Diagnostic Ultrasonography in Neurology.15

REVIEW ARTICLE
Diagnostic
Ultrasonography in

C O N T I N UU M A UD I O
I NT E R V I E W A V AI L A B L E
Neurology
ONLINE

VIDEO CONTENT
A VA I L A B L E O N L I N E By Elsa Azevedo, MD, PhD
ABSTRACT
OBJECTIVE: Ultrasonography allows neurologists to complement clinical
information with additional useful, easily acquired, real-time data. This
article highlights its clinical applications in neurology.
LATEST DEVELOPMENTS: Diagnostic ultrasonography is expanding its

applications with smaller and better devices. Most indications in neurology
relate to cerebrovascular evaluations. Ultrasonography contributes to
the etiologic evaluation and is helpful for hemodynamic diagnosis of
brain or eye ischemia. It can accurately characterize cervical vascular
atherosclerosis, dissection, vasculitis, or other rarer disorders.
Ultrasonography can aid in the diagnosis of intracranial large vessel
stenosis or occlusion and evaluation of collateral pathways and indirect
hemodynamic signs of more proximal and distal pathology. Transcranial
Doppler (TCD) is the most sensitive method for detecting paradoxical
emboli from a systemic right-left shunt such as a patent foramen ovale.
TCD is mandatory for sickle cell disease surveillance, guiding the timing
CITE AS:
for preventive transfusion. In subarachnoid hemorrhage, TCD is useful
CONTINUUM (MINNEAP MINN) in monitoring vasospasm and adapting treatment. Some arteriovenous
2023;29(1, NEUROIMAGING):
shunts can be detected by ultrasonography. Cerebral vasoregulation
3 24 – 3 63 .
studies are another developing field of interest. TCD enables monitoring
Address correspondence to of hemodynamic changes related to intracranial hypertension and can
Dr Elsa Azevedo, Department of diagnose cerebral circulatory arrest. Optic nerve sheath measurement
Neurology, Centro Hospitalar
Universitário de São João,
and brain midline deviation are ultrasonography-detectable signs of
Alameda Professor Hernani intracranial hypertension. Most importantly, ultrasonography allows for
Monteiro, 4200-319 Porto, easily repeated monitoring of evolving clinical conditions or during and
Portugal, elsa.azevedo@chsj.
min-saude.pt. after interventions.
RELATIONSHIP DISCLOSURE :
Diagnostic ultrasonography is an invaluable tool in
ESSENTIAL POINTS:
Dr Azevedo reports no
disclosure. neurology, used as an extension of the clinical examination. It helps
diagnose and monitor many conditions, allowing for more data-driven and
UNLABELED USE OF
PRODUCTS/INVESTIGATIONAL
rapid treatment interventions.
USE DISCLOSURE:
Dr Azevedo reports no
disclosure.
© 2023 American Academy

of Neurology.
324 FEBRUARY 2023
Copyright © American Academy of Neurology. Unauthorized reproduction of this article is prohibited.

KEY POINTS
INTRODUCTION
U
ltrasonography in neurology, or neurosonology, is the medical science ● Neurosonology can be
dedicated to the use of ultrasonography for the study of the used as an extension of the
nervous system. clinical neurologic
examination.
Neurosonology is a technique used by physicians as an extension of
the clinical examination. It is commonly used for the evaluation of ● Advantages of
cerebrovascular diseases, where it establishes the diagnosis or provides neurosonology are that it
complementary hemodynamic information to computed tomography can be performed at the
angiography (CTA) or magnetic resonance angiography (MRA). It is also used in bedside, is noninvasive,
provides real-time accurate
several other applications, such as in the study of the peripheral nervous system, information, and allows
and guides neurointerventional procedures (such as echo-guided injection of continuous monitoring.
botulinum toxin or lumbar puncture).
The main advantages of this tool are related to its (1) being performed at the ● An ultrasound machine
that provides B-mode
patient’s bedside, if appropriate, avoiding travel when patients are unstable; echography, color imaging
(2) giving real-time information, allowing immediate clinical action; (3) being of the vessels, and blood
noninvasive, with no ionizing radiation, with no sedation needed even for flow velocities spectrum
children or some agitated patients, not being influenced by central nervous allows extracranial and
many intracranial
system depressants, and having no iodinated contrast exposure or contrast
applications, including
side-effects; (4) being easily repeated to monitor changes and allowing vascular and parenchymal
monitoring during therapeutic and other interventions; (5) being a studies.
comparatively inexpensive method; (6) allowing the neurologist to
demonstrate changes to the patient during the procedure; and (7) most
importantly, giving accurate and validated information. As practice and
hands-on experience with a device offer the best instruction, an interesting
feature of ultrasonography is that the beginner can learn the first steps by
evaluating their own vessels and other structures. As with other techniques, it
requires an experienced operator.
For intracranial studies, one main limitation is the intact skull that prevents a
good ultrasound window in about 10% to 20% of patients, particularly in older
women, although for vascular studies this can be overcome by echo contrast agents.
GENERAL TECHNICAL REQUIREMENTS FOR NEUROSONOLOGY

Two main devices are used in neurosonology. First are ultrasound machines that
provide at least three pieces of information: B-mode echography, color imaging
of the vessels, and blood flow velocities spectrum. B-mode (brightness mode)
generates an echographic grayscale image. A superimposed color-Doppler mode
shows the blood flow direction and its velocity, through the Doppler effect,
which is the frequency difference of the transmitted and reflected ultrasound
proportional to the velocity of moving erythrocytes. Power-Doppler mode uses
the signal intensity of the returning Doppler signal instead of frequency shift,
providing a color map superimposed on a B-mode image. Spectral analysis shows
the graphic distribution of direction and velocities in moving erythrocytes over
time. Some indices are very useful in clinical practice, such as the resistance
(systolic flow velocity minus the diastolic velocity divided by the systolic
velocity) and the pulsatility (systolic flow velocity minus the diastolic velocity
divided by the mean velocity) indices, which give clues about upstream and
downstream pathology. This device is used for extracranial and many intracranial
applications, such as extracranial color Doppler sonography and transcranial color
sonography, and for parenchymal studies.
CONTINUUMJOURNAL.COM 325

DIAGNOSTIC ULTRASONOGRAPHY IN NEUROLOGY
TABLE 12-1 Main Applications of Neurosonology
Settings
◆ Prediction of vascular risk in primary prevention (atherosclerosis, sickle cell disease)
◆ Acute ischemic stroke and eye ischemic syndrome (etiology, hemodynamic monitoring)
◆ Monitoring of vasospasm in subarachnoid hemorrhage
◆ Monitoring during and after cerebrovascular interventions
◆ Neurocritical care monitoring
◆ Suspicion of temporal arteritis or dural fistula
◆ Brain parenchyma studies in neonatal pathology and in some movement disorders
◆ Eye pathology
◆ Neuromuscular diseases
Extracranial
◆ Neck vessel atherosclerotic disease (intima-media thickness, atherosclerotic plaques)
◆ Arterial dissection, fibromuscular dysplasia
◆ Cervical and temporal arteritis
◆ Transient perivascular inflammation of the carotid artery syndrome
◆ Isolated thrombus
◆ Signs of arteriovenous shunts (eg, dural fistula)
◆ Subclavian steal phenomenon
◆ Other indirect hemodynamic signs of upstream (eg, aortic valvular disease, proximal
stenosis) and downstream (eg, distal occlusion) lesions
◆ Neuromuscular diseases
◆ Echo-guided interventions (botulinum toxin, lumbar puncture)
Intracranial
◆ Intracranial arterial stenosis and occlusions (atherosclerosis, arteritis, embolus)
◆ Cerebral hemodynamics in sickle cell disease
◆ Intracranial impact of extracranial disease collateralization pathways (circle of Willis,
ophthalmic artery, inversion of vertebral flow direction)
◆ Microembolic signal detection
◆ Right-to-left shunt assessment (eg, patent foramen ovale, arteriovenous pulmonary fistula)
◆ Cerebral vasospasm in subarachnoid hemorrhage
◆ Reversible cerebral vasoconstriction syndrome
◆ Hemodynamic monitoring during and after interventions
◆ Cerebral vasoreactivity, autoregulation, and neurovascular coupling studies
◆ Intracranial hypertension and brain death
◆ Venous studies
◆ Eye (vascular or optic nerve pathology)
◆ Brain parenchyma studies, such as in neonatal pathology and in some movement disorders
326 FEBRUARY 2023

A second device is the transcranial Doppler (TCD) device examining only KEY POINTS
the Doppler effect through its spectral analysis. It does not provide
● A transcranial Doppler
echo-imaging information (“blind” TCD). Nevertheless, this smaller device, device providing only
with smaller probes, is very useful for the evaluation of hemodynamics Doppler spectral analysis is
because it allows hands-free and bilateral monitoring of cerebral hemodynamics a smaller device that allows
with a headframe. hands-free and bilateral
monitoring of cerebral
Pulsed-waved linear-array probes of approximately 5 MHz to 13 MHz are used
hemodynamics with a
for evaluating the cervical vessels. Probes of at least 15 MHz to 20 MHz are used headframe.
for more superficial vessels, such as the temporal arteries. Because intracranial
vessels are deeper, lower frequencies are needed, so for transcranial ● Atherosclerosis, sickle
examinations, 1.5-MHz to 3.5-MHz probes are used. cell disease, brain and eye
ischemia, subarachnoid
The cervical vessels (the common, internal, and external carotids and hemorrhage, suspicion of
vertebral arteries) are usually examined with the patient in a supine position, temporal arteritis or dural
neck slightly extended and laterally rotated. The intracranial structures are fistulas, intracranial
approached through three main windows: orbital (for ophthalmic artery, carotid hypertension, and cerebral
circulatory arrest are some
siphon, and optical nerve), temporal (for distal internal carotid; middle, anterior, of the settings for
and posterior cerebral arteries; and brain parenchyma), and occipital (for neurovascular
intracranial segments of vertebral arteries and the basilar artery). When the skull ultrasonography.
does not have good windows for ultrasonography, clinicians can use commercial
IV transpulmonary ultrasound contrast agents that improve the detection of flow
in intracranial vessels.
MAIN APPLICATIONS OF NEUROSONOLOGY

After clinical history and neurologic examination, neurosonology allows the
physician to look further right away, inside the patient. TABLE 12-1 lists the main
applications of neurosonology.
This article discusses neurovascular ultrasonography as the main
application of neurosonology. In primary prevention, it predicts vascular risk
(eg, atherosclerosis, sickle cell disease). In the setting of brain or eye ischemia, it
contributes to etiologic and hemodynamic diagnosis, which is useful in
hyperacute phase monitoring and for secondary prevention. The temporal
arteries can also be rapidly evaluated by ultrasonography. In subarachnoid
hemorrhage, TCD allows for monitoring of vasospasm, guiding treatment
options. Some arteriovenous shunts, such as dural arteriovenous fistulas in
patients with pulsatile tinnitus, are easily perceived by hemodynamic features
in ultrasonography. In neurocritical care, TCD enables monitoring of
hemodynamic changes associated with intracranial hypertension and can
diagnose cerebral circulatory arrest with high accuracy. Optic nerve sheath
measurement and brain midline deviation are other ultrasonography-
detectable signs of intracranial hypertension. Neurosonology allows for
easily repeated monitoring of clinical conditions or during and after
interventions.
Brain parenchyma may also be studied with ultrasonography, as in neonatal
pathology and potentially in movement disorders. Additionally, ultrasonography
allows for guidance of peripheral neurointervention procedures and the study of
the peripheral nervous system.1
New trends, such as ultraportable devices, ultrafast-ultrasonography,
ultrasound perfusion imaging, cerebral hemodynamic and vasoregulation studies
applied to guiding decisions, and the concept of point-of-care ultrasonography
for neurology, are other developing fields of interest.

KEY POINTS NEUROVASCULAR ULTRASONOGRAPHY

Ultrasonography can be thought of as a brain stethoscope providing insight
● A comprehensive
cerebrovascular
into cerebrovascular hemodynamics.
ultrasonographic evaluation A comprehensive cerebrovascular evaluation includes cervical as well as
should include cervical as intracranial vessels (FIGURE 12-1), both morphologic and hemodynamic features
well as intracranial vessels. at the cervical level, and hemodynamics concerning the intracranial vessels.
With this approach, neurosonology can help answer important clinical questions
● The degree of stenosis of
a cervical internal carotid in acute stroke settings, from etiology to monitoring in several steps, as listed
atherosclerotic plaque can in TABLE 12-2.
be measured by direct
morphologic and Extracranial Neurovascular Ultrasonography
velocimetric parameters, as
At the cervical level, it is possible to accurately assess morphologic changes of
well as by indirect criteria.
carotid and vertebral arteries, along with their hemodynamic
● Compensatory functional performance.
intracranial collateral
circuits (ophthalmic, ATHEROSCLEROTIC DISEASE. Cervical vascular ultrasonography is useful for
anterior communicating, and
posterior communicating
diagnosing atherosclerotic disease, measuring intima-media thickness, as a
arteries) provide indirect systemic marker of atherosclerosis, and atherosclerotic plaque characterization
signs of the hemodynamic and its hemodynamic effects. TABLE 12-3 reviews the criteria for defining the
effect of a cervical carotid degree of stenosis of a cervical internal carotid atherosclerotic plaque, most
stenosis.
frequently occurring in the carotid bulb.2 Other similar criteria have been
published,3 but all are essentially based on the morphologic assessment of the
degree of luminal stenosis, which can be measured by methods used in
angiographic studies such as NASCET (the North American Symptomatic
FIGURE 12-1
Normal cervical and brain vessels. A, Bifurcation of common (ACC) into external (ACE) and
internal (ACI) carotid arteries. B, Vertebral artery (V1) starting at the subclavian artery. C,
Transcranial temporal window: right and left segments of middle (M1, M2), anterior (A1, A2),
and posterior (P1) cerebral arteries. D, Transcranial occipital window: intracranial vertebral
(V4) and basilar arteries.
328 FEBRUARY 2023

Carotid Endarterectomy Trial) and ECST (the European Carotid Surgery Trial)
(FIGURE 12-2),4 complemented by hemodynamic assessment. Hemodynamics
are assessed by the blood flow velocity at the most stenotic point, comparison
with proximal and more distal segments, and the appreciation of possible
intracranial compensatory collateral circuits (ophthalmic, anterior
communicating, and posterior communicating arteries), which provide indirect
signs of the hemodynamic effect of the stenosis.
The following should be considered for carotid stenosis evaluation: (1) if a
good visualization of the stenotic channel is possible, morphologic criteria can be
prioritized, although hemodynamics should also be evaluated; (2) if visualization
of the stenotic channel is difficult, the velocimetric direct and indirect criteria
should be prioritized; and (3) intracranial signs of compensatory collateral
circuits favor a high degree of stenosis. In carotid occlusion, no velocity signal is
present for at least 1.5 cm, and at least one of the compensatory intracranial
collateral circuit signals must be present.
Beyond the degree of stenosis, ultrasonography provides other parameters
related to stroke risk attributable to a given carotid stenosis (stenosis of greater
than 50%, progression of degree of stenosis, plaque surface ulceration,
hypoechogenic and vascularized plaque, cerebral microembolic signals, bad
intracranial collateralization, and exhaustion of cerebral vasoreactivity), that
inform a decision regarding the need for revascularization. The mechanism of
stroke can be a decrease in distal perfusion pressure or a carotid atheroembolism.
Questions That May be Addressed by Neurosonology in the Setting of TABLE 12-2

Acute Stroke
◆ Has a large artery occlusion occurred? Do not delay the CTA (computed tomography
angiography)!
◆ How are the cerebral hemodynamics?
◆ Is the artery opening with thrombolysis?
◆ Was the revascularization hemodynamically satisfactory?
◆ Has an artery reoccluded?
◆ Was the stroke caused by an atherosclerotic lesion? Does it have a criterion for
revascularization?
◆ Is a dissection hemodynamically unstable and a candidate for revascularization?
◆ Has a cerebral hyperperfusion syndrome developed after cerebral artery revascularization
or after carotid endarterectomy?
◆ Are clues for a cardioembolic etiology present?
◆ Is a patent foramen ovale present and worth closing?
◆ Is a cerebral vasoconstriction syndrome, vasculitis, or more rare syndrome such as
moyamoya syndrome likely?
◆ Are any arteriovenous malformation clues present in a patient with an intracranial hemorrhage?
◆ Have subarachnoid hemorrhage vasospasm criteria for endovascular treatment been
evaluated?
◆ Are hemodynamic or optic nerve sheath signs of increased intracranial pressure present?
◆ Are signs of cerebral circulatory arrest present?

A higher degree of stenosis is related to both mechanisms, whereas unstable

plaques (characterized by irregular surface, hypoechogenic signal,
vascularization as evaluated with contrast agents, or those that generate
microembolic signals) tend to be more associated with embolism formation, and
a lack of good distal compensatory blood flow increases the risk of severe
hypoperfusion. FIGURE 12-3 illustrates some examples of unstable symptomatic
carotid plaques.
Cervical vertebral artery stenosis is most frequent at its ostium. Its severity can
be assessed by the decrease in lumen diameter and by blood flow velocity at the
stenotic segment and more distally. In the case of severe stenosis or occlusion, the
contralateral vertebral artery may compensate by providing flow in an inverted
TABLE 12-3 Criteria to Define Degree of Stenosis in Internal Carotid Atherosclerotic

Plaquea
Degree of stenosis as defined by NASCET (the North American Symptomatic Carotid

Endarterectomy Trial), %
10-40 50 60 70 80 90 Occlusion
Main criteria
1 B-mode image, diameter Applicable Possibly Imaging of

applicable occluded
artery
2 Color Doppler image Plaque Flow Flow Flow Flow Flow Absence
delineation of flow
3 PSV threshold, 125 230 NA NA

cm/s
4a PSV average, cm/s ≤160 210 240 330 370 Variable NA
4b PSV poststenotic, cm/s ≥50 <50 <30 NA
5 Collateral flow Possible Present Present Present

(periorbital arteries or
circle of Willis)
Additional criteria
6 Prestenotic flow Possibly Reduced Reduced Reduced

(diastole) (CCA) reduced
7 Poststenotic flow Moderate Pronounced Pronounced Pronounced Variable NA

disturbances (severity and
length)
8 End-diastolic flow <100 >100 Variable NA

velocity in the stenosis
(cm/s)
9 Carotid ratio <2 ≥2 ≥2 >4 >4 Variable NA

ICA/CCA
CCA = common carotid artery; ICA = internal carotid artery; NA = not applicable; PSV = peak systolic velocity.
a
Modified with permission from von Reutern GM, et al, Stroke.2 © 2012 American Heart Association.
330 FEBRUARY 2023

direction into the intracranial KEY POINTS
segment of the affected vertebral
● Higher degrees of
artery. It is more difficult to stenosis are related to both
establish velocimetric criteria for the decrease in distal
vertebral stenosis because perfusion pressure and
physiologic asymmetry in arterial atheroembolism.
Atheroembolic risk is further
diameter is frequent.5 This
linked to unstable plaque
asymmetry dictates blood flow features.
velocity variation, with a lower
velocity and higher resistance ● Cervical vertebral artery
index in the narrower side. stenosis can be assessed by
the decrease in lumen
In occlusion or tight stenosis diameter and measurement
of the proximal subclavian artery of blood flow velocity at the
proximal to the vertebral artery stenotic segment and more
ostium, the arm might be distally.
perfused by an inverted flow ● Subclavian steal effect
FIGURE 12-2
Assessment of the degree of luminal stenosis,
from the ipsilateral vertebral consists of inverted flow
measured by methods used in NASCET (the artery, while the contralateral from the ipsilateral vertebral
North American Symptomatic Carotid vertebral artery has a artery when a tight stenosis
Endarterectomy Trial) and ECST (the European or occlusion of the proximal
compensatory high blood flow
Carotid Surgery Trial) angiographic studies. subclavian artery is present.
CC = common carotid method; CCA = common carotid
velocity. This is called a
artery; ECA = external carotid artery; ICA = internal subclavian steal effect and, when ● Ultrasound signs of
carotid artery. symptomatic, subclavian steal dissection may include an
Reprinted with permission from Valdueza JM, et al.4 © 2017 enlarged artery with an
syndrome. FIGURE 12-4 illustrates
Thieme Medical Publishers, Inc. eccentric hypoechogenic
this phenomenon.4 luminal stenosis, tapering
CASE 12-1 is an example stenosis ending in a string
of a clinical case in which ultrasonography provided insight into multifocal sign, floating intimal flap,
atherosclerosis, subclavian steal effect, and paroxysmal atrial fibrillation. and double lumen
appearance, with to-and-fro
aspect in color and spectral
ARTERIAL DISSECTION. Arterial dissection is the cause of approximately 2.5% Doppler in the false lumen.
of all cases of cerebral ischemia and the second leading cause of stroke in
young adults. Cervical vascular ultrasonography can disclose signs of arterial
dissection, both directly and indirectly. Usually, an intimal tear has occurred,
leading to an intramural hematoma, provoking an enlargement of the artery with
a variable degree of eccentric intraluminal stenosis or even occlusion. Dissections
frequently occur at the postbulbar distal cervical or cervicocranial levels due to
neck mobility and trauma against bone surfaces. Direct ultrasound dissection
signs include an enlarged artery with an eccentric hypoechogenic luminal
stenosis, sometimes a tapering stenosis ending in a string sign, and a floating
intimal flap. Another possible finding is a double lumen appearance, with a to-
and-fro aspect in color and spectral Doppler in the false lumen. However, distal
dissections might be detected mainly through hemodynamic signs either by
finding a stenotic carotid flow acceleration in a distal retromandibular approach
or indirectly finding a significantly higher resistance index in the cervical carotid
segment, meaning an occlusion or high-degree stenosis is present distally. TCD
may also add hemodynamic information. Doppler ultrasonography might be
important to check if a dissection is hemodynamically unstable and if the patient
may be a candidate for revascularization.
Overall, the sensitivity, specificity, and positive and negative predictive values
for color Doppler sonography to diagnose patients with a spontaneous internal

FIGURE 12-3
Examples of unstable symptomatic carotid plaques. Left, Subocclusive hypoechogenic
stenosis (arrow) with high flow acceleration. Middle, Highly stenotic hypoechogenic and
ulcerated plaque (arrows). Right, Highly stenotic active plaque with a microembolic signal
in the ipsilateral middle cerebral artery (arrows).
ACI = internal carotid artery; DTA = right side.
FIGURE 12-4
Illustration of subclavian steal phenomenon and its effect on vertebral artery blood flow.
N = normal.
Reprinted with permission from Valdueza JM, et al.4 © 2017 Thieme Medical Publishers, Inc.
332 FEBRUARY 2023

carotid artery dissection causing carotid territory ischemia were 96%, 94%, KEY POINTS
92%, and 97%, respectively.6 Nevertheless, as carotid dissection lesions are often
● Concentric
high in the neck or intracranial where ultrasonography lacks morphologic hypoechogenic vessel wall
resolution, the diagnosis is better confirmed with other angiographic techniques. thickening is the
MRI is best suited to visualize the intramural hematoma characteristic of an sonographic hallmark of
arterial dissection. vasculitis.
In vertebral arteries, finding direct signs of dissection might be more
● Giant cell arteritis is the
challenging but is possible in the V1, V2, and sometimes in V3 segments, although most common form of large
dissection might be identified only by hemodynamic changes. and medium vessel
In some cases of aortic dissection, the dissection ascends to the proximal vasculitis affecting adults,
common carotid arteries. FIGURE 12-7, VIDEO 12-1, and VIDEO 12-2 show some characterized by a
hypoechogenic
ultrasonography examples of cervical carotid and vertebral dissection.7 noncompressible thickening
of the wall (the halo sign) in
VASCULITIS. Systemic vasculitis might also affect the cervical arteries. In this the temporal branch of the
case, concentric hypoechogenic vessel wall thickening is present, with blood flow external carotid artery.
acceleration if the intraluminal stenosis is significant, which may lead to vessel ● Transient perivascular
occlusion. Takayasu arteritis is an uncommon vasculitis affecting the aorta and inflammation of the carotid
main branches, with wall thickness in the typical macaroni sign (concentric artery syndrome associates
thickening of the arterial wall with a regular surface and intermediate carotid pain with an
eccentric carotid stenosis,
echogenicity). In clinical practice, the most common adult form of vasculitis is
disappearing within a few
giant cell arteritis (GCA). GCA frequently causes an intense and sustained weeks spontaneously or
headache, affecting the temporal branch of the external carotid artery, where after treatment with
arterial changes can be detected by ultrasonography. In suspected cases, a anti-inflammatory drugs.
hypoechogenic noncompressible wall thickening (the halo sign, seen in
● Isolated hypoechogenic
FIGURE 12-8) has a high diagnostic accuracy of 77% sensitivity and 96% mural thrombi might appear
specificity8; the bilateral halo sign has even higher diagnostic accuracy. This associated with
disease frequently affects other branches of the external carotid artery, the thrombophilia and
ophthalmic circulation, and sometimes the vertebral arteries, potentially leading disappear by lysis,
spontaneously, or after
to amaurosis and posterior circulation stroke. anticoagulation therapy.
Monitoring response to treatment with ultrasonography is important and will
become crucial as new treatments for GCA involving interleukin 6 inhibition
may impair the usefulness of measuring C-reactive protein and erythrocyte
sedimentation rate as follow-up parameters. TABLE 12-49 shows cutoff values for
ultrasound intima-media thickness in GCA, and FIGURE 12-8 shows clinical
examples of GCA.10
TRANSIENT PERIVASCULAR INFLAMMATION OF THE CAROTID ARTERY AND MURAL

THROMBI. A more recently described inflammatory entity is transient perivascular
inflammation of the carotid artery syndrome,11 characterized by carotid pain
associated with an eccentric carotid stenosis, disappearing within a few weeks
spontaneously or after treatment with anti-inflammatory medications.
Other potential transient stenotic lesions should be excluded, such as a carotid
dissection or an isolated nonocclusive mural floating thrombus in the absence of
atherosclerosis. These mural thrombi might appear associated with
thrombophilia and disappear by lysis, spontaneously, or after anticoagulation
therapy (FIGURE 12-9).
FIBROMUSCULAR DYSPLASIA AND CAROTID WEB. Fibromuscular dysplasia is a rare,

idiopathic, noninflammatory, and nonatherosclerotic fibrous or fibromuscular
thickening of the arterial wall. Any layer of the vessel wall may be affected,

CASE 12-1 A 68-year-old man who had a history of smoking and medication-
controlled hypertension presented with transient left arm paresis and
periods of dizziness. The neurologic examination was normal.
Ultrasonography showed a left-sided carotid occlusion and intracranial
collateralization to its territory through the anterior communicating
artery, although maintaining a dampened flow in the left middle cerebral
artery. It also demonstrated a right-sided significant carotid stenosis, a
left-sided subclavian steal effect, and probable paroxysmal atrial
fibrillation (FIGURE 12-5 and FIGURE 12-6). This information led to several
secondary prevention measures after the transient ischemic attack. The
patient started direct anticoagulant therapy, and a 24-hour ECG
confirmed paroxysmal atrial fibrillation. His low-density lipoprotein
cholesterol was 205 mg/dL, and he started statin therapy. Arterial
hypertension was well controlled with medications. Right carotid
revascularization surgery was performed. MR angiography confirmed a
left subclavian proximal near-occlusion that was treated with stenting.
The patient stopped smoking with the help of transdermal nicotine. All
intracranial hemodynamics were improved on a follow-up examination,
and the patient remained asymptomatic.
FIGURE 12-5
Ultrasonography of the patient in CASE 12-1 with multifocal atherosclerosis and paroxysmal
atrial fibrillation. Left-sided cervical carotid arteries (A): common carotid artery (ACC)
velocities spectral analysis with high resistance flow suggesting a downstream occlusion and
cardiac arrhythmia suggestive of atrial fibrillation. B, Internal carotid artery occlusion
(arrow). Right-sided cervical carotid arteries (C): common carotid artery (ACI) with normal
flow (D) and internal carotid artery with a 70% stenosis (arrow), with focal flow acceleration.
ACE = external carotid artery; Dta = right side; Esq = left side.
334 FEBRUARY 2023

FIGURE 12-6
Ultrasonography of the patient in CASE 12-1 with multifocal atherosclerosis and
paroxysmal atrial fibrillation. Intracranial collateralization through the anterior
communicating artery with turbulent and inverted flow direction in left A1 segment
(A, arrow), with partial compensation of left M1 flow (dampened) (B, arrow). Cervical
vertebral arteries: left vertebral artery with inverted flow direction (C, arrow) and
cardiac arrhythmia; right vertebral artery with normal direction and globally accelerated
flow (D). Intracranial vertebral arteries (V4) and basilar artery: left V4 with inverted flow
direction (E, arrow in color Doppler red, in contrast to the contralateral, in blue);
right V4 with normal direction flow (F); biphasic flow at proximal basilar (G, arrow), as
part of the flow from right V4 goes to left V4, and part follows to distal basilar; distal
basilar with normal flow direction (H).
AV = vertebral artery; dta = right side; esq = left side; INV = inverted flow.
This case exemplifies how useful a noninvasive ultrasound cerebrovascular COMMENT

examination can be for timely detection of lesions, leading to targeted
therapeutic and preventive treatments.

FIGURE 12-7
Examples of cervical carotid and vertebral dissection. A, Common carotid artery (CCA)
dissection as an extension of aortic dissection; also see VIDEO 12-1 and VIDEO 12-2 with a
floating intimal flap. B, Internal carotid artery (ICA) dissection with postbulbar occlusion
(left) and with hypoechogenic tapering distal cervical stenosis (right). C, CCA (left) and
vertebral (right) dissections with a double lumen.
Panel C reprinted with permission from Azevedo E and Castro P.7 © 2014 John Wiley & Sons, Inc.
resulting in arterial stenosis, occlusion, aneurysm, or dissection. It most

commonly affects the renal and extracranial carotid and vertebral arteries, where
it can cause headache or pulsatile tinnitus. Ultrasonography may reveal the
characteristic alternation of stenoses and dilations, causing a string-of-beads
appearance, associated with velocity shifts in the mid to distal cervical internal
carotid artery and the vertebral arteries. Although a sinusoidal curve in the internal
carotid artery is not specific to fibromuscular dysplasia, its presence on a carotid
ultrasonogram in a patient younger than 70 years of age should alert to the
possibility of fibromuscular dysplasia.12
336 FEBRUARY 2023

KEY POINTS
● Fibromuscular dysplasia
is suspected by a string-of-
beads appearance in the
distal cervical internal
carotid artery and the
vertebral arteries.
● Carotid webs are

potentially thrombogenic
and may be implicated in
ischemic stroke.
Sonographically it appears
as a shelf-like membrane in
the posterior aspect of the
internal carotid artery bulb
into the lumen, just beyond
the carotid bifurcation.
FIGURE 12-8
Examples of the halo sign in giant cell arteritis in an older woman with a vertebrobasilar
stroke and high inflammatory biomarkers. A, Concentric hypoechogenic thickness of the
vertebral artery walls, in some segments associated with a blood flow velocity acceleration,
which is suggestive of vasculitis. B, The superficial temporal arteries also showed concentric
hypoechogenic thickness of the walls that was suggestive of giant cell arteritis. C,
Compression led to the disappearance of the residual lumen, but the wall thickness was
maintained. D, The typical halo sign in a cross-sectional view. E, An axillary artery was also
affected and shows the typical halo sign. F, Appearance of the branches of the temporal
artery before (left) and after (right) starting corticosteroid treatment.
Carotid webs, shown in FIGURE 12-10, are rare variants of fibromuscular

dysplasia, defined as a thin, linear membrane that extends from the posterior
aspect of the internal carotid artery bulb into the lumen, located just beyond
the carotid bifurcation. It is highly thrombogenic and may be implicated in
ischemic stroke. Carotid ultrasonography may detect the carotid web as a
shelf-like echogenic lesion, although conventional angiography remains the

gold standard examination. Meticulous sonographic technique, appropriate

education, and a high index of suspicion are necessary to differentiate the
carotid web from arterial dissection, focal atherosclerotic plaque, and mural
thrombus.13,14
ARTERIOVENOUS SHUNTS. Doppler ultrasonography can reveal signs of

arteriovenous pathologic shunts. Normally, the internal carotid artery has a lower
resistance than the external carotid artery. When the external carotid artery
demonstrates high velocity and low resistance, one of its branches might be
involved in an arteriovenous shunt, namely a fistula between the occipital artery
and a dural sinus (FIGURE 12-11). The same type of hemodynamic changes can
raise the suspicion of arteriovenous shunts in other vessels. Ultrasound screening
for dural arteriovenous fistula in patients with pulsatile tinnitus revealed
sensitivity, specificity, and positive and negative predictive values of 96%, 100%,
100%, and 98%, respectively. The isolated use of a low external carotid artery
resistance index showed a sensitivity of 81%.15,16 These data are summarized in
TABLE 12-5.
Intracranial Neurovascular Ultrasonography

Even with transcranial color sonography, it is not possible to study the
intracranial arterial wall with ultrasonography. However, TCD and transcranial
color sonography contribute important hemodynamic information to the
understanding of clinical situations and are also tools for research. At an
intracranial level, vascular ultrasonography mainly allows for the detection of
flow direction, the measurement of blood flow velocities, and some
hemodynamic indices in the main basal arteries of the brain.
COMPENSATORY INTRACRANIAL COLLATERAL CIRCUITS OF PROXIMAL STENO-

OCCLUSIVE DISEASE. TCD and transcranial color sonography allow for the
detection of intracranial arterial stenosis and occlusions and the hemodynamic
effects of downstream and upstream disease.
In the setting of an extracranial carotid and vertebral stenosis or occlusion,
TCD and transcranial color sonography can identify compensatory intracranial
collateral circuits. The following may be seen in the setting of carotid steno-
occlusive disease: an inversion of ophthalmic flow direction perfused by branches
TABLE 12-4 Cutoff Values for Ultrasonography Intima-Media Thickness in Giant Cell
Arthritis
Anatomic region Cutoff intima-media thickness, mm

Common superficial temporal artery (TA) 0.42
Frontal branch of TA 0.34
Parietal branch of TA 0.29
Axillary artery 1.0
a
Reprinted with permission from Schafer VS, et al, Rheumatology (Oxford).9 © 2017 Oxford University Press.
338 FEBRUARY 2023

KEY POINTS
● When the external carotid

artery shows high velocity
and low resistance, an
arteriovenous shunt may be
suspected, especially in a
patient with pulsatile
tinnitus.
● The thrombolysis in brain

ischemia score helps in
evaluation of the flow
conditions in the
symptomatic intracranial
artery in acute ischemic
stroke, namely before and
after recanalization
treatment.
FIGURE 12-9
Floating mural thrombi in the absence of atherosclerosis. A 36-year-old woman was admitted ● Systolic and mean blood
48 hours after having an acute left faciobrachial paresis due to a cortical frontal ischemic flow velocity cut-offs help
stroke. Top, Ultrasonography showed, in the right carotid artery, mobile mural material diagnose intracranial
suggestive of nonocclusive thrombi, homogeneously hypoechogenic, and a relatively narrow stenosis and stratify it as
wall pedicle. An anticoagulant was prescribed. Bottom, Spontaneous revascularization <50%, >50%, and >70%.
occurred after 1 week, and treatment was shifted to aspirin.
ACC = common carotid artery; ACE = external carotid artery; ACI = internal carotid artery; DTA = right side.
of the external carotid artery, an inversion of flow direction in the A1 segment

of the anterior cerebral artery of the affected side and acceleration in the
contralateral (collateralization through the anterior communicating artery),
and collateralization through the ipsilateral posterior communicating artery
(marked by increase blood flow velocity in the P1 segment of posterior carotid
artery). For cervical vertebral steno-occlusive disease, an inversion of flow
direction in the distal intracranial vertebral artery, perfused by the contralateral
vertebral artery, may be seen.
THROMBOLYSIS IN BRAIN ISCHEMIA SCORE. In the setting of hyperacute ischemic

stroke, the TCD thrombolysis in brain ischemia score relates the spectral Doppler
wave with the distance to the point of arterial occlusion or identifies a local
significant stenosis (FIGURE 12-12). Thrombolysis in brain ischemia waveforms
are graded according to flow as follows: 0, absent; 1, minimal; 2, blunted; 3,
dampened; 4, stenotic; and 5, normal. This score is useful for monitoring
intracranial large vessel occlusion, recanalization, or even an eventual reocclusion,
in acute stroke.17
INTRACRANIAL STENOSIS. Intracranial stenosis is detected by a focal

systolic-diastolic acceleration of blood flow velocity. Comparing data from
transcranial color sonography and catheter angiography allows cutoff systolic
blood flow velocity values for intracranial stenosis, reliably being able to detect
50% or greater and less than 50% basal cerebral artery narrowing (TABLE 12-6).18
Other authors have validated mean blood flow velocity detected by TCD with
angiographic changes. They have also highlighted the importance of the ratio
between blood flow velocity in the most stenotic point and the previous

FIGURE 12-10
Carotid web in a 42-year-old woman with a middle cerebral artery ischemic stroke
successfully treated with thrombectomy. Ultrasonography revealed a thin, linear, protruding
membrane in the posterior aspect of the internal carotid artery (ICA) bulb (arrows). Top,
Longitudinal view. Bottom, Cross-sectional view.
ECA = external carotid artery.
lesion-free segment (a ratio greater than 2 related to more than 50% stenosis,
greater than 3 related to more than 70% stenosis), as shown in TABLE 12-7.19
Nevertheless, if a stenosis occurs after another critical stenosis, blood flow
velocity might not proportionally increase, and if the lumen is long and
narrow, rather than focally narrow, the blood flow velocity might be
decreased instead.20
FIGURE 12-11
Ultrasonography from a patient with pulsatile tinnitus and a dural arteriovenous fistula.
A, External carotid artery (ECA) with a low resistance flow (resistance index 0.51; arrow).
B, The ECA’s occipital branch demonstrated higher velocities and even lower resistance
index (0.40; arrow). C, Ipsilateral jugular vein with high-velocity flow, draining the fistula
(arrow).
CCA = common carotid artery; ICA = internal carotid artery.
340 FEBRUARY 2023

A middle cerebral artery branch occlusion can be suspected when the M1
segment has lower blood flow velocity than the ipsilateral anterior cerebral artery
and contralateral M1 segment. TCD or transcranial color sonography can detect
stenosis or occlusion of intracranial vessels in patients with acute ischemic stroke
with high sensitivity and specificity, and guide the need for more invasive
vascular neuroimaging.21
However, ultrasound diagnosis of an intracranial stenosis does not
specify its nature (eg, atherosclerotic or other). Factors favoring an
atherosclerotic nature are very focal blood flow velocity acceleration, the
absence of short-term relevant fluctuations of blood flow velocity, and
the presence of atherosclerotic pathology in extracranial vessels. Factors
favoring nonatherosclerotic vasculopathy (embolus, dissection, vasospasm,
vasculitis) include changing blood flow velocity over time, within days to a
few months.
Some findings are suggestive of a cardioembolic source of emboli22: a
nonlacunar stroke syndrome, absence of extracranial atherosclerosis, initial
documentation of stenosis or occlusion in the middle cerebral artery or basilar
bifurcation with early (hours to a few days) spontaneous recanalization, and
documentation of microembolic signals to bilateral vessels of the cerebral
circulation. The diagnosis of patent foramen ovale (PFO) with TCD is described
later in this article.
Regarding intracranial vasculitis, one of the sonographic clues to the diagnosis
is finding segmental blood flow velocity acceleration in different vessels,
especially if no atherosclerosis is present in cervical vessels and if it is a dynamic
process with velocities changing in the short term. Although rare in adults,
intracranial vasculitis is an important cause of stroke in children, sometimes
associated with infections as in the case of tuberculous cerebral vasculitis shown
in CASE 12-2, where transcranial color sonography helped detect the focal
vascular changes.
Another rare cause of intracranial steno-occlusive disease is moyamoya
disease, found mostly in the Asian population, although a moyamoyalike
phenomenon (moyamoya syndrome) is sometimes associated with other
conditions. With ultrasonography, suspicion for this syndrome is raised with
occlusion or tight stenosis of the distal intracranial internal carotid artery or even
Ultrasonographic Criteria for Arteriovenous Fistulaa TABLE 12-5
General suspicion of an arteriovenous fistula

◆ Artery with increased velocity and decreased resistance index
◆ Artery with decreased resistance index compared to the other side
◆ Increased jugular vein drainage on the same side
Suspicion of dural arteriovenous fistula
◆ Resistance index in external carotid artery (ECA) < 0.7 and resistance index in internal
carotid artery (ICA)/ECA > 0.9 (sensitivity, 55%; specificity, 88%)14
◆ Diastolic velocity in the ECA > 21 cm/s16
a
Data from Tsai LK, et al, Ultrasound Med Biol.15

FIGURE 12-12
Thrombolysis in brain ischemia score.
Reprinted with permission from Demchuk AM, et al, Stroke.17 © 2001 American Heart Association.
at the ostium of the middle cerebral artery and anterior cerebral artery. The
changes are often bilateral.
SICKLE CELL DISEASE. The STOP (Stroke Prevention Trial in Sickle Cell Anemia)
trial demonstrated that screening children with TCD and treating those with
abnormal TCD velocities with regular blood transfusion may result in a 10-fold
decrease in the prevalence of strokes in children.23 The burden of neurologic
complications of sickle cell disease in Africa is most likely underestimated.24
The threshold for regular blood transfusion therapy is two nonimaging TCD
measurements of 200 cm/s or greater time-averaged mean of the maximum blood
flow velocity measurement or a single TCD measurement greater than 220 cm/s in
the proximal portion of the middle cerebral artery or the distal portion of the
internal carotid artery. As recommended by the American Society of Hematology,
annual TCD screening should be offered for children (aged 2 to 16 years) with
sickle cell disease of the type HbSS (those with two genes, one from each parent,
that code for hemoglobin S) or of the type Sβ0 (sickle beta 0) thalassemia.25
SUBARACHNOID HEMORRHAGE. Patients with subarachnoid hemorrhage (SAH) are

at risk of delayed cerebral ischemia and cerebral infarction, usually occurring
between days 4 and 14. Focal hypoperfusion from reversible cerebral arterial
342 FEBRUARY 2023

Cutoff Peak Systolic Blood Flow Velocity Values for Intracranial Stenosis TABLE 12-6
by Transcranial Color Sonographya
Ultrasonography Angiography
Positive Negative
predictive predictive Number of Mean ± SD
PSV cutoff, cm/s Sensitivity, % Specificity, % value, % value, % patients studied degree (range)
Ultrasonic detection of ≥50% intracranial stenoses (n = 31) with angiography as standard of reference
ACA ≥155 100 100 100 100 4 60 ± 8 (52-71)
MCA ≥220 100 100 100 100 11 67 ± 11 (50-80)
PCA ≥145 100 100 100 91 10 63 ± 7 (50-72)
BA ≥140 100 100 100 100 3 67 ± 14 (53-85)
VA ≥120 100 100 100 100 3 69 ± 14 (55-84)
Ultrasonic detection of <50% intracranial stenoses (n = 38) with angiography as standard of reference
ACAb ≥120 100 99 73 100 5 38 ± 12 (20-47)
MCA ≥155 94 100 95 100 18 36 ± 8 (22-48)
PCA ≥100 100 100 100 100 5 29 ± 12 (13-41)
BA ≥100 100 100 100 100 4 33 ± 4 (29-37)
VA ≥90 100 100 100 100 5 32 ± 6 (25-39)
ACA = anterior cerebral artery; BA = basilar artery; MCA = middle cerebral artery; PCA = posterior cerebral artery; PSV = peak systolic velocity;
VA = vertebral artery.
a
Modified with permission from Baumgartner RW, et al, Stroke.18 © 1999 American Heart Association.
b
One stenosed anterior cerebral artery was missed because of an inadequate temporal bone window.
Cutoff Mean Blood Flow Velocity Values for Intracranial Stenosis by TABLE 12-7
Transcranial Dopplera
Artery Stenosis ≥ 50% (MFV, SPR) Stenosis ≥ 70% (MFV, SPR)

Middle cerebral artery ≥ 100 cm/s, ≥2 ≥ 120 cm/s, ≥3
Anterior cerebral artery ≥ 80 cm/s, ≥2 Not applicable, ≥3
Posterior cerebral artery ≥ 80 cm/s, ≥2 Not applicable, ≥3
Basilar artery ≥ 90 cm/s, ≥2 ≥ 110 cm/s, ≥3
Vertebral artery ≥ 90 cm/s, ≥2 ≥ 110 cm/s, ≥3
MFV = mean flow velocity; SPR = stenotic/prestenotic mean flow velocity ratio.
a
Data from Zhao L, et al, Stroke.19

CASE 12-2 A 20-month-old girl had recurrent fever in the previous 4 months, weight
loss, and cervical lymphadenopathy. After worsening lethargy,
irritability, and vomiting over several days, she was brought to the
emergency department. Neurologic examination disclosed altered
mental status and signs of meningeal irritation. Brain MRI showed focal
punctiform restriction of diffusion on the DWI study (FIGURE 12-13). CSF
findings included elevated total nucleated cell count (108 cells/mm3),
with neutrophil predominance (71%), elevated total protein level
(85 mg/dL), and reduced glucose level (26 mg/dL). In transcranial color
sonography, blood flow velocity showed several changes, namely
abnormally increased velocity in the left A1 segment and low velocity in
the right P2 segment, predicting ischemic lesions that were later seen on
head CT. The overall picture suggested cerebral vasculitis. An interferon
gamma release assay, tuberculin skin test, and Mycobacterium
tuberculosis polymerase chain reaction (PCR) sputum smears were
positive. The child started antituberculosis therapy with isoniazid,
rifampin, pyrazinamide, and ethambutol.
COMMENT This case exemplifies the usefulness of monitoring cerebral hemodynamics

in neurocritical care patients in whom the clinical course may be dynamic.
This evaluation is complementary to other neuroimaging examinations,
increasing the overall understanding of the ongoing pathophysiology.
344 FEBRUARY 2023

FIGURE 12-13
Imaging from the patient in CASE 12-2.Tuberculous cerebral vasculitis shown in the initial
transcranial color sonography with high velocity in the left anterior cerebral artery
suggestive of stenosis and low velocity in the right posterior cerebral artery suggestive of
a distal lesion (A, arrows). Initial axial diffusion-weighted (DWI) (arrow) and apparent
diffusion coefficient (ADC) MRI (B), and axial CT scan (C) 7 days after admission, with
global edema and bigger infarct areas in the left anterior cerebral artery and right posterior
cerebral artery territories.

vasospasm due to exposure of the arteries to perivascular blood is likely to play a

relevant causal role. Although angiography is the gold standard for detecting
vasospasm, TCD evidence of vasospasm is a good predictor of delayed cerebral
ischemia in aneurysmal SAH, with a 90% sensitivity and 71% specificity.26 TCD
is more appropriate for repetitive screenings with the American Heart
Association/American Stroke Association guidelines recommending it as a
technique for monitoring vasospasm.27
Vasospasm causes a blood flow velocity increase in the affected segments.
To correctly distinguish it from other physiologic and pathologic conditions
that could result in elevated blood flow velocity, such as hyperemia and
hypertension, a hemispheric ratio of the mean blood flow velocity in the middle
cerebral artery and distal ipsilateral extracranial internal carotid artery is applied
(TABLE 12-8).28 Elevations of blood flow velocity in both the middle cerebral
artery and internal carotid artery would result in a hemispheric ratio less than 3,
whereas vasospasm would preferentially elevate middle cerebral artery blood
flow velocity. Vasospasm is considered mild if the hemispheric ratio is 3 to 6
and severe if it is greater than 6. Regarding the posterior circulation, the
detection of more than 50% vasospasm in the basilar artery with a mean
blood flow volume greater than 85 cm/s and a modified ratio (basilar artery/
vertebral artery) greater than 3 have been shown to have a sensitivity of 92%
and specificity of 97%.29 TABLE 12-8 and TABLE 12-9 show TCD vasospasm
criteria in SAH,28 and FIGURE 12-14 illustrates sequential blood flow velocity
changes due to vasospasm in a case of SAH.
Cerebral ultrasound perfusion imaging has been recently found to be a feasible
technique to detect cerebral hypoperfusion after SAH, which might lead to
TABLE 12-8 Transcranial Doppler Vasospasm Criteria for the Middle Cerebral Arterya
Mean flow velocity Middle cerebral artery/internal

(MFV), cm/s carotid artery MFV ratio Interpretation
<120 ≤3 Hyperemia
>80 3-4 Hyperemia + possible mild

spasm
≥120 3-4 Mild spasm + hyperemia
≥120 4-5 Moderate spasm + hyperemia
≥120 5-6 Moderate spasm
≥180 6 Moderate to severe spasm
≥200 ≥6 Severe spasm
>200 4-6 Moderate spasm + hyperemia
>200 3-4 Hyperemia + mild (often

residual) spasm
>200 <3 Hyperemia
a
Reprinted with permission from Alexandrov AV.28 © 2004 John Wiley & Sons.
346 FEBRUARY 2023

delayed cerebral ischemia.30 TCD is also useful for follow-up hemodynamics
after endovascular intervention in vasospasm.
REVERSIBLE VASOCONSTRICTION SYNDROME. TCD can diagnose vasoconstriction

related to reversible vasoconstriction syndrome (RCVS) in the proximal cerebral
arteries, although it often fails when the affected arteries are more distal.
Follow-up monitoring of blood flow velocity using TCD may help identify
patients with more extensive vasoconstriction and higher risk of developing
neurologic complications related to RCVS.31 Velocities are not usually as high as
in SAH vasospasm (only a minority have mean blood flow velocity in the middle
cerebral artery greater than 120 cm/s and a hemispheric ratio greater than 3), but
they maintain a high plateau at the mean time of headache remission (day 22)
and remain abnormal even 10 days after headache resolution,32 so monitoring the
blood flow velocity changes in the time course may be more useful than the
isolated values.
THERAPY MONITORING WITH TRANSCRANIAL DOPPLER. Cerebral hemodynamic

monitoring is an important application of ultrasonography. Beyond monitoring
hemodynamic changes during acute stroke and in the neurocritical setting,
TCD permits real-time monitoring of the effect of drugs and other treatments,
such as thrombolytic and endovascular therapy in acute ischemic stroke or
antiedematous measures in the intensive care patient. TCD also allows for
monitoring of emboli and changes in perfusion during interventions such as
carotid revascularization and cardiac surgery. A higher blood flow velocity in a
successfully recanalized middle cerebral artery, compared with the contralateral
side, indicates a risk for postinterventional intracerebral hemorrhage and
worse prognosis.33
INTRACRANIAL HYPERTENSION AND CEREBRAL CIRCULATORY ARREST. Although TCD

and transcranial color sonography do not allow for measurement of intracranial
pressure (ICP) itself, they can provide indirect information regarding changes in
ICP. In normal conditions and as an organ of low resistance, the brain is well
Transcranial Doppler Vasospasm Criteria for Intracranial Arteriesa TABLE 12-9
Arterial mean flow velocity, cm/s
Definite
Possible vasospasm Probable vasospasm vasospasm
Internal carotid artery >80 >110 >130
Anterior cerebral artery >90 >110 >120
Posterior cerebral artery >60 >80 >90
Basilar artery >70 >90 >100
Vertebral artery >60 >80 >90
a
Reprinted with permission from Alexandrov AV.28 © John Wiley & Sons.

perfused during the full cardiac

cycle. As ICP increases, the
cerebral blood flow velocity
during diastole decreases,
disappears, and even reverses;
systolic blood flow velocity also
decreases. When positive
diastolic blood flow velocity is
still present in the main cerebral
arteries, increasing blood
pressure and decreasing ICP
might improve cerebral blood
flow and eventually the clinical
condition. At least 30 minutes
without diastolic positive blood
flow velocity and decreased
systolic blood flow velocity in
both middle cerebral arteries and
the basilar artery indicates
cerebral circulatory arrest, and
clinical brain death tests will
likely be positive.34 TABLE 12-10
shows the criteria for cerebral
circulatory arrest by TCD, and
FIGURE 12-15 shows a case of
cerebral circulatory arrest.
Limitations of this
examination might be poor bone
windows for ultrasonography
and distortion of vascular
structures. In cases of very high
FIGURE 12-14
A case of subarachnoid hemorrhage with a
intracranial hypertension and no
sequential velocity increase due detectable intracranial flow with
to vasospasm on days 7 (A), 9 (B), and 11 (C). TCD and transcranial color
TABLE 12-10 Criteria for Cerebral Circulatory Arrest by Transcranial Dopplera
◆ Biphasic flow with diastolic reflux

◆ Flow only with protosystolic peaks with velocity lower than 50 cm/s
◆ Flow with an intermediate pattern between the two criteria above
a
Any of the three flow patterns in the table might be present in cerebral circulatory arrest diagnosis by
transcranial Doppler. To achieve criteria for cerebral circulatory arrest, any of these flow patterns should be
recorded in three intracerebral arteries from different territories, in both carotid territories (usually in the
middle cerebral arteries) and in the vertebrobasilar (usually in the basilar artery). If the blood flow velocity
cannot be registered with transcranial Doppler because of excessive intracranial pressure, the above
criteria might be found in cervical internal carotid and vertebral arteries. This pattern should be continuously
present for at least 30 minutes.
348 FEBRUARY 2023

FIGURE 12-15
Cerebral circulatory arrest ultrasonography shows only protosystolic peaks with a velocity
lower than 50 cm/s and the absence of diastolic flow (arrow) in both the middle cerebral
(ACM) and basilar arteries (top) and in extracranial internal carotid (ACI) and vertebral
arteries (bottom).
sonography, the flow patterns referred to earlier can be observed in extracranial

carotid and vertebral artery color Doppler sonography.
Although ultrasonography is not influenced by central nervous system
depressants, it is influenced by the patient's hemodynamic status, PaCO2, and
temperature. Therefore, the examination should be performed with systolic
blood pressure greater than 90 to 100 mm Hg, with PCO2 35 to 45 mm Hg, and
temperature greater than 32°C (89.6°F).
TCD and transcranial color sonography have approximately 100% specificity
for cerebral circulatory arrest confirmation, provided they are performed by an
experienced operator with the aforementioned criteria and in the context of
suspected clinical brain death. Sensitivity is approximately 90% because false
negatives may be associated with irreversible brainstem damage without a major
impact on ICP.35
TCD and transcranial color sonography are not validated for diagnosis of
cerebral circulatory arrest in children, although the findings are similar.36
TCD can be used to support a diagnosis of brain death in patients on
extracorporeal membrane oxygenation who have sufficient cardiac contractility
or an intra-aortic balloon pump to produce pulsatile flow. TCD utility in patients
on extracorporeal membrane oxygenation who have low left ventricular ejection
fraction needs further study.37
Beyond the blood flow velocity features, brain and eye sonography also
contribute to the evaluation of a patient with elevated ICP, informing eventual
midline shift with space-occupying lesions, and optic nerve changes (see the
Neuro-orbital Ultrasonography section).
TRANSCRANIAL DOPPLER FOR DIAGNOSIS OF RIGHT-TO-LEFT CARDIAC SHUNT. PFO is

present in approximately 25% of the general population and can be a cause of

stroke through a paradoxical cerebral embolism. TCD and a nontranspulmonary

gaseous contrast injection is a reliable and less invasive alternative to the gold
standard transesophageal echocardiography (TEE) for diagnosis of PFO and
enables the detection of eventual extracardiac right-to-left shunt. A well-agitated
mixture of 9 mL of saline and 1 mL of air, in a three-way stopcock, is injected into
the brachial vein. The examination is performed during the resting state and,
unless strongly positive, repeated after the Valsalva maneuver.
In the presence of a right-to-left shunt, the contrast bypasses the pulmonary
circulation and causes microembolic signals (high-intensity signals of short
duration) to be detected in the middle cerebral artery by TCD, visualized in the
velocity spectrum, and heard as “blips” seconds after the injection (FIGURE 12-16
and VIDEO 12-3). The time of occurrence and number of microembolic signals
are used to assess the shunt location (intracardiac if early after injection,
extracardiac if later) and the size and functional relevance of the right-to-left
shunt. The following scale may be used to grade the size of the shunt: (1)
negative; (2) 1 to 10 microembolic signals; (3) more than 10 microembolic
signals and no curtain; and (4) curtain (shower of microembolic signals with no
single bubble being identified).38 The size of a PFO measured by TEE correlates
with the amount of microembolic signals on TCD.39 Nontranspulmonary gaseous
contrast injection TCD is more sensitive than TEE in detecting PFO because
medication-induced sedation and the esophageal probe used in TEE prevent an
adequate Valsalva maneuver. The pooled sensitivity and specificity of TCD for a
PFO are 96.1% and 92.4%, respectively.40 However, TEE and TCD are
complementary and should be applied jointly to detect a PFO and to characterize
its morphologic features.
Microembolic Signal Detection by Transcranial Doppler

TCD can detect and quantify the burden of embolization (microembolic signals)
driven by large artery disease and cardioembolic sources. Although these
microemboli are clinically silent, they may be clinically important by indicating
FIGURE 12-16
Detection with transcranial color sonography of a right-to-left cardiac shunt, caused by a
patent foramen ovale. A, Four microembolic signals are visible in the velocity spectrum
(arrow) of the middle cerebral artery, a few seconds after the gaseous contrast injection in a
brachial vein. B, Repetition of the injection is followed by the Valsalva maneuver with the
early appearance of a curtain of microembolic signals (arrow).
ACM = middle cerebral artery; CMV = with Valsalva maneuver; SMV = without Valsalva maneuver.
350 FEBRUARY 2023

stroke risk because they are associated with a sixfold to eightfold increase in the KEY POINTS
risk of recurrent vascular events after acute stroke.41 Many studies have detected
● Transcranial Doppler
microembolic signals in patients with symptomatic carotid stenosis, and their (TCD) and transcranial color
presence correlates with recent symptoms, ulcerated plaques, and high-grade sonography can accurately
stenosis. In asymptomatic carotid stenosis, microembolic signals are less frequent detect significant
and data are less robust.42 As noted earlier, microembolic signal detection is also intracranial artery stenosis
and occlusion.
useful during carotid endarterectomy and cardiac surgery. This technique is
increasingly used to guide patient management and as a surrogate marker of ● Atherosclerotic stenosis
antithrombotic drug efficacy.43,44 has a more focal and stable
Microembolic signal monitoring is performed over 30 to 60 minutes, usually blood flow velocity increase
with bilateral 2-MHz probes fixed in a headframe. Currently, robotized probes than dynamic intracranial
stenoses such as those
allow the patient to move and walk while being monitored, making longer caused by an embolus,
evaluations easier. dissection, vasospasm, or
vasculitis.
Dynamic Vasoregulation Assessment
● In children with sickle cell
The cerebral distal arteriolar system is responsible for vasomotor regulation and disease, screening with TCD
maintenance of appropriate perfusion of a given volume of cerebral tissue. When for high blood flow velocity
this regulation is disturbed or exhausted, the risk of ischemia, edema, and (≥200 cm/s) and treatment
hemorrhage increases. Dynamic vasoregulation assessment may be performed with regular blood
transfusion may result in a
with ultrasonography. Data analysis is becoming more user friendly, allowing
10-fold decrease in the
this important information to increase knowledge about patient risk and support prevalence of strokes.
clinical decision making, particularly in acute stroke and in patients in the
intensive care unit. ● Annual TCD screening
should be offered for
children aged 2 to 16 years
CEREBRAL AUTOREGULATION. Cerebral autoregulation is one the main with sickle cell disease of
cerebrovascular regulating principles, allowing, in normal conditions, stable the types HbSS or Sβ0
cerebral blood flow within a wide range of systemic blood pressure variation thalassemia.
(within about 50 to 150 mm Hg mean arterial pressure). Cerebral autoregulation
● In patients with
may be assessed via spontaneous fluctuations of blood pressure (by arterial line subarachnoid hemorrhage,
or plethysmography) and blood flow velocity measurement with TCD. As vasospasm can be
previously mentioned, the TCD is performed with bilateral 2-MHz probes fixed monitored with TCD, which
in a headframe to prevent probe sliding and loss of signal. Then, with transfer helps adjust medical and
intervention therapy aiming
function analysis, cerebral autoregulation in the frequency domain can be
to prevent delayed cerebral
characterized by three parameters: phase, gain, and coherence (FIGURE 12-17). ischemia and cerebral
More effective cerebral autoregulation is evidenced by lower coherence and gain infarction.
and higher phase. In the intensive care setting, in patients with an ICP catheter,
the pressure-reactivity index can be derived instead. ● TCD can diagnose
vasoconstriction related to
Worse cerebral autoregulation correlates with increased risk of hemorrhagic reversible cerebral
transformation, larger infarcts, and worse outcome in ischemic stroke.45 vasoconstriction syndrome
Cerebral autoregulation operates slowly (requires at least 6 to 10 seconds) at low in the proximal cerebral
frequencies. No cutoff between normal and abnormal cerebral autoregulation arteries, although there are
no standardized blood flow
has been validated, but a phase shift inferior to 30 degrees has been proposed to velocity criteria.
represent cerebral autoregulation failure, matching the cutoff for worse outcome
in a cohort of patients with ischemic stroke.46,47 ● Changes in blood flow
velocity over time in patients
with reversible cerebral
CEREBRAL VASOREACTIVITY. Cerebral vasoreactivity, or vasomotor reactivity,
vasoconstriction syndrome
is an index of blood flow velocity response to a vasomodulatory stimulus may be more informative
(eg, to acetazolamide or carbon dioxide). The easiest way to evaluate vasomotor than the isolated values.
reactivity is by monitoring blood flow velocity with the previously described
bilateral TCD probes in a headframe while changing PaCO2 because carbon

FIGURE 12-17
Cerebral autoregulation (CA) calculation. Calculation of various CA index values within
6 hours of stroke onset in a patient with the total territory of the middle cerebral artery
(MCA) affected. The continuous signals of transcranial Doppler (TCD) (A) cerebral blood
flow velocity (CBFV) from affected (blue) and unaffected (green) MCA territories and
arterial blood pressure (ABP, red ) are inspected (B) and mean values calculated (mean
blood flow velocity [MFV] and mean arterial pressure [MAP], respectively). From
300 seconds of these time series (C), CA can be calculated in time and frequency
domains. In the first case (D), MFV is plotted against MAP and a Pearson correlation
coefficient is obtained (Mx). Note Mx = 0.52 in the affected hemisphere, while Mx = –0.18
on the contralateral side, meaning CA is worse on the affected side (E). In the frequency
domain (F), the transfer function analysis outputs are coherence, gain, and phase. CA is
highly impaired on the affected side. The patient had a hemorrhagic transformation at
24 hours and remained bedridden (3-month modified Rankin scale of 5).
ARI = autoregulation index.
Reprinted with permission from Castro P, et al, Curr Atheroscler Rep.45 © 2018 Springer Nature.
dioxide is a potent cerebral vasodilator. This can be achieved by either giving the
patient a carbon dioxide-rich air mixture to breathe or inducing hypoventilation
and hyperventilation.
A simple bedside test to assess vasomotor reactivity is to perform a
breath-hold test. After a period of rest and a normal inspiration, the patient
remains in apnea for approximately 30 seconds (or a minimum of 24 seconds).
Then the breath-hold index is calculated, using mean blood flow velocity
(MFV) values: [(maximum MFV at end of apnea – baseline MFV) / baseline
MFV)] 100, divided by apnea time in seconds.
Carbon dioxide vasomotor reactivity can also be assessed with continued
monitoring of mean blood flow velocity changes by TCD and end-tidal carbon
dioxide by capnography (FIGURE 12-1848).49
The grade of vasomotor reactivity has been linked to prognosis in patients in
critical care settings. Importantly, vasomotor reactivity can help in deciding
352 FEBRUARY 2023

KEY POINTS
● TCD can be used to

monitor cerebral
hemodynamics during acute
stroke and in the
neurocritical setting, as well
as before, during, and after
therapeutic interventions.
● TCD and transcranial

color sonography allow for
monitoring intracranial
pressure changes. With
intracranial pressure
increase, cerebral blood
flow velocity, mainly
diastolic, decreases.
● Cerebral circulatory
FIGURE 12-18 arrest is indicated by no
Carbon dioxide vasoreactivity testing. Compared with normocapnia, in hypercapnia the small diastolic flow for at least
resistance vessels dilate, and the blood flow velocity measured proximally at the middle 30 minutes in the middle
cerebral artery increases. The opposite occurs with hypocapnia. cerebral arteries and the
CBFV = cerebral blood flow velocity; ETCO2 = end-tidal carbon dioxide; TCD = transcranial Doppler. basilar artery, and
Reprinted with permission from Castro P and Azevedo E, Neurosonology in Critical Care.48 decreased systolic blood
© 2022 Springer Nature. flow velocity.
● TCD and transcranial

color sonography are highly
about treatment of a carotid stenosis because it might be helpful to understand if accurate ancillary tests for
compensatory vasodilatation is exhausted and determine the stroke risk and cerebral circulatory arrest
urgency of revascularization. A cutoff of the breath-hold index distinguishing confirmation.
between impaired and normal cerebrovascular reactivity was determined
● TCD and a
to be 0.69.50
nontranspulmonary gaseous
When vasomotor reactivity is disturbed or exhausted, a “reversed Robin contrast injection are a
Hood” effect may occur: hypercapnia will cause vasodilatation on the unaffected reliable and less invasive
side but not in the affected one, thus shifting the cerebral blood pool to complement to gold
nonischemic areas.51 standard transesophageal
echocardiography in the
diagnosis of a patent
NEUROVASCULAR COUPLING. Functional TCD is a tool designed to measure the foramen ovale and enable
increase of local cerebral blood flow due to regional cortical neuronal activation the detection of
extracardiac right-to-left
and is accomplished by neurovascular coupling at the neurovascular unit.
shunt.
Dysfunction of neurovascular coupling might occur in the early and
presymptomatic stages of cerebrovascular pathology.52 ● The size of a patent
Functional TCD can also be used to evaluate cerebral laterality, which is foramen ovale measured by
sometimes needed when deciding on a neurosurgical intervention. It is transesophageal
echocardiography
performed by monitoring both middle cerebral arteries while the patient is correlates with the amount
performing a language task, and a significantly higher increase in blood flow of microembolic signals
velocity will be seen in the dominant hemisphere middle cerebral artery. observed by TCD.
Venous Disease
Raised blood flow velocity in collateral venous drainage is the most frequent
sonographic finding in patients with cerebral venous sinus thrombosis.
Interpretation of blood flow velocity in venous ultrasonography must be done
carefully because some physiologic (arachnoid granulations, physiologic

asymmetries) and pathologic conditions (arteriovenous malformations or

dural fistulas) might also contribute to flow increase. Moreover, in
approximately 30% of cases of cerebral venous thrombosis, no pathologic
ultrasound findings can be found.53
Neck ultrasound evaluation of venous outflow might also provide useful
information regarding the insufficiency of the venous system or an obstruction
due to thrombosis. The compression ultrasound maneuver has been shown to be
a highly reliable tool in the diagnosis of internal jugular vein thrombosis.54
NEURO-ORBITAL ULTRASONOGRAPHY
Ultrasonography of the optic nerve sheath diameter and papilla in search for
signs of increased ICP, measurement of pupil reactivity, and the analysis of
orbital vascularization are all potential ultrasonographic applications. This
can be performed with the same probe as for the cervical carotid examination
(linear-array probe of 6 MHz to 12 MHz). The optic nerve serves as a landmark
and is easily detected as a hypoechogenic structure near the distal pole of the
globe with hyperechoic striped bands at its edges (sheath). B-mode ultrasound
markers at the outer edges of the hyperechoic striped bands or at the transitions
from the single dark region to the hyperechoic retrobulbar fat (FIGURE 12-19)
yield the highest sensitivity of optic nerve sheath diameter measurements for
increased ICP.55
The standard point of measurement of the optic nerve sheath diameter
is approximately 3 mm behind the papilla. Normal values for the optic
nerve sheath diameter are 4 to 5 mm. Large discrepancies may be caused
by incorrect positioning of the markers. An increased optic nerve sheath
diameter indicates an increase in ICP. During the same examination, the
clinician can also assess the presence of papilledema, that is, the prominence
of the papilla (FIGURE 12-19), with the normal value of less than 0.5 mm.
In several neurologic conditions, including in neurocritical settings,
pupillometry can be done with
ultrasonography with very
good accuracy.56
Regarding vascular disease
in acute vision loss, in addition
to assessing for a carotid stenosis,
blood flow velocity can be
evaluated in the central retinal
artery running within the optic
nerve. Sometimes it is possible
to identify a calcified embolus
(suggestive of arterial plaque
embolism) lodging in the
central retinal artery just
behind the papilla. This spot
sign correlates with a lower
probability of revascularization,
FIGURE 12-19 spontaneously or with a
Ultrasonography from a patient with chronic
cerebral venous thrombosis with an enlarged
thrombolytic, and a worse
optic nerve sheath and elevated papilla (arrow) prognosis for visual recovery,
suggestive of intracranial hypertension. as exemplified in CASE 12-3.
354 FEBRUARY 2023

Also, evaluation of the orbital vessels may give important clues to vascular KEY POINTS
pathology elsewhere. As discussed earlier, inversion of ophthalmic artery
● Microembolic signal
flow direction suggests a critical cervical internal carotid stenosis. The monitoring is useful in
inversion and arterialization of the flow in the superior ophthalmic vein provide evaluating arterial lesion
clues for a carotid-cavernous fistula in a patient with pulsatile tinnitus, cavernous stroke risk and as a
sinus syndrome, exophthalmos, or chemosis (FIGURE 12-21). surrogate marker of
antithrombotic drug
efficacy.
ULTRASONOGRAPHY OF THE PERIPHERAL NERVOUS SYSTEM
Neuromuscular ultrasonography is an increasingly used application of ultrasound. ● Microembolic signal
It allows the clinician to view most nerves and muscles in real time and to detect monitoring is performed
anomalies through changes in size, echogenicity, and vascularity. It is useful in over 30 to 60 minutes,
usually with bilateral 2-MHz
compressive, demyelinating, and traumatic neuropathies and can quickly and probes fixed in a headframe.
noninvasively assess muscle dysfunction.1
Ultrasonography allows the clinician to evaluate muscles and nerves both in ● Reduced cerebral
static and dynamic conditions, which provides information about pathologic autoregulation is associated
with worse outcome in acute
features and is also important in identifying the structures. stroke and in the
The classic ultrasound finding of affected muscle, resulting from either a neurocritical care setting.
primary neurogenic or myopathic disorder, is increased brightness and reduced
size. Dynamic ultrasonography reveals fasciculations, an important finding in ● Functional TCD studies
may allow identification of
early amyotrophic lateral sclerosis.1
the dominant hemisphere
In carpal tunnel syndrome, as in entrapment neuropathies in general, a and identification of early
hypoechoic focal nerve enlargement occurs either proximal or distal to the site of neurovascular unit
entrapment. dysfunction in
In traumatic neuropathies, ultrasonography is useful in distinguishing cerebrovascular
pathologies.
transected nerves from those with anatomic continuity.
In more generalized neuropathies, ultrasonography might show nerve ● Raised flow velocities in
enlargement, which is useful for detecting hypertrophic hereditary (as in collateral venous drainage
Charcot-Marie-Tooth disease) or inflammatory neuropathies (as in chronic are the most frequent
finding in patients with
inflammatory demyelinating polyradiculoneuropathy and multifocal motor cerebral venous sinus
neuropathy).1 thrombosis, although it has
Ultrasonography can provide real-time guidance for needle placement and can low sensitivity.
sometimes make a diagnosis when electromyography is not tolerated or is no
● Ultrasound evaluation of
longer informative.57
the optic nerve allows for
New technologic advances show promise in the field of neuromuscular detection of signs of
ultrasonopraphy.58 Ultra-high-resolution ultrasonography enables imaging of the increased intracranial
nerve at the fascicular level. Shear wave elastography imaging can provide pressure, namely increased
measures of tissue stiffness that can act as a surrogate measure of nerve and muscle optic nerve sheath diameter
and raised papilla.
health. Photoacoustic imaging may overcome neuromuscular ultrasonography's
current lack of contrast agents to detect inflammation and other functional ● Especially in the
changes within nerve and muscle, while artificial intelligence stands to address neurocritical care setting,
operator dependency and improve diagnostic imaging. ultrasonography can be
useful for the measurement
of pupil reactivity.
ULTRASONOGRAPHY FOR GUIDING PROCEDURES
In addition to the usefulness of ultrasonography to guide safer and faster ● Analysis of orbital
vascular catheterization, especially in the context of neurocritical care, it is also vascularization may provide
evidence of central retina
useful to guide other interventions in neurologic clinical practice.
artery occlusion, which has a
worse prognosis if an
Echo-Guided Lumbar Puncture embolic echogenic spot sign
Lumbar puncture is commonly used as a diagnostic and therapeutic procedure is present.
in neurologic diseases and routinely performed based on landmarks.

Nevertheless, in patients with unfavorable anatomy, such as obesity or

spinal deformities, its success rate decreases. Ultrasound imaging of the
lumbar spine might help guide lumbar puncture by revealing the anatomic
landmarks and select the widest interspinous space, as is shown in
FIGURE 12-22. Previous studies have provided evidence supporting its
59
use for patients with a body mass index of 25 kg/m2 or greater, as well as
in neonates.59,60
Ultrasonography in Headache and Painful Cranial Neuropathies

Minimally invasive techniques such as peripheral nerve blocks may provide pain
relief in headaches refractory to pharmacologic therapy as well as decrease
systemic side effects of pharmacologic therapy. Cranial neuropathies such as
supraorbital, auriculotemporal, or the more common occipital neuropathies
also benefit from peripheral nerve blocks as a diagnostic and treatment
approach. Ultrasound-guided peripheral nerve blocks might allow a more
precise location of the nerve, reducing the anesthetic volumes needed and
avoiding blockage of closer nerves and nonspecific analgesic effects due to
intramuscular spread.61,62
CASE 12-3 A 73-year-old man with hypertension, diabetes, and dyslipidemia

presented to the emergency department with sudden acute vision loss in
his right eye. He also reported chronic mild to moderate headache for
several months. He was diagnosed with acute retinal ischemia and
discharged with aspirin. One month later, he presented again with sudden
visual loss, at that time in his left eye, that had occurred 60 minutes
earlier. Because he did not recover from the previous episode, he had
complete vision loss. The ultrasound examination showed a bilateral
retrobulbar hyperechoic spot signal and absent flow in both central
retinal arteries (FIGURE 12-20). This confirmed the ischemic and embolic
nature of the retinal ischemic events, arguing against an arteritic
etiology. Temporal artery ultrasonography was normal, as was the
sedimentation rate.
COMMENT This case exemplifies that the presence of the hyperechoic embolic
material is a sign of a worse prognosis and of unlikely spontaneous
revascularization and of the importance of a rapid search for the cause of
vision loss, including for an embolic source, to reduce the risk of a
recurrence of ischemic events. This patient was found to have a severe
aortic arch stenosis as the cause of the embolic episodes and did not
recover from blindness at follow-up.
356 FEBRUARY 2023

Ultrasonography in Botulinum Neurotoxin Injection
To improve quality of life, patients with focal dystonia or spasticity are treated
with intramuscular botulinum neurotoxin injections. Several studies show low
accuracy of muscle selection when anatomic landmarks are used.63 To maximize
the efficacy of treatment, an accurate selection of muscles is critical. In this
setting, ultrasonography allows clinicians to unequivocally identify target
muscles for botulinum neurotoxin injection and to better select the site of
administration, which may lead to a more effective treatment and a lower risk of
iatrogenic effects, such as dysphagia.64,65
FUTURE TRENDS
Some new trends, such as ultraportable devices, ultrafast ultrasonography,
ultrasonography perfusion imaging, and cerebral hemodynamic and
vasoregulation studies applied to guiding decisions, as well as the concept of point-
of-care ultrasonography for neurology, are other developing fields of interest.
Ultraportable ultrasonography devices allow more flexible and faster
neurovascular studies, not only at the patient’s bedside but also in other
environments such as the emergency department, the radiography suite, or
FIGURE 12-20
Sequential bilateral loss of vision. A, B, Bilateral retrobulbar spot sign (arrows) and absent
flow in both central retinal arteries. C, D, Preserved flow in ophthalmic arteries.

FIGURE 12-21
Carotid cavernous fistula: “arterialized” (pulsatile flow on right side, arrow) superior
ophthalmic vein (left side, arrow).
FIGURE 12-22
Ultrasound-guided lumbar puncture. A, Transverse view of lumbar spine
ultrasound image. An ultrasound probe was first placed on the lumbar area
perpendicular to the axis of spinous process, with slow movements of the
transducer allowing identification of the spinous processes; it showed the
typical hypoechoic crescent shape of the spinous process with posterior
acoustic shadowing. B, Longitudinal view of lumbar spine ultrasound image.
After locating the spinous process in the center and a mark is drawn, the
transducer was rotated 90 degrees to align the ultrasound beam longitudinally
over the midline and was moved along to find the widest interspinous space:
crescent-shaped structures are identified as the “eyebrow” shape, indicating
spinous processes. Centered between these spinous processes is the
intervertebral space with visible superior and inferior borders.
Reprinted with permission from Li Y, et al, Neurol Clin Pract.59 © 2020 American Academy
of Neurology.
358 FEBRUARY 2023

even in the ambulance. Point-of-care ultrasonography is a goal-directed and
-focused ultrasound examination performed where the patient is being
observed and treated, to obtain in real time a prompt answer to a specific
clinical question related to neurologic symptoms, or for supporting
procedures (eg, image-guidance).66
Ultrasonic cerebral perfusion imaging permits improved vessel imaging and
contrast-enhanced tissue imaging. Studies performed in a stroke setting allow
following up brain perfusion status and effect of recanalization therapeutics.
Trials such as the ongoing SONAS Ultrasound for Detecting Stroke,67 which uses
a portable ultrasound machine and a semiquantitative algorithm to detect a large
vessel occlusion in a prehospital setting, may expand the application of these
procedures into clinical practice. Moreover, ultrasonic cerebral perfusion
imaging might help delineate the border of intracerebral hemorrhage for more
valid volume measurement.
Ultrafast ultrasonography enables transcranial imaging of deep vasculature
in the adult brain at microscopic resolution and the quantification of
hemodynamic parameters. It will facilitate the understanding of brain
hemodynamics and how vascular abnormalities in the brain are related to
neurologic pathologies.68 New ultrasonography cerebral hemodynamic and
vasoregulation studies are promising for guiding clinical decisions, as in the acute
stroke setting, as well as in the noninvasive assessment of ICP.46,47,69
CONCLUSION
Diagnostic ultrasonography in neurology enables the physician to better
understand a clinical case using a noninvasive and accurate tool that can be used
at a patient’s bedside.
Neurovascular ultrasonography provides morphologic and hemodynamic
information, complementing data from CT or MRI. As ultrasonography
examinations can be easily repeated, they are ideal for monitoring an unstable
patient or during and after interventions. Recently, brain and eye sonography
have added new applications, namely for ICP assessment.
Diagnostic ultrasonography can be a powerful tool for morbidity and
mortality prevention. In adults, it allows early detection of atherosclerosis and
the opportunity to prevent progression to stroke with timely aggressive control
of vascular risk factors. In children with sickle cell disease, it is important to have
access to TCD screening to select patients for transfusion and reduce the risk of
stroke. In conclusion, diagnostic ultrasonography helps neurologists provide
select patients better and more timely treatment.
USEFUL WEBSITES
THE AMERICAN SOCIETY OF NEUROIMAGING EUROPEAN SOCIETY OF NEUROSONOLOGY AND
The mission of the American Society of CEREBRAL HEMODYNAMICS
Neuroimaging is to provide neuroimaging The European Society of Neurosonology and
informatics education, certification, support, and Cerebral Hemodynamics brings together the
guidance to neurologists and other neuroscience professionals most dedicated to the use of
clinicians, technologists, sonographers, and ultrasound in neurology and is very active in the
researchers. It aims to ensure all individuals with dissemination of neurosonology, in the certification
neurologic disorders have access to experts in of professionals, in the constitution of study groups
neuroimaging and neurosonology. and multicenter initiatives to promote the practice,
asnweb.org and teaching and research in the area.
esnch.org/

VIDEO LEGENDS
VIDEO 12-1 VIDEO 12-3
Video shows a common carotid artery dissection as Video shows microembolic signals in a patient with
an extension of aortic dissection. The intimal flap of a patent foramen ovale. While monitoring middle
the dissection is visible as an echogenic (white) cerebral artery (red area in the video) blood flow
linear moving image within the artery in a velocity (bottom), a nontranspulmonary
longitudinal view of the proximal common carotid microbubble solution was injected into an arm vein.
artery. At 12 seconds, microembolic signals are visible in
ACC prox. Direito = right proximal common the velocity spectrum as high-intensity signals;
carotid artery. simultaneous typical “blip” sounds are heard.
Between 18 and 28 seconds, the patient is doing a
© 2023 American Academy of Neurology. Valsalva maneuver, which is reflected in a decrease
in blood flow velocity in the spectrum, and some
VIDEO 12-2 more microembolic signals follow.
Video shows a common carotid artery dissection © 2023 American Academy of Neurology.
as an extension of aortic dissection. The intimal
flap of the dissection is visible as an echogenic
(white) linear moving image within the artery,
in a cross-sectional view of the proximal common
carotid artery.
© 2023 American Academy of Neurology.
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LATEST DEVELOPMENTS: Diagnostic ultrasonography is expanding its

© 2023 American Academy

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GENERAL TECHNICAL REQUIREMENTS FOR NEUROSONOLOGY

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TABLE 12-1 Main Applications of Neurosonology

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MAIN APPLICATIONS OF NEUROSONOLOGY

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KEY POINTS NEUROVASCULAR ULTRASONOGRAPHY

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Questions That May be Addressed by Neurosonology in the Setting of TABLE 12-2

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A higher degree of stenosis is related to both mechanisms, whereas unstable

TABLE 12-3 Criteria to Define Degree of Stenosis in Internal Carotid Atherosclerotic

Degree of stenosis as defined by NASCET (the North American Symptomatic Carotid

1 B-mode image, diameter Applicable Possibly Imaging of

3 PSV threshold, 125 230 NA NA

4a PSV average, cm/s ≤160 210 240 330 370 Variable NA

4b PSV poststenotic, cm/s ≥50 <50 <30 NA

5 Collateral flow Possible Present Present Present

6 Prestenotic flow Possibly Reduced Reduced Reduced

7 Poststenotic flow Moderate Pronounced Pronounced Pronounced Variable NA

8 End-diastolic flow <100 >100 Variable NA

9 Carotid ratio <2 ≥2 ≥2 >4 >4 Variable NA

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TRANSIENT PERIVASCULAR INFLAMMATION OF THE CAROTID ARTERY AND MURAL

FIBROMUSCULAR DYSPLASIA AND CAROTID WEB. Fibromuscular dysplasia is a rare,

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334 FEBRUARY 2023

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This case exemplifies how useful a noninvasive ultrasound cerebrovascular COMMENT

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resulting in arterial stenosis, occlusion, aneurysm, or dissection. It most

336 FEBRUARY 2023

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● Carotid webs are

Carotid webs, shown in FIGURE 12-10, are rare variants of fibromuscular

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gold standard examination. Meticulous sonographic technique, appropriate

ARTERIOVENOUS SHUNTS. Doppler ultrasonography can reveal signs of

Intracranial Neurovascular Ultrasonography

COMPENSATORY INTRACRANIAL COLLATERAL CIRCUITS OF PROXIMAL STENO-

Anatomic region Cutoff intima-media thickness, mm

Frontal branch of TA 0.34

Parietal branch of TA 0.29

Axillary artery 1.0

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● When the external carotid

● The thrombolysis in brain

of the external carotid artery, an inversion of flow direction in the A1 segment

THROMBOLYSIS IN BRAIN ISCHEMIA SCORE. In the setting of hyperacute ischemic

INTRACRANIAL STENOSIS. Intracranial stenosis is detected by a focal

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