Ultrasound assessment of brain supplying arteries (transcranial)

Transcranial ultrasound examination is a standard technique in neurovascular medicine, not least because of its bedside and noninvasive application. Due to the much broader availability of high-quality ultrasound devices with integrated color duplex ultrasound and Doppler sonography, pure Doppler sonography of the brain-supplying arteries hardly plays any role in daily routine today. Transcranial Doppler sonography (TCD) has specific value in bedside diagnosis, especially in intensive care patients, or as a supplement to special examination modalities discussed in the text. The collection and interpretation of intracranial vascular findings requires profound anatomical and pathophysiological knowledge of cerebral structures. A sufficiently long training period under supervision, as well as dedicated knowledge of the alternative imaging methods, is a prerequisite for a valid image interpretation, especially if the method is used for follow-up. The examination of extracranial vessels is described in detail in an accompanying article [1]; for didactic reasons, transorbital ultrasound is also discussed in this article. Notes for basic documentation can be found in the article on extracranial vascular imaging [1]; in summarized form, the recommendations can be found in [Table 1]; reference is made to the current standard literature and recommendations of professional societies [2] [3] [4] [5].

Table 1 Recommendations for Basic Documentation.

	Doppler sonography	Duplex ultrasound/B-mode imaging
Ophthalmic artery (terminal branch)	Supratrochlear artery; compression test	Ophthalmic artery, transorbital insonation
Orbital
		Central retinal artery
		Optic nerve sheath diameter
		Papilledema (Optical disc elevation)
		Spot sign
Transtemporal
Middle cerebral artery	M1 at 45–55 mm	Color-coded axial section with Doppler spectrum M1 section
Anterior cerebral artery	A1 at 70–75 mm	Color-coded axial section with Doppler spectrum A1 section
Carotid artery T	–	Color-coded coronary section with Doppler spectrum of the internal carotid artery
Posterior cerebral artery	P1 or P2 at 65–75 mm	Color-coded axial section with Doppler spectrum P1 section
Basilar artery	–	Color-coded coronary section with Doppler spectrum of the basilar artery
Transtemporal and transnuchal
Vertebral artery	65–75 mm	Color-coded depiction of the vertebral-basilar junction (“vertebrobasilar Y”) with Doppler spectrum of the vertebral and basilar arteries
Basilar artery	As far cranially as possible

Transorbital examination and orbital sonography

In the case of severe stenosis or occlusion of the internal carotid artery (ICA), a collateral circulation via anastomosis between the external carotid artery (ECA) and the ophthalmic artery can be detected by examining the supratrochlear artery at the medial angle of the eye. The intracranial and extracranial arteries are connected via the supratrochlear artery. In a normal case (antegrade, orthograde direction of flow), blood flow increases in direction towards the probe when the extracranial vascular stems of ECA (superficial temporal artery, facial artery) are compressed (i. e., the extracranial pressure is reduced, and the physiological flow balance increases from intracranial to extracranial). In the case of an obstruction of the extracranial blood supply due to high-grade stenosis or occlusion of the internal carotid artery, the drainage of the supratrochlear artery may show near-zero flow or even retrograde flow (flow from extracranial to intracranial), which characteristically decreases after compression of an extracranial branch (= pressure extracranial is reduced, pathological retrograde flow from extracranial to intracranial decreases) or reverses. Examination of the supratrochlear artery at the medial angle of the eye is most easily achieved by continuous wave (cw) Doppler sonography using an 8 MHz pencil probe. Collateralization via the external ophthalmic anastomosis can also be diagnosed by demonstrating a retrograde flow direction in the ophthalmic artery with color-coded duplex sonography, whereby the ophthalmic artery is depicted with color flow imaging via the transorbital sound window with a duplex 7.5-MHz linear or 2.5-MHz sector transducer after reducing the transmission power (mechanical index ≤ 0.2 in B-mode). Examination of the patient is done in a supine position; the orbita is scanned through the closed eyelid with a sufficient lot of contact gel, if possible without pressure from the probe ([Fig. 1]). The ALARA principle applies: “as low as reasonably achievable”. This is achieved by setting the transmitting power as low as possible (even when the duplex mode is turned on) and increasing the gain settings. A default preset helps not to overlook this.

Fig. 1 Probe positioning and image plane. a Transorbital and transnuchal probe position, b axial and c coronal transtemporal image plane.

Cave

When setting the device, care must be taken to keep the mechanical index (≤ 0.2) as low as possible to avoid potentially conceivable damage to the lens and retina.

Note

Typical questions of orbital sonography are the assessment of papilledema, a possible increase in intracranial pressure with determination of the optic nerve sheath diameter (ONSD), and the recording of the Doppler spectrum and the flow velocities of the central retinal artery.

To determine the ONSD, the probe is placed slightly laterally and scanned medially. To avoid eyeball movement, the patient can fixate on a virtual point with the eyes closed. In order to avoid any confusion regarding the correct side in the documentation, a uniform labeling and documentation form should be established by the laboratory; a uniform convention has not yet been established. The standard values and exact measurement points for the determination of ONSD vary somewhat between laboratories; a uniform convention is being developed by both DEGUM and an international consortium [6]. A width of 5.4 ± 0.5 mm, measured 3 mm behind the retinal plane, can be used as a guiding standard value [7].

Duplex ultrasonography can be used to visualize the retrobulbar central retinal artery; the low flow velocities (standard value: 10.3 ± 2 cm/s) should be taken into account when creating a preset in the sense of a low pulse repetition frequency (PRF). Absence of flow is found, for example, in the case of central retinal artery occlusion. In the acute phase of central retinal artery occlusion, orbital sonography may become more important, as it enables visualization of a distal embolism in the retinal artery in more than half of cases (“spot sign”) that cannot be visualized on normal CT angiography ([Fig. 2]) [8] [9]. Whether this “spot sign”, may influence therapeutic decision making regarding systemic thrombolysis is currently under investigation. It is suspected that a visualizable, highly echogenic thrombus is likely to correspond to distal embolization of a calcified plaque component and therefore might not respond as effectively to systemic thrombolysis [9]. In contrast to this, absence of a spot sign is more likely to be attributed to a low echogenic embolus, which should respond better to systemic thrombolysis.

Fig. 2 Orbital sonography focusing on the retrobulbar region in a 73-year-old patient with acute loss of vision in the left eye. Behind the retinal plane, the width of the nerve sheath of the optic nerve can be determined at a depth of 3 mm (this is only possible to a limited extent in the illustration due to the oblique course of the optic nerve). There is a strongly echogenic signal in the tip of the hypoechoic optic nerve, which may correspond to a calcified embolism of the distal central retinal artery (“spot sign”, arrow).

Transcranial examination

In addition to the transorbital access described above, the intracranial vessels are examined via a transtemporal and a transoccipital or transcuchal bone window ([Fig. 1]) using either a phased-array duplex transducer (usually 2.5 MHz) or a 2 MHz pencil probe. Duplex ultrasonography has become increasingly established as standard in recent years, as it enables better vessel identification, angle-corrected measurement, and assessment of intracranial structures (parenchyma, ventricle, etc.) [10] [11]. Whether or not to perform angle correction is a topic of controversial debate in the literature. The angle correction should be placed in a straight vessel segment of sufficient length (about 15 mm) in which the main flow vector can be identified. This enables a more valid measurement of flow velocities, as the measurement can be adapted to the vascular course in case of anatomical variations. If correct positioning of the angle correction is not possible, the measurement must be performed without correction and the maximum values of the measured flow velocities are used for the assessment. In the case of insufficient bone windows, the 2 MHz Doppler probe can be used. A smaller footprint of the probe and a narrower ultrasound beam makes it possible to insonate through smaller bone windows, which are too small for the duplex transducer. In case of a still insufficient bone window, sufficient vascular imaging can be achieved with the help of ultrasound contrast enhancing agents (used as an amplifier of the reflected ultrasound).

Cave

It should be noted that the flow velocities measured with ultrasound contrast enhancing agents are incorrectly high, and the absolute values cannot be used. It is only possible to detect side-to-side differences of flow velocities.

The best transtemporal bone window is usually found on an imaginary junction between the outer angle of the eye and the upper ear. A good bone window is achieved when the opposite side of the skull (insonation depth: 15 cm) is sufficiently displayed. The brainstem (mesencephalon) is set as an intracranial guiding structure with its typical hypoechoic butterfly-shaped contour with surrounding high echogenic basal cistern. Switching to color coded imaging (insonation depth: 10 cm), the posterior cerebral artery (PCA) can be seen winding around the brainstem. Rostrally to the PCA, the middle cerebral artery (MCA) (M1) and also the bifurcation/trifurcation with its M2 branches can be depicted with a flow direction towards the probe ([Fig. 3], [4]). In approximately 3 % of cases, the MCA has a medial bifurcation, which acts like a “doubled M1 segment”.

Fig. 3 Normal findings of the intracranial arteries. Middle cerebral artery (1) with flow to the probe (red) in the horizontal (left) and coronary cross-sectional plane (center; 5: hyperechogenic double outline of the carotid canal). The anterior cerebral artery (2, blue) flows away from the probe. The posterior cerebral artery (3) surrounds the brainstem (4) and is depicted in red in the area of origin and blue in the posterior section. On the right is the vertebrobasilar “Y”, the confluence of the bilateral vertebral arteries (6) into the basilar artery (7) displayed with transnuchal insonation.

Fig. 4 A 46-year-old patient with sudden onset of severe headaches, with marked meningism appearing on clinical examination. The medical history reports an additional short-term headache event seven days prior; cranial computed tomography showed a subarachnoid hemorrhage. Transcranial duplex ultrasonography shows greatly increased flow velocities in the intracranial vessels; the image shows the right middle cerebral artery with a peak systolic velocity (PSV) of almost 400 cm/s and a mean flow rate of 254 cm/s, corresponding to a significant vasospasm.

Towards the midline, the anterior cerebral artery (ACA) is visible, normally with a flow direction away from the probe (“antegrade”) (A1). The most common pathological finding is a reverse flow direction (“retrograde” ACA, “anterior-cross-filling”) in case of a high-grade stenosis/occlusion in the extracranial internal carotid artery (ICA) representing a collateral circulation. The anterior and posterior communicating arteries cannot be depicted regularly due to their small size and anatomy. Assessment of the carotid T, or the cavernous distal ICA, and the basilar head is possible by tilting the transducer vertically and aligning it in the direction of the opposite zygomatic arch (coronal incision) ([Fig. 1], [3]). For documentation purposes, the vessel is to be displayed in duplex mode (B-mode imaging plus color coding) for each vessel section examined, together with a Doppler spectrum derived from this vessel segment. In straight vessel segments with a length of about 15 mm in which the flow vector can be clearly determined, the derivation of the Doppler spectrum should be angle-corrected [12]. The electronic caliper of the ultrasound device can be used to measure peak systolic velocity (PSV) and end diastolic velocity (EDV). For many devices, the intensity-weighted mean flow velocity (MFV) is also automatically calculated; calculation: (PSV-EDV)/3 + EDV). However, in the case of poor bone windows or even higher-grade stenosis, the latter can be distorted by artifacts in the Doppler spectrum due to aliasing, turbulence, or a poor signal-to-noise ratio.

Note

In North American literature, MFV is widely used in transcranial Doppler and duplex ultrasound as a reference measure of flow rates, while PSV and EDV are also commonly used in Europe.

Flow accelerations of the intracranial vessels are the most common pathological findings. When grading stenosis, a division into greater or less than 50 % has been established. A detailed list of the PSV cut-off values can be found in [Table 2], along with the guiding standard values [4] [5] [13]. Occlusions of intracranial arteries are more difficult to diagnose; this is certainly possible for the M1 segment of the middle cerebral artery provided a sufficient insonation window. If ipsilateral ACA and PCA can be visualized, a missing M1 segment of the MCA is evidence of occlusion ([Fig. 5]).

Table 2 Standard values of transcranial duplex ultrasound, and to discriminate between mild (30–50 %) and ≥ 50 % stenosis.

	Standard value (PSV) [cm/s ± SD]	< 50 % stenosis (PSV) [cm/s]	≥ 50 % stenosis (PSV) [cm/s]
Middle cerebral artery	108 ± 18	≥ 155	≥ 220
Anterior cerebral artery	82 ± 17	≥ 120	≥ 155
Posterior cerebral artery	60 ± 14	≥ 100	≥ 145
Vertebral artery	60 ± 16	≥ 90	≥ 120
Basilar artery	67 ± 16	≥ 100	≥ 140

PSV: peak systolic velocity; SD: standard deviation

Fig. 5 Middle cerebral artery occlusion: With insonation through the left temporal bone window, the middle cerebral artery (MCA) cannot be visualized either proximally or distally (see arrow in the graph). The remaining cerebral basal arteries are depicted as orthograde. Typical finding in proximal media occlusion (arrow: lack of flow signal from the left occluded MCA).

For the assessment of vasospasm, e. g., after a subarachnoid hemorrhage, it is common to determine the mean flow velocity (MFV) and the ratio of MFV between the middle cerebral artery and the internal carotid artery (Lindegaard index [14]). Doppler sonography with a 2 MHz probe is still frequently used to assess vasospasm. It has been shown to be permanently available and reliable in application, especially in intensive care units, so that it is often used in practice rather than duplex ultrasound.

Note

MFV of more than 120 cm/s is referred to as incipient vasospasm, from 160 cm/s it is considered as significant, and from 200 cm/s it is considered critical ([Fig. 4]). An increase in flow velocities of over 50 % or 40 cm/s per day or an MCA/ICA ratio > 3 [15] is also an indication of a possible intracranial vasospasm.

Another differential diagnosis for increased flow velocities in the intracranial vessels is the rare hyperperfusion syndrome, which can occur in the first days after revascularization of a high-grade stenosis of the internal carotid artery. In terms of the post-interventional situation, probably favored by a previously limited cerebrovascular reserve capacity, there is a significant increase in intracranial blood flow with the risk of secondary intracerebral hemorrhage or the provocation of epileptic seizures. Although criteria for hyperperfusion vary in the literature, a > 100 % increase in intracranial flow rates with reduced pulsatility and a decreased Lindegaard index indicate cerebral hyperperfusion.[16] Usually, this remains without clinical complications and manifests itself only as mild headache and patient discomfort; effective blood pressure management (normotonia) is the therapy of choice and can prevent manifest hyperperfusion syndrome.

Cave

In hyperperfusion syndrome, flow velocities are increased in both the extracranial and intracranial vessels, whereas in vasospasm, only the flow rates of the intracranial vessels are increased, but not those of the extracranial vessels.

Transnuchal examination

In the transnuchal examination to assess the vertebrobasilar arteries, the foramen magnum is set as the hypoechogenic guiding structure. For this purpose, the probe is placed about 2–3 cm below the occiput ([Fig. 1], [3]). The virtual image plane goes in the direction of the forehead (nasion); the chin of the subject to be examined should be slightly tilted towards the breast. A lateral positioning of the patient with a small head pillow, sparing the neck, allows a relaxed examination position. If tolerated by the patient, this examination can also be performed in a seated position. In color flow imaging, the V4 segments can be depicted on both sides, and the confluence to the basilar artery (vertebrobasilar “Y”, usually at a depth of 7–8 cm) is adjusted and tracked distally. If the probe is tilted slightly laterocaudally, the vertebral artery can also be visualized in the V3 segment. The entire imaging of the basilar artery is often not possible [16], so that indirect stenosis criteria must also be taken into account here. In addition, pw Doppler (TCD) can be helpful, as it can occasionally be used to examine a larger area, and is well suited as a follow-up modality for confirmed pathological findings.

Special neurovascular indications

In the diagnostic work-up in patients with an ischemic stroke, a “bubble test” can be performed to test for a right-left shunt (RLS). With continuous recording of the cardiac or pulmonary left or right middle cerebral artery (unilateral monitoring, higher sensitivity is achieved with simultaneous bilateral recording), or alternatively, in the case of insufficient transtemporal insonation, recording of the basilar artery or the extracranial internal carotid artery), a ultrasound contrast enhancing agent which cannot pass the pulmonary circulation, is injected and a Valsalva maneuver is performed, which, if implemented correctly, leads to a reduction of intracranial arterial flow. After the preparate Echovist was taken off the market, an isotonic saline solution (10 mL solution ‘agitated’ with 1 mL air) has proven useful as a contrast enhancing agent. After injecting IV (right cubital vein) as quickly as possible, the Valsalva maneuver is started 5 seconds after the injection, and the middle cerebral artery is recorded for a total of 30 seconds. A further 5–7 seconds after the Valsalva maneuver, the first HITS (high intensity transient signals) can be detected at presence of an RLS ([Fig. 6]). A semiquantitative estimate of the number of HITS (> 10: particularly relevant RLS; “curtain”: particularly large RLS) can provide an initial classification [18] [19]. There is no general consensus on the exact timing and the quantification or diagnosis of a patent foramen ovale (PFO) based on the number of shunted contrast bubbles. The test can be repeated without Valsalva maneuver in order to detect spontaneous RLS. Transcranial RLS detection only allows assessing the presence of RLS, with high sensitivity. Based on the number of microbubbles and time delay in occurrence, no reliable statement can be made about the type (shunt at the cardiac or pulmonary level) and size of PFO. This can only be achieved by qualified transesophageal echocardiography, which also assesses morphological aspects of the PFO.

Fig. 6 A 68-year-old patient with symptomatic left-sided carotid artery stenosis. Continuous embolism detection of the left middle cerebral artery showed multiple MES/HITS (see arrow for an example). Signal behavior and the typical acoustic “chirp” signal are characteristic. In the upper half of the image, the continuous Doppler recording can be seen at a depth of 55 mm, in which the embolism signal can be clearly differentiated from the normal flow. Below is the so-called Power M mode; here, the path of the embolism is also depicted over a depth of 55 mm.

Continuous recording of the middle cerebral artery is also important in the assessment of asymptomatic carotid artery stenosis. For example, the occurrence of HITS or MES (microembolic signals) in case of an extracranial stenosis is an indication of increased embolicity and is considered an argument for referring asymptomatic carotid artery stenosis to surgical or interventional therapy [19]. The recording is usually automated for 30–60 minutes after manual adjustment via a special probe holder; software-based preselection of the events helps in the evaluation. Differentiating emboli from artifacts requires sufficient expertise; a short duration (< 300 ms) is typical of HITS, the amplitude intensity should be by at least 3 dB greater than the background signal of blood flow, their occurrence is independent of the heartbeat, and with the typical “chirp” sound. If available, power M mode can also provide better differentiation from artifacts. Here, a row of multiple Doppler sample volumes are imaged in the M mode format ([Fig. 6]) [21].

Another criterion that can predict an increased risk for the subsequent symptomatology of a clinical silent carotid stenosis is an exhausted vasomotor reserve capacity. This reflects impaired cerebrovascular autoregulation and occurs with hemodynamically relevant extracranial stenosis or occlusions. Here, the intracranial arterioles are already maximally dilated, so that an additional vasodilator stimulus no longer leads to a relevant increase in blood flow. In this constellation, cerebral perfusion pressure is more dependent on systemic blood pressure than it would be with intact autoregulation. Vasomotor reserve capacity can be tested by administering a 5 % CO₂ gas mixture (CO₂ represents a potent vasodilator stimulus), while the flow velocities in the proximal middle cerebral artery is recorded. If no relevant increase in the flow velocities of the middle cerebral artery (i. e., > 30 % of the baseline) occurs, this is referred to as depleted or limited reserve capacity, which is associated with an increased risk of stroke [22]. Alternatively, acetazolamide (1000 mg i. v.) can also be administered instead of CO₂, or a breath-holding test (difference between flow rate at hyperventilation and air retention for > 30 s, assuming patient compliance) can be applied.

For the sake of completeness, the field of application for the detection of irreversible brain function loss should also be mentioned, since transcranial Doppler/duplex ultrasound is used in a bedside setting and does not require laborious patient transport to the intensive care unit. For the detailed formal and technical implementation provisions, please refer to the current literature [23].

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