N e u ro - u l t r a s o n o g r a p h y

Ryan Hakimi, DO, MS, FNCS, NVSa,*, Andrei V. Alexandrov, MD, RVT
b
,
Zsolt Garami, MDc,d

KEYWORDS
 TCD  Transcranial Doppler ultrasonography  Vasospasm  Neurosonology
 Subarachnoid hemorrhage  Neurocritical care  Optic nerve sheath diameter
 Emboli detection

KEY POINTS
 Transcranial Doppler ultrasonography (TCD) is a noninvasive, bedside, portable tool for
assessment of cerebral hemodynamics and detection of focal stenosis, arterial occlusion,
monitoring the treatment effect of intravenous tissue plasminogen activator and assess-
ment of vasomotor reactivity.
 Modern TCD head frames allow continuous hands-free emboli detection, allowing risk
stratification and assessment of treatment efficacy in several cardiovascular disease
processes.
 TCD is an excellent screening tool for vasospasm in aneurysmal subarachnoid hemor-
rhage because of its high sensitivity and negative predictive value.
 The use of intraoperative TCD during carotid endarterectomy and stenting allows optimal
intraoperative hemodynamic management while minimizing the risk for brain ischemia.

TRANSCRANIAL POWER MOTION DOPPLER AND SPECTRAL DISPLAY

Transcranial Doppler ultrasonography (TCD) is a noninvasive, portable, bedside tool

for assessment of cerebral hemodynamics (Box 1). The instrument displays spectral
waveforms that represent the depth, direction, and intensity of the blood flow through
the intracranial vasculature. Although the instrument does not measure blood flow
directly, the parameters that it does calculate do correlate with cerebral blood flow
(CBF).
In the past, TCD machines were only able to display a spectral waveform. The oper-
ator was left to deduce which vessel was being insonated by attempting to obtain the

a
Director, Neuro ICU, Inpatient Neurology, and TCD Services, Greenville Memorial Hospital,
Prisma Health-Upstate, University of South Carolina School of Medicine-Greenville, 200 Pate-
wood Drive, Suite B350, Greenville, SC 29615, USA; b Department of Neurology, The University
of Tennessee Health Science Center, 855 Monroe Avenue, Suite 415, Memphis, TN 38163, USA;
c
Institute for Academic Medicine, Research Institute, Houston, TX, USA; d Vascular Ultrasound
Laboratory, Houston Methodist Hospital, Weill Cornell Medical College, 6550 Fannin Street,
Suite 1401, Houston, TX 77030, USA
* Corresponding author.
E-mail address: [email protected]

Neurol Clin 38 (2020) 215–229

https://doi.org/10.1016/j.ncl.2019.09.006 neurologic.theclinics.com
0733-8619/20/ª 2019 Elsevier Inc. All rights reserved.
216 Hakimi et al

Box 1
Transcranial Doppler ultrasonography parameters

PSV (peak systolic velocity)

EDV (end diastolic velocity)
MFV (mean flow velocity) 5 1/3 PSV 1 2/3 EDV
Pulsatility index 5 (PSV EDV)/MFV
Resistivity index 5 (PSV EDV)/PSV
Lindegaard ratio 5 (MFV of middle cerebral artery)/MFV of ipsilateral extracranial internal
carotid artery

same waveform or an inverted version of the same waveform using a variety of

different approaches, termed windows, at different depths. With the addition of power
motion–mode Doppler (PMD), sonographers are able to obtain the spectral waveform
as well as knowing the depth of the insonated vessel, the direction of flow relative to
the probe, and the intensity of the signal (Box 2, Figs. 1 and 2).

Fig. 1. Normal TCD signals on Power M Mode screen: middle cerebral artery (MCA) (red: 40–
60 mm), anterior cerebral artery (ACA) (blue: 60–70 mm), contralateral ACA (red: 70–80
mm), and Contralateral MCA (blue: 80–90 mm). (From Garami Z, Alexandrov AV. Neuroso-
nology. Neurol Clin. 2009;27(1):89–108; with permission).

The temporal bone is the thinnest portion of the human skull and is located imme-
diately superior to the tragus. A 2-MHz TCD probe is placed at this location and the
intracranial arteries are insonated to produce the aforementioned spectral wave-
forms and physiologic parameters. The skin surface where the probe contacts the
head serves as the zero depth and distances are measured from that point onward.
For most adults the midline lies at approximately 70 to 80 mm. At deeper depths the
contralateral vasculature is insonated, whose spectral waveforms would be
expected to have the opposite direction of that obtained when imaged from the ipsi-
lateral side.
 Neuro-ultrasonography 217

Fig. 2. Doppler velocity.

Box 2
Criteria for identification of a focal stenosis

Waveform after the area of stenosis shows delayed systolic upstroke relative to the waveform
proximal to the stenosis, and:
Poststenotic MFV is greater than 100 cm/s and is 2 times the prestenotic MFV, or
Poststenotic MFV is greater than 100 cm/s and is 2 times the MFV of the contralateral
homologous segment

EMBOLI DETECTION AND MONITORING

TCD can be used for microemboli detection. Modern TCD manufacturers have
created adjustable head frames allowing the operator to affix up to 2 TCD probes to
insonate vessels bilaterally, most commonly the middle cerebral arteries (MCAs), in
a hands-free fashion. However, operators can increase the gait to allow each probe
to insonate multiple vessels at the same time. Such technology has a vast number
of applications, including risk stratification of carotid artery dissection, risk stratifica-
tion of asymptomatic carotid stenosis,1 monitoring the effect of tissue plasminogen
activator (tPA) on an acutely occluded vessel, assessing the efficacy of anticoagula-
tion in nonvalvular atrial fibrillation,2 and risk stratifying moderate carotid artery
stenosis.

INTRACRANIAL STENOSIS AND DETECTION OF FOCAL ARTERIAL OCCLUSION

TCD can detect and grade the severity of intracranial stenosis from acute throm-
bosis, intracranial dissection, or focal intracranial atherosclerosis. Although a variety
of mean flow velocity (MFV) criteria have been used to make this assessment, the
authors suggest a multistep approach, beginning by looking at the waveform
morphology and MFV of the Doppler signal before and after the area of stenosis
and then comparing the MFV with the contralateral homologous segment (see
Box 2; Fig. 3).
Thrombolysis in brain ischemia classification has been created to describe residual
flow or to monitor clot dissolution.3 Such a classification allows better communication
between providers about the extent of revascularization and can be used to determine
the optimal systemic blood pressure in post-tPA and mechanical thrombectomy pa-
tients, and detection of reocclusion, particularly in patients under general anesthesia
(Fig. 4).
218 Hakimi et al

Fig. 3. Waveform morphology and MFV of the Doppler signal before (LMCA at 78 mm) and
after (LMCA at 50 mm) the area of stenosis (red arrow), then comparing the MFV with the
contralateral homologous segment (RMCA at 54 mm).

Fig. 4. Detection of reocclusion, particularly in patients under general anesthesia. (From Ga-
rami Z, Alexandrov AV. Neurosonology. Neurol Clin. 2009; 27(1):89-108; with permission.)
 Neuro-ultrasonography 219

CEREBRAL ARTERY VASOSPASM

Cerebral artery vasospasm, a reduction in the caliber of a cerebral artery, is a com-

mon consequence of aneurysmal subarachnoid hemorrhage (aSAH). Even now,
aSAH portends a 50% mortality, chiefly caused by delayed cerebral ischemia
(DCI). DCI can be prevented by identifying and appropriately treating vasospasm,
which occurs in 50% to 70% of aSAH cases.4–6 TCD can predict symptomatic
vasospasm and has high sensitivity, specificity, positive and negative predictive
values.7–11 Three major neurologic bodies endorse the use of TCD in the care of
patients with aSAH, namely the American Heart Association/American Stroke Asso-
ciation (AHA/ASA), the American Academy of Neurology (AAN), and the Neurocrit-
ical Care Society (NCS). The AHA/ASA designates the use of TCD in aSAH as class
IIA/level B evidence, whereas the other 2 entities designate it as moderate-quality
evidence/strong recommendation. The largest meta-analysis to date, by Kumar
and colleagues,12 reviews the use of TCD for aSAH in 17 pooled studies (2870 pa-
tients). They reported TCD evidence of vasospasm to be highly predictive of DCI,
with a sensitivity of 90%, specificity of 71%, positive predictive value of 57%,
and negative predictive value of 92%. The excellent sensitivity and high negative
predictive value makes TCD an ideal screening tool for detecting vasospasm in
aSAH.
In general, TCD is less reliable at identifying posterior circulation than anterior circu-
lation vasospasm (because of greater anatomic variance). There are multiple pub-
lished criteria for anterior circulation vasospasm. One often used set of criteria is
shown in Table 1.
Given that each individual’s baseline anatomic and physiologic parameters are
different, identification of vasospasm is improved by performing daily TCD and
trending the MFV, because the trends and waveform morphology are often more
valuable than simply the numerical values. For example, an increase in the MFV
of 50 cm/s or greater in a vessel between one day and the next is suggestive of
vasospasm even if the MFV is less than 120 cm/s. Therefore, it is optimal to obtain
a daily TCD, including on the day of presentation, to establish a baseline and to
monitor for trends suggesting vasospasm, thereby allowing prompt treatment
and prevention of DCI (Figs. 5 and 6).
Ideally, every TCD laboratory should be accredited by the Intersocietal Accredita-
tion Commission (IAC), or an equivalent body, and every sonographer should be certi-
fied by the American Society of Neuroimaging (ASN), American Registry for Diagnostic
Medical Sonography (ARDMS), or an equivalent body to ensure diagnostic accuracy
and optimal patient care.

Table 1
Criteria for vasospasm

Mild vasospasm 120–160 cm/s Lindegaard ratio (MCA velocity/extracranial ICA) 3–4
Moderate vasospasm 160–200 cm/s Lindegaard ratio (MCA velocity/extracranial ICA) 4–6
Severe vasospasm >200 cm/s Lindegaard ratio (MCA velocity/extracranial ICA) >6

Abbreviation: ICA, internal carotid artery.

SUBCLAVIAN STEAL

Side-to-side blood pressure variance of 20 mm Hg or more is often the first sign of

subclinical subclavian steal.13 Such patients often have global atherosclerosis,
220

Fig. 5. Daily TCD. (From Garami Z, Alexandrov AV. Neurosonology. Neurol Clin. 2009;
27(1):89-108; with permission.)

Fig. 6. Velocity trend report. LICA-EC, extracranial left ICA; RICA-EC, extracranial right ICA;
LMCA, left MCA; RMCA, right MCA.
 Neuro-ultrasonography 221

including the proximal subclavian artery. This condition results in varying degrees of
retrograde flow within the ipsilateral vertebral artery, limiting perfusion of the ipsilateral
arm. Symptomatic subclavian steal manifests as paroxysmal vertigo, syncope, and
ipsilateral arm claudication.
TCD serves as an excellent screening tool for such patients.14 Although reported,
complete reversal of vertebral artery blood flow at rest is uncommon. Therefore, in or-
der to make the diagnosis, an ischemic cuff test is performed wherein the cuff is
inflated to 20 mm Hg greater than the patient’s own systolic blood pressure and main-
tained for a few minutes. This pressure renders the arm ischemic. During this process
the ipsilateral vertebral artery is insonated. The cuff is then rapidly deflated, resulting in
rapid reperfusion of the arm and varying degrees of reversal of flow in the ipsilateral
vertebral artery confirming the diagnosis of subclavian steal syndrome. Most
commonly these patients are treated with medical therapy. In some more advanced
cases, subclavian artery stenting is required13 (Figs. 7–9).

Fig. 7. Alternating flow signal in the vertebral artery (VA). PMD display: on the yellow line,
red color signal, steal direction/toward the probe in systole; blue, away (normal direction) in
diastole. Spectral display: negative and positive waveforms corresponding with direction
changes.

Fig. 8. Abnormal waveform in the VA indicates subclavian steal phenomenon. V-shaped

cutout is the first form of the alternating flow signal. (From Garami Z, Alexandrov AV. Neu-
rosonology. Neurol Clin. 2009; 27(1):89-108; with permission.)
222 Hakimi et al

Fig. 9. Hyperemia test: overinflated blood pressure cuff released, flow reversal (red signal)
in the vertebral-basilar system, and various waveforms returned to baseline (spectral
display).

CEREBRAL CIRCULATORY ARREST

Brain death, also termed death by neurologic criteria, is the irreversible cessation of
whole-brain function with sustained systemic perfusion caused by support of me-
chanical ventilation, medications, and various medical measures. This support was
not possible until the development of mechanical ventilation and the advancement
of critical care techniques, allowing patients to be systemically stable after developing
cessation of brain function. Brain death remains a clinical diagnosis requiring a variety
of clinical, laboratory, and respiratory criteria to be met.15 However, in some instances,
the patient is clinically unstable and cannot meet all of the necessary criteria, and thus
an ancillary test is needed. The AAN only endorses 3 ancillary tests with level B or
higher designation. TCD is one such test with level A evidence for use as an ancillary
test for determination of brain death.
Bilateral insonation of the anterior and posterior circulation is performed through
the temporal and suboccipital windows, showing reverberating flow or small sys-
tolic spikes. Absence of flow can only be used as a marker for cerebral circulatory
arrest if an acoustic signal that had previously been obtained in the same patient is
now absent. This finding distinguishes cerebral circulatory arrest from technical is-
sues, such as absence of windows seen with hyperostosis of the skull (Fig. 10).

Fig. 10. TCD waveform progression from normal MCA to cerebral circulatory arrest. (Cour-
tesy of A. Razumovsky, PhD.)

VASOMOTOR REACTIVITY

Vasomotor reactivity can be assessed using a variety of means, including CO2 reac-
tivity testing with TCD, acetazolamide testing with TCD, and the breath-holding index
(BHI).16,17 The first 2 modalities require a special gas hookup and an intravenous (IV)
 Neuro-ultrasonography 223

medication, respectively. However, the last modality can easily be performed in an

outpatient setting provided that the patient is capable of breath holding for 30 seconds.
To begin, patients are instructed to hold their breath for 30 seconds and the MFV of the
MCA is measured. The MFV is again measured 4 seconds after the breath hold when
the patient is allowed to breath. For a breath hold of 30 seconds, the following formula
is used to calculate the BHI:

BHI 5 3.33  (MFVend MFVbaseline)/MFVbaseline

Vasomotor reactivity has a variety of applications, including determining the risk for
ischemic stroke in individuals with severe asymptomatic carotid artery stenosis or
intracranial stenosis, in particular in those with a BHI of less than 0.69.18 The presence
of impaired vasomotor reactivity has also been suggested in individuals following a
concussion or those with Alzheimer dementia.19
Vasomotor reactivity testing with TCD can also detect paradoxic MFV reduction dur-
ing increase in CO2 levels. This intracranial steal phenomenon, termed reversed Robin
Hood, can lead to neurologic deterioration and high risk of early stroke recurrence.20,21

REAL-TIME PROCEDURAL MONITORING

Neurologic complications of carotid endarterectomy (CEA) and carotid artery stenting

(CAS) are commonly related to cerebral hypoperfusion, cerebral hyperperfusion, or
most often thrombosis and embolization.22–26 Real-time detection of such events
with TCD monitoring is critical to prevent, diagnose, and reverse procedure-related
complications. By monitoring the bilateral MCAs, TCD is the only modality that mon-
itors the intracranial vessels to prevent end-organ damage. Intraoperative TCD allows
direct visualization of the patient’s intracranial collateral flow, giving patient-specific
information to the surgeon performing the CEA. This technique allows surgeons to
perform vascular shunting only when necessary, thereby preventing unnecessary
complications. By monitoring the amplitude of the diastolic component of the Doppler
waveform to ensure that it is approximately half of the peak systolic amplitude, intra-
operative TCD also allows anesthesiologists the patient-specific information needed
to augment or reduce patients’ blood pressure during CEA or CAS to prevent cerebral
hypoperfusion and hyperperfusion. The lack of global acceptance of this practice cen-
ters on the lack of lucrative reimbursement for this outcome-changing modality (Figs.
11 and 12).

OPTIC NERVE SHEATH DIAMETER

Bedside ocular ultrasonography can identify foreign bodies, globe rupture, retinal
detachment, and increased intracranial pressure (ICP) as shown by an increased optic
nerve sheath diameter.27 In order to measure optic nerve sheath diameter, a 7.5-MHz
to 10-MHz linear array transducer is placed on the patient’s closed eye after applying a
copious amount of ultrasonography gel. The optic nerve sheath is marked 3 mm
behind the posterior aspect of the eye. Two measurements of the transverse diameter
of the optic nerve sheath are then obtained at this position. The 2 values are then aver-
aged. If they exceed 5 mm, it is supportive of increased ICP28 (Fig. 13).
In a recent large meta-analysis, Robba and colleagues29 concluded that optic nerve
sheath diameter may be a useful surrogate for increased ICP when standard invasive
monitors are not available or indicated. The investigators noted marked heterogeneity
in the publications, including variability in the units of ICP measurement and cut points
for high ICP.
224 Hakimi et al

Fig. 11. (A) Bilateral MCA monitoring was performed during left carotid endarterectomy.
Clamp placement produced blunted signals in both MCAs. Indirect evidence for bilateral dis-
ease clamped carotid feeding the other MCA. (B) Clamp released, producing microembolic
signals in both MCAs. Pulsatility restored in the MCA bilaterally. (From Garami Z, Alexandrov
AV. Neurosonology. Neurol Clin. 2009; 27(1):89-108; with permission.)
 Neuro-ultrasonography 225

Fig. 12. Bilateral MCA monitoring during right CAS. Stent placement resulted in Micro-
embolic signals (MES) only in the ipsilateral MCA. (From Garami Z, Alexandrov AV. Neuroso-
nology. Neurol Clin. 2009; 27(1):89-108; with permission.)

Fig. 13. Two measurements of the transverse diameter of the optic nerve sheath are
obtained.

NEUROCRITICAL CARE APPLICATIONS OF BRAIN ULTRASONOGRAPHY

The use of TCD in neurocritical care units continues to grow, and regulatory bodies are
beginning to mandate its availability in order for institutions to obtain the highest-level
designations, such as level 1 neurointensive care unit (neuro-ICU) and comprehensive
stroke center.30,31 The increasing availability of TCD has led to use outside of standard
vasospasm monitoring for aSAH.
Optimization of CBF and oxygen delivery are the goals of neurologic manage-
ment of patients with traumatic brain injury. Historically, this has been monitored
by measuring ICP and monitoring cerebral perfusion pressure (CPP). However,
this model is inadequate because some patients have poor neurologic outcomes
despite appropriate management of these two parameters. Among noninvasive
modalities, TCD is the most accurate tool for measuring brain perfusion at the
bedside.32
 226
Hakimi et al
Fig. 14. TCD can non-invasively monitor cerebral perfusion by assessing the diastolic component of the spectral waveform (EDV). Left panel shows high
resistance waveforms with EDV less than 50% of the PSV. The patient then had an external ventricular drain placed (right panel) and the pulsatility
indices normalized resulting in an increase in the diastolic component of the waveform such that the EDV is greater than 50% of the PSV.
 Neuro-ultrasonography 227

The brain’s cerebral perfusion is maintained in both systole and diastole, as

shown by the systolic and diastolic component of the TCD waveform. In contrast,
the hand is perfused only in systole, as shown by a radial arterial line waveform.
This difference is caused by the marked difference in resistance, with the brain be-
ing a low-resistance system and the hand being a high-resistance system, as well
as the higher energy requirements of the brain compared with the hand. Therefore,
the adequacy of CBF can be assessed by evaluating the diastolic component of the
TCD waveform and ensuring that its amplitude is approximately half of the peak
systolic amplitude. If it is less, the clinician can: a) increase the patient’s blood
pressure using IV fluids, vasopressors, or by giving a blood transfusion; b) decrease
the PaCO2 by decreasing the respiratory rate on the ventilator (with intubated pa-
tients) or increasing the patient’s sedation; c) reducing the patient’s ICP by cere-
brospinal fluid diversion, increasing sedation, or treating the patient’s fever,
among other means (Fig. 14).
Insonation of the anterior cerebral arteries (ACAs) can be a challenge in neuro-ICU
patients because of cerebral edema, recent surgery, or intracranial mass lesions.
Frontal bone TCD has previously been described in the pediatric neurology and neuro-
radiology literature as an alternative window for insonating the ACAs and is a newly
described modality for neuro-ICU patients.33–38
Hemicraniectomy affords sonographers an excellent window for intracranial imag-
ing. Transporting such patients to the computed tomography (CT) suite poses obvious
safety risks to the patients. Serial monitoring of a patient’s subdural hematoma and
postoperative hygroma can be achieved using a broadband sector array transducer
with a 4-MHz to 2-MHz operating frequency range.39 Bedside ultrasonography also
spares the patients radiation exposure and added cost (Fig. 15).

Fig. 15. Axial views of the initial (A) noncontrast CT scan of the head; (B) ultrasonography
(C, zoomed to show detail) with follow-up; (D) noncontrast CT scan of the head; and (E) ul-
trasonography. The CT scans show the right-sided subdural hygroma (white arrows), which
corresponds to the near-contemporaneous ultrasonography views of the hygroma
(measured by the white plus [1] icons on the ultrasonography images). (F) Ultrasonography
settings used to obtain images.
228 Hakimi et al

DISCLOSURE

Dr R. Hakimi has nothing to disclose. Dr Z. Garami has nothing to disclose. Dr A.V.

Alexandrov has received consulting fees from Cerevast Inc and is on the speaker’s bu-
reau for Genentech.

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