lead to confusion between VA and, for
example, a prominent PICA. In contrast with the extracranial ICA insonation, calcified plaques seem not to hinder
flow signal detection. This is probably due to the lower
insonation frequencies used for transforaminal insonation
and also to a lesser extent of VA of calcification. If VA
evaluation is difficult, in the acute posterior stroke setting
it is important to avoid delays and proceed to the next step
of neuroradiologic examination, for example, a CTA or
MRA.
However, analysis of the intracranial VA and the transitional segment between V3 and V4 may also prove difficult
with both techniques. As seen in our patient, a distinct and
long circumferential calcification can hinder CTA to assess
a V4-VA stenosis. In such cases, the detailed analysis of the
axial source images or a combined approach with MRA can
be helpful (Hirai et al. 2002). Analysis of the time-of-flight
(TOF)MRAtechniqueincomparisonwithDSAbytwo
readers has demonstrated a lower sensitivity and specificity in detection of intracranialVA stenoses (84 and 93 %; 74
and82%)comparedwithextracranialocclusiveVAprocesses (92 and 96 %; 100 and 90 %). TOF MRA accurately
diagnosed only 43 % of intracranial and 75 % of extracranial
VA stenosis (Bhadelia et al. 2001). Because of the increasing availability of fast gradient MR systems, the TOF MRA is
gradually being substituted by contrast-enhanced MRA
techniques which display better image contrast, require
less time, and are therefore less susceptible to movement
artifacts (Ersoy et al. 2003). Compared with the analysis of
the carotid arteries, contrast-enhanced MRA, however, is
less sensitive and specific in detecting steno-occlusive
processes of the vertebrobasilar circulation (Yang et al.
2005). In equivocal or conflicting situations catheter angiography may be required (for further information on
assessment of intracranial stenoses, see also Case 5, p. 149).

Case 9
Moyamoya Disease with Bilateral Carotid-T Stenosis
171
Clinical Presentation
A 34-year-old Caucasian woman presented after three
separate episodes of transient left-sided brachiofacial
hemiparesis within the last 4 weeks, each lasting a few
minutes. Since the birth of her first child 4 years previously, she had suffered from a pregnancy-induced hypertension. No further vascular risk factors were present.
Initially she was admitted to a district general hospital.
Transient ischemic attacks (TIAs) were suspected, and a
cranial magnetic resonance (MR) scan and an MR angiogram were performed revealing bilateral middle cerebral
artery (MCA) stenosis more pronounced on the right side.
The patient was started on antiplatelet treatment with
aspirin and dipyridamole and was referred to our department for further evaluation.
Initial Neuroradiologic Findings
The externally performed MRI did not show ischemic brain
lesions (not shown). Intracranial time-of-flight (TOF) MRA,
however, was suspicious of bilateral proximal MCA and
anterior cerebral artery (ACA) stenoses with a right-sided
accentuation (Fig. B9.1).
Initial Neurosonologic Findings (Day 1)
Extracranial Duplex Sonography
B-mode and color-mode imaging revealed no atherosclerotic vascular changes. Doppler spectrum analysis showed
normal and symmetric flow signals. Assessment of the
vertebral arteries (VAs) was also normal.
Transcranial Duplex Sonography
A mildly elevated flow velocity was seen in the right distal
internal carotid artery (ICA) reaching 160 cm/s. Both M1MCA segments were markedly affected reaching a peak
systolic flow of 380 cm/s on the right side and 210cm/s on
the left side. The right M2-MCA segments presented a
poststenotic flow pattern. Flow in the right A1-ACA segment demonstrated normal velocities but with a clearly
reduced pulsatility, probably indicating an additional collateral flow toward the MCA territory. The left A1-ACA
segment presented elevated flow velocities reaching
175 cm/s peak systolic flow without turbulence, corresponding to either a low-grade ACA stenosis or collateral
flow. Normal flow velocities were detected in both posterior cerebral arteries (PCAs) (Figs. B9.2–B9.8).
Suspected Diagnosis
Recurrent left-sided TIAs in bilateral high-grade proximal
MCA and ACA stenoses of unknown origin.
Questions to Answer by Ultrasound Techniques
• Was there any evidence of pathologic vascular changes
in the cervical vessels?
• What was the grading of the intracranial stenoses?
• Were there any other intracranial stenotic processes or
collateral blood flow?
Conclusion
Bilateral carotid-T pathology with right high-grade M1MCA stenosis and moderate M1-MCA stenosis on the left
side. Moderate stenosis of the right terminal ICA. Indirect
signs of partial leptomeningeal collateralization via both
A1-ACA segments and possible additional low-grade A1ACA stenosis.
Conventional Angiography (Day 2)
Selective right ICA contrast filling demonstrated a moderate stenosis of the terminal ICA continuing into a long
segmental high-grade M1-MCA stenosis. Furthermore, a
network of small capillary collateral vessels was visible in
the region of the distal ICA and proximal MCA. The distal
branches of the right MCA showed regular contrast. The
proximal A1-ACA segment demonstrated moderate stenosis. Selective left ICA filling yielded a mild caliber reduction
from the distal ICA to the M1-MCA segment and to a lesser

Case 9 Moyamoya Disease with Bilateral Carotid-T Stenosis
172
Degree of Neurosonologic Difficulty: Low
Fig. B9.1 Intracranial 3D TOF MRA, coronal MIP. Bilateral stenosis of
the MCA and ACA at their respective origins with a right-sided
accentuation (arrows).
Fig. B9.3 TCCS (transtemporal approach), right-sided insonation,
midbrain plane. Distinct flow increase in the right M1-MCA (flow
velocity: 379/220 cm/s).
Fig. B9.2 TCCS (transtemporal approach), right-sided insonation,
upper pontine plane. Moderately increased flow in the right C2ICA (flow velocity: 160/90 cm/s).
Fig. B9.4 TCCS (transtemporal approach), right-sided insonation,
midbrain plane. Poststenotic flow pattern in the right M2-MCA.
Fig. B9.5 TCCS (transtemporal approach), right-sided insonation,
midbrain plane. The right A1-ACA shows a reduced pulsatility due
to an increased diastolic flow (flow velocity: 95/63 cm/s).
Fig. B9.6 TCCS (transtemporal approach), left-sided insonation,
midbrain plane. Raised flow velocity in the left M1-MCA (peak
systolic flow velocity: 212 cm/s).

Discussion
173
Degree of Neurosonologic Difficulty: Low
Fig. B9.7 TCCS (transtemporal approach), left-sided insonation,
midbrain plane. Normal flow in a left M2-MCA.
extent in the A1-ACA segment. Again, a network of small
vessels indicating collateral pathways was seen. The posterior circulation was normal (Fig. B9.9).
Clinical Course
The finding of bilateral stenotic carotid-T processes including both MCAs, ACAs, and in part the distal ICAs as well as
small-caliber collateral pathways were suggestive of the
diagnosis of a yet indistinct moyamoya disease.The absent
vascular risk factors and the normal status of extracranial
vessels further supported this diagnosis. As the patient
complained of a daily, dull headache, her medication was
changed from dipyridamole plus aspirin to aspirin alone.
The headaches disappeared and no further ischemic
events occurred. The patient was referred to the department of neurosurgery to evaluate the possibility of an
extra-intracranial vascular bypass. Thereafter she was
lost to follow-up.
Fig. B9.8 TCCS (transtemporal approach), left-sided insonation,
midbrain plane. Increased but not turbulent flow in the left A1ACA (peak systolic flow velocity: 175 cm/s).
Fig. B9.9 DSA, superimposed right and left selective ICA injection,
posteroanterior view. Right-sided moderate terminal ICA stenosis
continuing into a proximal high-grade M1-MCA and moderate A1ACA stenosis. Note the poststenotic dilatation of the distal M1-MCA
and the M2-MCA branches. Similar but milder stenoses are seen on
the left side. Bilateral networks of small vessels within the region of
the distal ICA and proximal MCA.
Final Diagnosis
Recurrent TIAs, presumably of hemodynamic origin in the
right MCA territory caused by bilateral right-pronounced
high-grade carotid-T stenoses on the basis of presumed
moyamoya disease.
Discussion
Clinical Aspects
Here we discuss a 34-year-old Caucasian woman who
presented with bilateral intracranial stenotic processes
within the distal ICA as well as the proximal MCA and
ACA. Apart from mild hypertension, no classic vascular
risk factors were present. Correspondingly, no atheroscle-
rotic lesions were found in the extracranial arteries. Age
and location of the stenotic processes were suggestive of
rare causes of ischemic stroke. Based on the angiographic
finding of bilateral intracranial ICA stenoses, additional
involvement of circle of Willis (CW) arteries and the typical formation of small collateral vessels, moyamoya disease was considered.
Moyamoya disease was first described by Takeuchi and
Shimizu in 1957 and is predominantly found in Japan. The
annual incidence is 0.35% per 100 000 inhabitants (Fukui
and Kawano 1996). Precise epidemiological data for Europe and North America are not available. Until 1996 the
total number of reported moyamoya cases was 239 in
North America (Chiu et al. 1998). Within the Asian and,
in particular, within the Japanese population the incidence

Case 9 Moyamoya Disease with Bilateral Carotid-T Stenosis
174
is tenfold higher than in Europe or in North America (Yonekawa 1997). Generally young women seem to be more
frequently affected than men. A clustering within families
is seen in up to 10% of affected patients. The disease may
manifest at any age. However, there are peaks in presentation in those aged < 10 years and between 30 and 40
years.
Inthecourseofthedisease,thereisaslow,spontaneous,
and progressive development of stenoses in the CW. Generally the affected vessels are the ICA, MCA, and ACA.
Concomitantly, a network of intracerebral and extracerebral collaterals can be found. The collaterals in the region
Degree of Neurosonologic Difficulty: Low
of the CW appear in DSA imaging as fog or smokelike
structures, which give the disease its name (moyamoya
is Japanese for smoke or fog).
Macroanatomically, a stenosed or occluded vessel lumen is found in the affected arteries caused by an intimal
thickening of the vessel. On histologic examination, mural
thrombi are frequently found with the stenosed regions,
which are thought to be responsible for the eccentric
reductionofthevessellumen(Hosodaetal.1997).However, until now the exact cause of the disease remains
unclear despite continuing effort. The predominance
among the Asian population and the reported inheritance
in some families argue in favour of a multifactorial, hereditary etiology.
Clinically moyamoya frequently manifests itself by reoccurring TIAs. Atypical reported symptoms are chronic
headaches and focal or generalized epileptic seizures. In
Asia an increased incidence of intracranial bleeding has
been reported as a further first manifestation of moyamoya in the adult population, whereas TIAs prevail in
the juvenile form. In Europe this difference between age
groups does not seem to exist. In our presented patient,
age, gender, and the clinical presentation with supposedly
hemodynamic TIAs corresponded well with the suspected
diagnosis of moyamoya disease.
As moyamoya is a rare disease of unknown etiology, a
number of focal and systemic diseases have tobe excluded,
including chronic meningitis or atherosclerotic vascular
disease. In some middle-aged patients, the latter may lead
to a picture similar tothe moyamoyafindings. This group of
patients, however, demonstrates additional macroangiopathic changes in the extracranial brain-supplying arteries
(Hinshaw et al. 1976). As the foglike collateral network can
also be foundin these patients, it hasto be interpreted asan
unspecific compensatory reaction to a slowly progressing
stenotic process. Finally, radiation may also cause moyamoya-like vascular changes as a side effect.
To date, there is no medical treatment to stop or delay
the disease progression although antiplatelet agents and
anticoagulation are frequently used. The only effective
treatment is surgical revascularization of the malperfused
brain regions. Several surgical techniques are used. The
most common is direct revascularization with an extracranial–intracranial (EC–IC) bypass between the superficial
temporal artery and a cortical MCA branch (STA–MCA
bypass) (for further information on EC–IC bypass, see
Case 25, p.297). An indirect form of revascularization is
the placement of the STA on the dura, muscle, or pia
(encephaloduroarteriosynangiosis, encephalomyosynangiosis, or pial synangiosis). All approaches improve the
perfusion of the poststenotic brain regions and are able
to minimize or even to stop clinical events. The indirect
approach is more frequently applied in children and the
direct approach in adults.
Angiologic and Anatomic Aspects
Diagnosis of moyamoya is based on morphological vascular aspects depicted by the angiologic imaging methods.
An additional diagnostic criterion is the bilateral occurrence of stenotic processes. Bilateral involvement confirms
the suspected diagnosis; in unilateral cases, a possible
moyamoya has to be postulated.
First-line techniques are the noninvasive CT and CTA as
well as MRI and MRA. In suspected cases, these are followed by DSA. Conventional CT findings are variable and
often unspecific. They range from mild brain atrophy with
frontal accentuation to multiple hypodense ischemic areas
within the regions of the vascular border zones. Although
rare, even a subarachnoid hemorrhage can occur. If contrast CT is performed, the lenticulostriatal collateral network might be seen. MRI is more sensitive in identifying
ischemic lesions if diffusion and perfusion sequences are
applied. These techniques are helpful in representing the
regionsatriskaswellasconfirmingthepostoperative
perfusion improvements. The described typical collateral
vessels can sometimes be seen in the form of flow artifacts
(“flow void” phenomenon). On post contrast sequences, a
leptomeningeal enhancement (“ivy sign”)mightbeobserved which is caused by multiple fine leptomeningeal
anastomoses (Ohta et al. 1995). MRA is able to detect
collateral vessels at the basal skull level in cases with
advanced disease. The overall diagnostic sensitivity of
MRAincomparisontoDSAis73%andthespecificityis
100 % (Yamada et al. 1995). There have been no systematic
analyses of CTA results.
For final confirmation of moyamoya, DSA is required,
which should at the latest be performed before planning
an intervention. The technique shows stenoses or occlusions of the distal intracranial ICA and the proximal MCA
and/or ACA in addition to the collateral vascular network
adjacent to the stenotic process (see also chapter 6,
Fig. 7C). An angiographically determined definition of six
stages of the disease has been reported by Suzuki and
Takaku (1969). The chronologic stages of the disease are:
I. Narrowing of the carotid siphon.
II. Initiation.
III. Intensification.
IV. Minimization.
V. Reduction.
VI. Disappearance of moyamoya vessels.

Discussion
175
Our patient’s findings correspond with stage II (early dis-
ease)—demonstrating carotid-T stenoses, the fine collateral network, and a poststenotic dilatation of the distal
intracranial arteries.
Doppler and duplex ultrasound may also contribute
important diagnostic information in patients with moyamoya disease. TCCS permits identification and quantification of intracranial stenosis. More importantly, ultrasound
allows the evaluation of collateral pathways. For example,
raised flow velocities in the P1- and P2-PCA segments
seldom affected in moyamoya disease are indirect indicators of leptomeningeal collateralization in cases with affected proximal MCA. As the A1-ACA segments can be
affected by the disease, it may be impossible, as it was in
our case, to sonographically differentiate between compensatory collateral flow and raised flow velocity caused
by a stenosis. The same is true for the criterion of turbulent
flow, as turbulence is not pathognomonic for a stenosis
and can frequently occur in regions with tortuous vessels
even without the presence of a stenosis. Other indirect
sonographic signs of collateral involvement are a reduced
pulsatility as a result of a peripheral vascular dilatation.
A number of recent ultrasound studies have systematically analyzed flow patterns in moyamoya disease. These
studies have found reduced flow velocities and raised
pulsatility indices in the extracranial CCA and ICA which
frequently revealed a narrowed lumen. Intracranially, the
aforementioned multilocular stenoses can be detected.
Furthermore, low flow velocities with low pulsatility
(due to low resistance) can be detected within the distal,
poststenotic basal cerebral arteries, which in the case of a
severe flow alteration, might appear occluded on catheter
angiography (Muttaqin et al. 1993, Ruan et al. 2006). Finally, the small fine moyamoya collaterals can be depicted
as scattered colored dots in about half of cases, comprising
low flow velocities and reduced pulsatility indices on
Doppler spectrum analysis (Ruan et al. 2006). In our presumed case of early-stage moyamoya disease, these signals were not found.
Degree of Neurosonologic Difficulty: Low
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