Ultrasonography has become one of the basic diagnostic tools for vascular diseases of the central nervous system (CNS). Due to the widespread availability of ultrasound, it seems necessary to define standards for equipment requirements, the scope of ultrasound and the experience of the person performing the procedure. The goal of this paper is to standardize the testing protocol in all neurosonology laboratories. We hope that the presented standards will prove useful in everyday patient management as well as will become the basis for discussion and comments to be taken into account in subsequent versions. The paper further describes different types of neurosonological tests, such as those used in the diagnosis of the cerebral circulatory arrest or right-to-left shunts.
The proposed diagnostic criteria should be standardized in all neurosonology laboratories due to differences between ultrasonographic devices, particularly in relation to velocity calibration.
Vasospasm secondary to subarachnoid hemorrhage
The examination should be performed using 4 MHz continuous-wave Doppler (CW) (‘blind’ Doppler) and 2 MHz pulsed-wave Doppler (TCD) or an ultrasound with a linear 7.5–13 MHz probe and 2–2.5 MHz sector probe (TCCD). The ALARA (as low as reasonably achievable) principle, i.e. the lowest intensity of ultrasounds for optimal image of structures and flow in possibly the shortest time, is applied.
The test is performed in a patient lying in supine position.
The scanning is performed in a standard manner, as described in the section TCD of the extracranial segments of the cerebral arteries, in the first part of the paper (J Ultrason 2015; 15: 307–317).
Examination of the extracranial segments of the intracerebral arteries is necessary to distinguish between vasospasm and a potential hyperemia.
The scanning should be performed within the first two days after bleeding (as a baseline examination). This should be followed by arterial blood flow velocity monitoring performed at least once every 3 days(1).
The images (mainly spectral Doppler) of the flow in the extracranial internal carotid and vertebral arteries; middle, anterior and posterior cerebral arteries; as well as vertebral arteries and the basilar artery, should be recorded.
The results should contain the type of the method applied (TCD or TCCD), the name of the device, probe frequency, the list of evaluated arteries or a statement that the test was performed according to standard protocol. It is necessary to specify the day (if known) after of the onset of bleeding. This should be followed by the outcomes of the measurement of the average flow velocity in the middle, anterior and posterior cerebral arteries, the vertebral arteries and the basilar artery, as well as the Lindegaard Index (or, optionally, the basilar index). The description should include a statement on the presence of vasospasm and, if present, specify the vessel and the risk of symptomatic vasospasm. In the case of difficulty differentiating between vasospasm and hyperemia, further diagnostic testing, e.g. perfusion CT scan, should be suggested(1–3).
We suggest the following criteria for the diagnosis of vasospasm (assuming that extracranial cerebral arterial stenosis is excluded):
Borderline criteria for the diagnosis of vasospasm in the M1 segment of the middle cerebral artery:
The risk of symptomatic vasospasm in the middle cerebral artery(1, 3, 4):
Criteria for the diagnosis of vasospasm in the other arteries at the base of the brain(1, 4):
or arbitrary velocities set for each of the arteries:
anterior cerebral artery vasospasm: mean velocity >120–140 cm/s;
vertebral or basilar artery vasospasm: mean velocity >70 cm/s in patients aged <55 years and >55 cm/s in patients aged ≥55 years;
posterior cerebral artery vasospasm: mean velocity >110 cm/s in patients aged <55 years and >80 cm/s in patients aged ≥55 years.
Monitoring in the acute phase of stroke
The examination is performed using 4 MHz continuous-wave Doppler (‘blind’ Doppler) and 2 MHz pulsed-wave Doppler (TCD) or an ultrasound with a linear 7.5–13 MHz probe and 2–3.5 MHz sector probe (TCCD).
The test is performed in a patient lying in supine position.
The ‘short path’ protocol was developed for a rapid identification of the site of stenosis or obstruction in the acute phase of stroke as well as to determine the extent of the maintained residual flow. Depending on the time at investigator's disposal, further testing steps are performed, beginning from the affected (symptomatic) side. Ultrasound imaging in the acute phase of stroke is used as a complementary testing technique – it should not be the reason for the delay in thrombolytic therapy initiation. During thrombolysis, scanning is usually performed several times to monitor the duration and the extent of recanalization or reocclusion.
If time permits, the examination is performed in accordance with the standard protocol(1, 5).
Clinical suspicion of cerebral ischemia in the anterior circulation(5)
Transcranial Doppler Ultrasound
If time permits, insonation should begin on the asymptomatic (non-affected) side to establish the temporal window, normal MCA waveform (M1 depth 45–65 mm, M2 30–45 mm) and velocity for comparison with the affected side.
If short of time, the examination should be initiated on the symptomatic (affected) side: first, the MCA at 50 mm should be assessed. If no signals are detected, the depth is increased to 62 mm. If an anterograde flow signal is detected, the depth is reduced to trace the MCA stem or identify the poorest residual flow signal. Potential flow diversion to ACA, PCA or M2 MCA should be found. Waveform shapes and systolic flow acceleration should be evaluated and compared.
The imaging should be continued on the affected side (transorbital window). Flow direction and pulsatility in the OA at a depth of 40–50 mm should be checked, followed by the evaluation of ICA siphon at a depth of 55–65 mm.
If time permits or in patients with purely motor or sensory deficits, BA (depth 80–> 100 mm) and terminal VA (40–80 mm) should be evaluated.
Carotid/vertebral duplex Doppler
The scanning should begin on the affected side in transverse B-mode planes, followed by color- or power Doppler from proximal to distal carotid segments. CAA and its bifurcation should be assessed on B-mode and flow-carrying lumens.
It should be documented if ICA (or CCA) has lesions visible in the B-mode image and corresponding disturbances on flow mages. In patients with concomitant chest pain, CCA as close to its branching from the aortic arch as possible, should be assessed.
Velocity measurements in the mid-to-distal CAA, ICA and ECA should be performed.
If time permits or in patients with purely motor or sensory deficits, cervical portion of the vertebral arteries should be assessed (longitudinal B-mode, color or power mode and spectral Doppler) on the affected side.
If time permits, transverse and longitudinal scanning of the arteries on the non-affected side should be performed.
Clinical suspicion of cerebral ischemia in the posterior circulation(5)
Transcranial Doppler Ultrasound
The scanning should begin with suboccipital insonation at a depth of 74 mm (VA junction) and the identification of BA flow at a depth of 80–100 mm or more.
If abnormal signals are present at 75–100 mm, the terminal VA on the non-affected side should be identified for comparison and evaluation of the terminal VA on the affected side at similar depth.
The scanning is continued through the transtemporal window to identify PCA (55–75 mm) and possible collateral flow through the posterior communicating artery (both sides should be evaluated).
If time permits, both MCA and ACA (60–75 mm) should be evaluated to identify possible compensatory velocity increase as an indirect sign of basilar artery obstruction.
Vertebral/carotid duplex Doppler Ultrasound
The scanning should be initiated on the affected side by locating CAA using longitudinal B-mode, followed by visualization of shadows of the transverse processes in the mid-cervical part.
Color or power mode and spectral Doppler should be used to identify flow in the intratransverse VA segments.
VA course should be followed from its branching from the subclavian artery and Doppler spectra should be recorded. Similar examination should be performed on the other side.
If time permits, bilateral duplex scanning of the CCA, ICA and ECA should be performed.
Flow images and Doppler spectra in the subsequently evaluated arteries should be documented.
The result should contain the type of method (TCD or TCCD, Doppler or duplex scanning of the intracerebral arteries), the name of the apparatus, probe frequency, the list of arteries evaluated in accordance with the ‘short path’ protocol or a statement that the examination was performed according to the standard protocol. In addition to basic data, which should be included in the description of the examination (discussed above in the section on the extracranial arteries and transcranial ‘blind’ or duplex Doppler), the description should further include certain specific elements(4).
If arterial obstruction or stenosis is identified, its location and the TIBI (thrombolysis in brain ischemia) classification of residual flow should be documented(1):
In the case of obstruction or stenosis in the extracranial portion of the intracerebral artery, the routes of collateral circulation should be identified(1, 4).
When monitoring spontaneous recanalization or during thrombolysis, time to and grade of recanalization obtained (TIBI classification) should be documented(1).
Detection of direct right to left shunt
Under normal conditions, injection if gas bubbles larger than 10 microns into the peripheral vein results in their uptake by the pulmonary circulation.
In the case of direct right to left shunt (RLS), e.g. a patent foramen ovale, administration of specific ultrasonography contrast agent in the form of larger gas bubbles (unstable) will result in their direct passage into systemic circulation, including cerebral vasculature, and inducing cerebral microembolic signals. The signals are characterized by short duration (<300 ms) and high intensity (>3 dB above the spectral background signal), random occurrence of velocity in the spectrum and unidirectional course (always in the direction of the flow in the vessel). Their formation is accompanied by a characteristic high-frequency sound(2). The number of signals recorded in the cerebral artery following contrast agent administration determines the grade of the shunt. Right to left shunts can be intracardiac (patent foramen ovale, interatrial septum defects) or intra-pulmonary (pulmonary artery fistula). Ultrasound does not allow a precise localization of shunt(1, 3, 4).
The examination is performed using 2 MHz ‘blind’ pulsed Doppler. The use of a monitoring head band facilitates the examination. The sensitivity may be increased by simultaneous bilateral monitoring, i.e. dual-channel monitoring (if the apparatus features this option). Dual-channel monitoring also allows to shorten scanning duration.
The test is performed in a patient lying in supine position. A needle (preferably with an elongated, flexible tip and a tap) should be inserted into the ulnar vein. Optionally, a monitoring band in placed on the patient's head and dual-channel monitoring can be set. This is followed by checking the transparency of the temporal bone window.
Next, 10 mL syringes should be prepared and each filled with 9 mL of 0.9% NaCl and 1 mL of air; small volume of patient's blood can be withdrawn from the injection site (about 0.3 mL). The syringe should be shaken vigorously. (Echovist® contrast agent, 5 mL for each test, can be also used) (3, 4).
The examination is performed after obtaining a clear spectrum of the flow velocity in the middle cerebral artery through the temporal window. The patient is asked to breathe normally. After contrast agent administration, the flow spectrum in the middle cerebral artery should be observed for 60 sec. If more than 20 microembolic signals occur (particularly if they merge), repeating the test with Valsalva maneuver should be abandoned. If no microembolism occurs for about 60 sec., Valsalva maneuver is performed. Shaken saline (10 mL) should be administered, and, after 5 seconds, the patient should be asked to perform Valsalva's maneuver for 10 seconds [adequately performed Valsalva's maneuver will be confirmed by the signs of increased intracranial pressure in TCD image (significantly increased resistance and decreased systolic and diastolic velocity), and minor hyperperfusion after restoration of normal breathing]. TCD should be used to follow the occurrence of microembolism on the flow spectrum background for about 60 seconds.
The result is considered negative if no microembolic signal is detected following three subsequent Valsalva's maneuvers(3, 4).
Images from the basic scanning and after Valsalva's maneuver, preferably in the form of a film, should be documented. If this is not possible, static images of the flow in the middle cerebral artery indicative of microembolic signals or their absence during each phase of examination should be recorded.
The result should contain the name of the device, probe frequency, the type of monitoring (single- or dual-channel) of the middle cerebral artery, data on the type and dose of the administered contrast agent as well as the number of Valsalva's maneuvers.
This should be followed by the shunt grade determined with a single-channel monitoring, in accordance with the classification in Table 1 (1–4).
Right to left shunt grade classification with single-channel monitoring of the middle cerebral artery(1–4)
|Shunt grade||Number of signals||The range of RLS|
|0||no microembolic signals||no RLS|
|1||1–10 signals||minimal RLS|
|2||More than 10 signals, countable, non-merging||moderate RLS|
|3||Rain of signals (‘curtain effect’ – counting of the individual signals is impossible due to their merging)||significant RLS|
Diagnosis of cerebral circulatory arrest
The examination is performed either before or after forming a suspicion of brain death. It should be performed by a physician with extensive experience in neurosonology(6, 7).
The examination is performed using 4 MHz ‘blind’ continuous-wave Doppler (extracranial intracerebral arteries) with 2 MHz pulsed-wave Doppler (transcranial Doppler) (6, 7).
The test is performed in a patient lying in supine position.
Technical settings(3, 6):
sweep – possibly free;
power – maximum;
gain – high;
high frequency filter ≤50 Hz;
sample volume ≥15 mm;
the envelope should be preferably off;
the depth of flow measurement in the middle arteries – 50–65 mm (carotid artery bifurcation should be avoided).
The examination is performed using 2 MHz pulsed-wave Doppler through the temporal window (middle, anterior and posterior cerebral artery) and suboccipital window (vertebral arteries and the basilar artery). Additionally, the flow in the extracranial portion of the internal carotid artery is assessed using 4 MHz CW Doppler (or duplex Doppler of the extracranial arteries is performed).
The examination should be performed twice with an interval of at least 30 minutes unless artery with oscillating flow is monitored for 30 minutes(6, 7).
Cerebral circulatory arrest cannot be diagnosed in the following cases: mean systemic pressure of less than 80 mmHg, tachycardia >120/min, significant loss of skull bone, a child with an open fontanel(7).
During the examination, pressure must be maintained constant; arterial carbon dioxide partial pressure should not decrease below normal values (i.e. <35 mmHg)(7).
The obtained spectra from both middle arteries and the basilar artery should be documented. Additionally, spectra from extracranial internal carotid and vertebral arteries should be recorded.
The result should contain the name of the device and probe frequency, as well as the list of evaluated arteries. Additionally, arterial carbon dioxide partial pressure, pulse and blood pressure recorded during the examination should be documented. The diagnosis of cerebral circulatory arrest should include criteria met by individual arteries.
The diagnosis of cerebral circulatory arrest requires identification of the following types of flow in both middle cerebral arteries and the basilar artery(1, 3, 6):
early systolic small peaks indicating a maximum amplitude of <50 cm/s, or
‘rebound’ flow (oscillating) with short systolic complex and a diastolic component with direction opposite to systolic complex throughout the diastole – in this situation the patient should be monitored for 30 seconds to exclude the effects of transient rise in the intracranial pressure (no need for repeating the test after 30 minutes), or
absence of cerebral flow in three arteries at the base of the brain, where the flow was previously recorded (i.e. several days or weeks earlier) (baseline examination performed within the previous days is needed). Absence of flow should be clearly demonstrated.
Identification of the absence of cerebral flow without reference to baseline findings does not indicate cerebral circulatory arrest due to the possible lack of transparency of the bone window(3, 6, 7).
The presence of the above mentioned pathological types of flow in both intra- or extra-cranial vertebral and internal carotid arteries (extracranially using duplex Doppler) is an additional, indirect and optional criterion (7).
Conflict of interest
Authors do not report any financial or personal connections with other persons or organizations, which might negatively affect the contents of this publication and/or claim authorship rights to this publication.
List of abbreviations
posterior cerebral artery
transcranial color-coded duplex