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119Arterial Pathology

Valdueza et al., Neurosonology and Neuroimaging of Stroke: A Comprehensive Reference, Second Edition (ISBN 978-3-13-141872-2), copyright © 2017 Thieme Medical Publishers All rights reserved. Usage subject to terms and conditions of license.

Area reduction [%]

96846436

600

500

400

300

200

100

Blood volume flow (mL/min)

0 0

Diameter reduction [%]

Fig. A5.34 Mathematical ﬂ ow model in ICA stenosis (Spencer’s curve). Theoretical relationship of stenosis grade (assessed by diameter and area measurements) and systolic blood ﬂ ow velocity (blue line) within the stenosis. In very high-grade stenosis velocity values drop, and they further decrease in near-occlusion. Note the blood volume ﬂ ow (red line) values remain constant until a 70–80% diameter reduction, deﬁ ning the start of a hemodynamic relevant stenosis. (Adapted from Spencer and Reid 1979.)

300

200

Flow velocity (cm/s)

100

100806040200

in the region with maximal lumen reduction from the inner border zone of the wall. The grade of stenosis is calculated from the relation of the total vessel diameter (D and the minimal stenosis diameter:

Grade (%) = D

stenosis/Dtotal

× 100

total

Area: Unlike DSA but similar to CTA and (with some restrictions) to MRI, duplex ultrasound allows measurement and calculation of the grade of stenosis from the vessel’s cross-sectional area, a parameter which correlates best with results derived from postoperative histologic planimetric analysis (Alexandrov et al 1993, Eckstein et al

2001). It is the true relevant anatomic parameter for the measured ﬂ ow velocities according to the physics of ﬂ ow. Area measurement is also independent of the morphological conﬁ guration of the stenosis, while the diameter approach only measures correctly in the case of a cylindrical stenosis. The grade of stenosis is calculated from the relation of the total vessel area (A stenosis diameter (A

Grade (%) = A

stenosis

stenosis/Atotal

) and the minimal

total

× 100

Examples of both diameter and area measurements are given in Fig. A5.32. Although assessed in exactly the same vessel segment, the two methods yield diﬀ erent results. The diameter calculation (D in a 62% stenosis, the area calculation (A

= 10.1 mm2) in 81% stenosis. This phenomenon can

stenosis

also be described mathematically (Fig. A5.33). Depending

= 9 mm, D

total

= 3.4 mm) results

stenosis

= 52.4 mm2,

total

on the type of stenosis (axisymmetric or asymmetric) the nonlinear relation between area and diameter varies in favor of diameter or area (Spencer and Reid 1979). Up to now all

major clinical trials with catheter angiography as the main method have used the diameter approach, so it will currently continue to be the preferred method of assessment. In the future, however, the area method recommended for duplex sonography in the 1990s (de Bray and Glatt 1995) will probably gain importance, particularly considering the increasing use of the CTA technique, with which it is also possible to perform exact planimetric cross-sectional measurements (Bartlett et al 2007).

Direct Hemodynamic Assessment

Hemodynamic eﬀ ects can be observed using the color mode of the ultrasound system. The color signal not only reveals the regions with preserved ﬂ ow but also gives in- formation about ﬂ ow direction (antegrade or retrograde ﬂ ow). Furthermore, a color-aliasing phenomenon may indicate the presence of raised ﬂ ow velocities, such as those caused by a stenosis of at least medium grade. However, the main source of hemodynamic information is provided by the Doppler spectrum analysis, from which several parameters can be derived.

Blood Flow Velocity: Blood ﬂ ow velocity values, i.e., the maximal systolic velocity (also referred to as peak velocity), maximal end-diastolic ﬂ ow velocity, or the mean ﬂ ow velocity, are derived from the Doppler spectrum (for further details see Chapter 3, “Cerebral Blood Flow Velocity”).

)

Their assessment may reveal normal, raised, or reduced values. Vessel narrowing is directly correlated with increased ﬂ ow velocities but this relation is not linear over the whole range of stenosis grades. In very high-grade stenosis and near-occlusion, ﬂ ow velocity drops to normal or below normal values, as demonstrated in the Spencer’s curve (Fig. A5.34). According to this curve, which was developed to describe ﬂ ow properties in a straight vessel without bifurcation and an axisymmetric stenosis, the initial increase in ﬂ ow velocity compensates the lumen re- duction to maintain a constant blood ﬂ ow volume. With a stenosis of 70% (which correspond to an area reduction of 90%) or more, the blood ﬂ ow volume drops despite a fur- ther increase of ﬂ ow velocity. When the stenosis reaches ~85% the blood ﬂ ow velocity also starts to fall. The same velocity may therefore be seen in a 60% stenosis as in a 90% stenosis (rising or falling shoulder of the curve). To assess the grade of stenosis correctly it is crucial to consider the pre- and poststenotic waveforms as well as the presence of collateral vessel activation. These indirect signs are of paramount importance for conﬁ dent grading of stenoses. Note that the deﬁ nition of a hemodynamically relevant stenosis refers to the decreased blood volume ﬂ ow and not to an increased blood ﬂ ow velocity; this term should therefore be used only for a stenosis of at least 70–80%.

The Spencer’s curve was mainly developed to predict arterial hemodynamics in a proximal ICA stenosis, and has several limitations. For instance, it applies to short and a x i s y m m e t r i c c o n c e n t r i c s t e n o s e s , w h e r e a s p a t i e n t s w i t h macroangiopathic lesions usually reveal irregular, eccentric stenoses of diﬀ ering lengths. Atherosclerotic stenoses are usually short compared with stenoses caused by vessel dissection or arteritis. Long-segmented stenoses will be underestimated as high ﬂ ow velocities are usually missed

120 5 Vascular Pathology

Fig. A5.35 Increased ﬂ ow in the VAs in bilateral ICA occlusion. Left: Ce-MRA, anterior MIP, showing bilateral ICA occlusion (ar-

rowheads) and a bilaterally pronounced VA signal (arrows). Right: Duplex sonography, longitudinal plane, color-mode image and corresponding Doppler spectrum analysis: Turbulent ﬂ ow and in- creased ﬂ ow velocities in the right V2-VA, diameter 3.9 mm, ﬂ ow velocity 93/44 cm/s (top) and in the left V2-VA, diameter 4.1 mm, ﬂ ow velocity 108/48 cm/s (bottom). Identical ﬂ ow patterns were observed in the intracranial VAs and BA. Note, the mild poststenotic and turbulent ﬂ ow aspect results from the increased VA ﬂ ow.

in such conditions. Also, Spencer’s model implies straight vessel walls resembling a channel: However, the major site of stenotic lesions in extracranial brain-supplying vessels is the proximal ICA which has a physiologic proximal widening, the carotid bulb. The carotid bulb is rarely absent but has a highly variable diameter ranging from normal to pseudo-aneurysmatic dilation doubling the normal ICA diameter (see also Chapter 2, “Extracranial Arterial Anatomy” under “General Arterial Anatomy”). Because of this physiologic dilation a nonlaminar ﬂ ow, even with partly retrograde ﬂ ow components, is the usual duplex ultrasound appearance and should not be misinterpreted. A bulb stenosis of ~30% may therefore not reduce the intraluminal diameter compared with that of the distal ICA segment and may even “normalize” the ﬂ ow signal by showing ﬂ ow that is now laminar. A 50% stenosis would also not alter waveform and velocities and a local 80% stenosis might not lead to any hemodynamic compromise. The carotid bulb therefore makes interpretation of velocity data somehow diﬃ cult. The good news is that all the other brain-supplying vessels follow the prediction of the Spencer’s curve better, as they normally do not have a bulb equivalent. According to the model a 50% stenosis should double blood ﬂ ow velocities and a 70% stenosis should lead to a fourfold increase in velocity. Despite these and other shortcomings, sonographers should use the Spencer’s curve as the basic tool to understand hemodynamics and the consequences of brain-supplying artery stenosis.

It is important to know that raised ﬂ ow velocities are not limited to lumen reductions. For example, a global velocity increase may be observed in hemodilution and anemia to compensate for the loss of oxygen transporters, or in increased blood volume ﬂ ow (hyperperfusion) which may be seen in the early phase following severe head trauma, in the subacute phase after subarachnoid hemorrhage, or in general hypoxia. In all these conditions ﬂ ow velocities are globally increased. Segmental hyper-

Fig. A5.36 Doppler spectra, obtained from follow-up transcranial insonation of the MCA in a patient with severe hypoxia. (A) Normal blood ﬂ ow and ﬂ ow velocity. (B) Hyperperfusion—note the increased ﬂ ow velocities as well as the reduced pulsatility. (C) Hypoperfusion—note the reduced ﬂ ow velocity as well as the increased pulsatility resembling an extracranial ﬂ ow signal (“no brain, no ﬂ ow”).

perfusion and concomitant raised ﬂ ow velocities are ob- served in extra- and intracranial collateral ﬂ ow pathways in steno-occlusive disorders, e.g., in the anterior (ACoA) or posterior (PCoA) communicating arteries or extracranially in the neck vessels in occlusions of other major vessels. For example, in bilateral VA occlusion an increased blood ﬂ ow and a corresponding increase in ﬂ ow velocity is expected in one or both ICAs (see also Case 41). Contrarily and more evidently, in bilateral ICA occlusion raised blood ﬂ ow and ﬂ ow velocity may be observed in the extra- and intracranial segments of the VAs and the BA (Fig. A5.35; see also Case 12). Similar ﬁ ndings will be encountered in feeding vessels of ar- teriovenous angiomas or dural ﬁ stulas (see also Case 34 and Case 40). In all these cases the diastolic ﬂ ow velocity will be disproportionately high, indicating a loss of peripheral resistance and dilation of the low-resistance vessels. Conversely, global low ﬂ ow velocities can be observed if the he- matocrit is high (Brass et al 1988), in severe cardiac output failure, in generalized dilated intracranial vessels—usually in long-standing arterial hypertension—or in the chronic state after severe head trauma or hypoxia. Regional ﬂ ow velocity reductions may indicate hemodynamically relevant occlusive processes proximal or distal to the measurement site. All the above-mentioned conditions obviously hinder a simple interpretation of velocity ratios. A sophisticated analysis therefore needs a critical overview of all accessible direct and indirect ultrasound ﬁ ndings. Furthermore, the optimal time for insonation must also be considered. In the ﬁ rst hours of severe global cerebral hypoxia, a distinct reduction of cerebral blood ﬂ ow and consequently of blood ﬂ ow ve- locity occurs. Subsequently a reactive hyperemic phase can be observed, comprising generally increased ﬂ ow velocities as well as reduced pulsatility. If the hypoxia leads to massive brain tissue necrosis, such as in persistent vegetative state, the chronic phase may reveal low ﬂ ow velocities and a high pulsatility similar to the proﬁ les seen in the ECA. A similar

121Arterial Pathology

Fig. A5.37 CCT and TCCS in chronic MCA infarc tion. Left: CCT scan, axial planes showing a residual almost complete territorial MCA infarction. Right: TCCS (transtemporal approach), right-sided insonation, midbrain plane, color-mode image and Doppler spectrum analysis of the M1-MCA: Reduced ﬂ ow velocity of 58/15 and increased PI of 1.84 in the aﬀ ected side (top) compared with the contralateral M1-MCA (insonated via the same side) with normal ﬂ ow velocity of 68/28 mm/s and PI of 1.07 (bottom).

phenomenon occurs after large territorial infarctions in the involved arteries (Fig. A5.36, Fig. A5.37, Fig. A5.38).

Blood ﬂ ow velocity measurement in the brain-supplying

arteries crucially depends on the angle of correction as this greatly aﬀ ects the ﬁ nal velocity measurement (for further details see Chapter 1, “Doppler Shift and Flow Velocity” under “Ultrasound Principles,” and Chapter 3, “Cerebral Blood Flow Velocity” under “Parameters of Cerebral Hemodynamics”). In nonpathologic vessels angle correction should preferentially be done parallel to the vessel walls, which usually corresponds to the ﬂ ow stream visualized in the color mode. In a stenosed vessel the ﬂ ow may diﬀ er from the anatomic course of the vessel due to eccentric stenoses. Here, the angle should be corrected according to the ﬂ ow stream (also called the “jet”). A Doppler angle greater than 60° should be avoided as it may lead to velocity overestimation. This problem particularly occurs in V2-VA insonation as the vessel course is practically at a 90° angle in relation to the ultrasound beam, which already causes problems in the colormode visualization of ﬂ ow. We recommend improving the insonation angle by mild angulation of the probe into the soft neck tissue. Intracranially, nonoptimal insonation angles occur during the insonation of the A2-ACA, PCoA, and the transitional zone between the proximal and the distal P2-PCA, as well as during coronal transtemporal insonation of distal ICA and BA.

Velocity Ratios: As discussed earlier, ﬂ ow velocity meas- urements give only surrogate information about blood ﬂ ow. Under physiologic conditions cerebral blood ﬂ ow and ﬂ ow velocities are well correlated. In pathologic conditions, high velocities may still reﬂ ect normal blood ﬂ ow (e.g., in nonhemodynamically relevant stenosis), decreased blood ﬂ ow (e.g., in hemodynamically relevant stenosis), and even increased blood ﬂ ow (e.g., in hyper- perfusion). High velocities might even be caused by a mixture of stenosis and hyperperfusion which may be

Fig. A5.38 MRI and TCCS in complete MCA infarction. (A) 3D TOFMRA, coronal view, indicating proximal MCA occlusion (arrow). (B) MRI, T2-weighted image, axial view. M1-MCA ﬂ ow void with reduced diameter compared with the contralateral side (arrow) indicating residual ﬂ ow. (C–E) TCCS, transtemporal approach, ax- ial midbrain plane, color-mode and corresponding Doppler spectra. (C) Normal PRF and color gain TCCS settings easily depicting the main stems of the contralateral MCA, both ACAs, and PCAs. Ipsilateral proximal MCA vessel sheath is visible within the lateral ﬁ ssure but M1-MCA is missed (arrow), wrongly suggesting occlusion. (D,E) Reduced PRF and increased color gain result in aliasing of color signals (“dirty image”) now showing a proximal MCA color signal (arrow) and a ﬂ ow signal with low ﬂ ow velocities (15/6 cm/s).

observed in the subacute phase after subarachnoid hemorrhage (SAH) (simultaneous presence of hyperperfusion and vasospasm). In addition to pure velocity measurements, velocity ratios comparing homologous vessels on both sides or intra- and prestenotic or intra- and poststenotic signals on the ipsilateral side may be of help.

ICA/CCA Index: The index is calculated from the maximal systolic ﬂ ow velocity within the ICA stenosis (V

ICA syst stenosis

within the ipsilateral CCA (V that is independent of general blood ﬂ ow alterations,

) and the maximal systolic ﬂ ow velocity

). It is a parameter

CCA syst

but it only works if the CCA is itself not aﬀ ected by ath- erosclerotic vessel wall changes.

ICA/CCA index = V

ICA syst stenosis/VCCA syst

ICA/ICA Index: The index is calculated from the maximal systolic ﬂ ow velocity within the ICA stenosis (V

ICA syst stenosis

)

122 5 Vascular Pathology

200

150

100

DCBA

Fig. A5.39 Top: Schematic of ﬂ ow pattern in a normal and in an in- creasingly stenosed blood vessel. Bottom: Corresponding Doppler spectra: (A) Preserved systolic window in the unaﬀ ected vessel (ar- row); (B) Turbulent ﬂ ow with spectral broadening and disappearing systolic window but still normal velocity; (C) Turbulent ﬂ ow with in- creased velocity indicating a higher grade of stenosis; (D) Severe turbulent ﬂ ow with retrograde ﬂ ow components and high ﬂ ow velocity.

and the maximal systolic ﬂ ow velocity of the contra- lateral (unaﬀ ected) ICA (V

ICA/ICA index = V

ICA syst contralateral

ica syst stenosis/VICA syst contralateral

It only works if the contralateral ICA shows normal ﬂ ow proﬁ les. Flow velocity measurement should not be per- formed in the carotid bulb but in a straight segment of the unaltered ICA. Because of this limitation the ICA/ ICA index is not commonly used. The angle-corrected intrastenotic ﬂ ow velocities of the ICA may be compared with the ﬂ ow velocities of the distal ICA. To get reliable values the poststenotic ﬂ ow signals should not be dis- turbed and a suﬃ cient length of the distal ICA must be visualized to use angle correction. This index resembles the Lindegaard Index (LI) which is widely used after SAH (see also Case 33). As with the LI, a high ICA/ICA index indicates a more severe stenosis (Alexandrov 2013).

Flow Proﬁ le Alterations—Spectral Broadening: Doppler spectrum analysis of normal blood ﬂ ow classically reveals a laminar ﬂ ow characterized by a systolic window, which means that the highest velocity is in the center of the vessel and the lowest at its wall, best seen in the systolic phase as an “empty” area below the systolic peak. Turbulent ﬂ ow is observed when blood starts to form eddy currents. Turbulence starts early but is usually seen as a progressive d i s a p p e a r a n c e o f t h e s y s t o l i c w i n d o w a t a l o c a l d i a m e t e r reduction of ~50%. Turbulence may also be present without pathologic meaning near sharp changes of ﬂ ow direction, e.g., in vessel bifurcations and loops. Because of their short lengths and smaller sizes this is more often observed in the intracranial arteries and especially in the carotid siphon (Fig. A5.39). Experienced ultrasonographers can also iden- tify turbulence by hearing a disturbed audio signal. In very

Fig. A5.40 Musical murmurs. (A) TCD Doppler spectrum of a highgrade M1-MCA stenosis (peak systolic ﬂ ow velocity >300 cm/s). Note the mirror-image parallel strings as the visual correlate of a musical murmur. (B–D) TCCS Color-mode images and Doppler spectra: (B) Transtemporal approach, midbrain plane showing a high-grade P1-PCA stenosis; (C) Transtemporal approach, midbrain plane demonstrates a functional stenosis at the ACoA; (D) Transtemporal approach, posterior coronal plane showing a highgrade basilar artery stenosis.

high-grade stenosis a harmonic phenomenon, the so-called musical murmur, can be observed. Acoustically it resembles a bird call and is therefore also frequently called the “seagull cry” or “goose cry.” In the Doppler spectrum, mirror-image parallel strings or bands can be observed (see Fig. A5.40 and

Video

A5.7). The phenomenon presumably results from

harmonic frequencies, generated from regular vibrations of the vessel walls caused by the increased blood ﬂ ow veloci- ties. Musical murmurs are usually observed in intracranial stenosis. A recent study reporting on 66 musical murmurs found 94% of murmurs occurring in intracranial vessels and 6% in extracranial vessels (Lin et al 2006). In 88% of cases a high-grade stenosis was detected. In the remaining cases, the musical murmur was found mainly in the communicating intracranial arteries. Here the musical murmur indicates a “functional stenosis,” when blood ﬂ ow is too high for the size of the ACoA or PCoA. As a rule of thumb it can be postulated that whenever a musical murmur is detected in one of the communicating arteries, even if the maximal ﬂ ow ve- locities are not clearly increased, a proximal steno-occlusive process has to be present.

Spectral broadening and musical murmurs, however, are additional and not exclusive criteria for stenosis. They depend on the grade as well as the conﬁ guration of the stenosis and are not mandatory.

Indirect Hemodynamic Assessment

In any case of a suspected or known stenosis, not only the intrastenotic ﬂ ow signal but also the waveforms from ves- sel segments proximal and more importantly distal to a stenosis (prestenotic and poststenotic ﬂ ow pattern) must be analyzed. This distinguishes between stenoses with or without a hemodynamic eﬀ ect (Fig. A5.41 and Fig. A5.42). If the poststenotic ﬂ ow of an ICA stenosis is not visualized extracranially, the C6-ICA and OA may be analyzed for validation of its hemodynamic relevance (Fig. A5.43). By deﬁ ni- tion, stenoses are hemodynamically relevant if they cause a

123Arterial Pathology

Fig. A5.41 Left: Contrast-enhanced MRA, coronal MIP showing a severe extracranial hemodynamically relevant high-grade 90% ICA stenosis. Note the signal void at the stenosis and the collapse of the poststenotic segment of the ICA due to the drop of pressure and reduced volume ﬂ ow. Right: Extracranial duplex, longitudinal view. Doppler spectrum analysis in poststenotic ICA, ﬂ ow velocity 26/5 cm/s (top), intrastenotic ICA, ﬂ ow velocity 360/105 cm/s (middle) and prestenotic CCA, ﬂ ow v e l o c i t y 3 8 / 1 2 c m / s ( bottom). Note the increased pulsatility in the prestenotic CCA and the distinctly delayed systolic ﬂ ow a c c e l e r a t i o n i n t h e p o s t s t e n o t i c I C A .

Fig. A5.42 Extracranial duplex of a hemodynamically relevant ICA stenosis. Longitudinal view, color-mode image, and Doppler spectrum analysis. Top: Shortly after the stenosis (arrow) a serrated ﬂ ow signal indicates relevance of the stenosis. The acceleration time (AT) is normal: 50 milliseconds. Bottom: Insonation further distal reveals an obvious poststenotic ﬂ ow pattern with prolonged AT (120 milliseconds). For further reading on the AT see below.

Fig. A5.43 (A) Extracranial duplex, longitudinal view. Doppler spectrum analysis showing a proximal ICA stenosis (ﬂ ow velocity: 414/181 cm/s). (B) TCCS, color-mode image and corresponding Doppler spectrum analysis, transtemporal axial insonation, lower pontine plane. Poststenotic ﬂ ow pattern and reduced ﬂ ow velocity in the C6-ICA (24/13 cm/s). (C) TCCS, transorbital approach, colormode image and corresponding Doppler spectrum analysis reveal-

Fig. A5.44 Flow pattern distal to a hemodynamically relevant VA ste nosi s. ( A) Increased ﬂ ow velocity in a distal V1-VA stenosis (257/46 cm/s). (B) Turbulent ﬂ ow in the proximal V2-VA between C5 and C6 (69/17 cm/s). (C) Mild poststenotic ﬂ ow pattern in the mid V2-VA between C3 and C4 (108/34 cm/s, AT 136 milliseconds). (D) Apparent poststenotic ﬂ ow pattern in V3-VA (53/23 cm/s, AT 200 milliseconds).

ing an OA ﬂ ow signal similar to C6-ICA (15/6 cm/s).

124 5 Vascular Pathology

Fig. A5.45 TCCS, Doppler spectrum analysis of normal M1-MCA (1) and moderate (2,3) to severe (4) and pseudo-venous (5) poststenotic ﬂ ow pattern.

reduced blood volume ﬂ ow and poststenotic pressure drop. According to the Spencer’s curve discussed earlier, this occurs if the diameter is decreased by more than 70–80% or the cross-sectional area is reduced by 90–95%. Archie and Feldtman (1981) found similar results, suggesting that relevant blood ﬂ ow reduction of 40% begins at 75% diameter stenosis or 94% area stenosis. Considering waveform appearance together with ﬂ ow velocities will therefore help to recognize a hemodynamically relevant stenosis.

Note that the terminology for pre- and poststenotic ﬂ ow signals is not well standardized. In this book, we use the terms pre- and poststenotic ﬂ ow pattern for detecta- ble proximal or distal ﬂ ow signal alterations in stenoses and occlusions.

The prestenotic ﬂ ow pattern comprises a mostly nor- mal systolic ﬂ ow velocity and always a normal rise in systolic ﬂ ow. However, distal ﬂ ow obstruction leads to raised peripheral resistance, reduced prestenotic diastolic ﬂ ow, and subsequently raised pulsatility. In cases with an unclear cause of the distal ﬂ ow obstruction (occlusion or stenosis) but highly pulsatile ﬂ ow signals, the term “high-resistance ﬂ ow pattern with increased pulsatility” might be more appropriate.

A poststenotic ﬂ ow pattern requires a relevant proximal obstruction of at least 70–80%, which then leads to the phenomenon of delayed systolic acceleration. For assessment of a poststenotic ﬂ ow pattern, the insonation has to be per- formed at a certain distance from the stenosis to avoid signal artifacts caused by severe turbulence. The poststenotic ﬂ ow may also become more obvious in the run of a vessel with a long course. This can also be observed in proximal VA st en os es w he n t he V 2 s eg m en t r ev ea ls no o bv io us d elayed systolic increase, but this becomes evident in its V3 or V4 segments (Fig. A5.44). A reduced blood ﬂ ow results in a compensatory dilatation of the resistance vessels to avoid downstream hypoperfusion. As a consequence the total arterial cross-sectional area increases, with subsequent reduction of the peripheral resistance causing a raised diastolic ﬂ ow component and reduced pulsatility. For these

Fig. A5.46 TCCS, Doppler spectrum analysis of normal M1-MCA and M1-MCA of a patient with an ipsilateral ICA occlusion revealing typical signs of a poststenotic ﬂ ow pattern. Top: Reduced blood ﬂ ow velocity 42/24 cm/s versus 137/44 cm/s. Middle: Prolonged acceleration time (AT) 120 milliseconds versus 56 milliseconds. Bottom: Reduced pulsatility index (PI 0.59 versus 0.88).

ﬂ ow patterns, terms such as “blunted ﬂ ow,” “low-resistance ﬂ ow,” “tardus parvus waveform” or, in case of distinct al-

terations, “venous-like ﬂ ow” can be used (Fig. A5.45). The delayed systolic acceleration (delayed upstroke/upslope) as integral part of the poststenotic ﬂ ow pattern can be quan- tiﬁ ed by the acceleration time (AT), measured from the onset of systole to the ﬁ rst peak systole. The AT is widely used in renal artery stenosis to diagnose hemodynamically signiﬁ cant diseases, with 70 ms generally considered as the cut-oﬀ . An AT of >100 ms has a sensitivity of 32% and a speciﬁ city of 100% in diagnosing a hemodynamically rele- vant renal stenosis (Motew et al 2000). AT analysis may also be of interest in neurosonology, but here its use is not yet well established. In clinical practice a visual comparison of homologous vessel segments appears to be adequate.

Besides delayed systolic ﬂ ow acceleration and a con- comitantly increased diastolic ﬂ ow, reduced ﬂ ow velocities are usually present as signs of a hemodynamically compromised poststenotic ﬂ ow (

Fig. A5.46). R

educed or nor

mal ﬂ ow velocities help to distinguish real poststenotic ﬂ ow from similar patterns which may be seen in hyperperfused vessels like feeders of dural arteriovenous ﬁ stulas and ar- teriovenous malformations (AVMs) or otherwise normal vessels that serve as collaterals in major vessel occlusions (see Fig. A5.35). General low-resistance ﬂ ow patterns in all brain-supplying arteries may be also seen in severe aortic valve stenosis.

To obtain the greatest diagnostic certainty in everyday clinical practice, we recommend that signals in an assumed stenosis should be obtained from all three vessel segments (prestenotic, intrastenotic, and poststenotic) whenever possible. The above criteria are of special signiﬁ cance when performing serial measurements over long periods to detect disease progression. For instance, if initially absent indirect hemodynamic criteria develop over time, an increase of the stenosis to a range of at least 80% is likely. Assessment of only intrastenotic ﬂ ow velocities alone is problematic, as velocities may even decrease with increasing grade of stenosis (see the Spencer’s curve, Fig. A5.34).

ICA

125Arterial Pathology

ECA

Fig. A5.47 Left: Contrast-enhanced MRA, coronal MIP showing an ICA stenosis. The ICA was considered to reveal only wall irregularities. Top r igh t: Extracranial duplex, color-mode image, cross-sectional plane: Area reduction according to a 65% stenosis (left), diameter reduction according to a 50% stenosis (right). Bottom right: Color- mode image and corresponding Doppler spectrum analysis revealing a nonturbulent ﬂ ow with normal velocities of 72/22 cm/s.

Ultrasound Criteria of Occlusions

Direct Morphologic Assessment

Extracranial B-mode duplex ultrasound may reveal complete ﬁ lling of the vessel lumen with thrombotic material of varying echogenicity (see Video

A5.8). In chronic

occlusion, precise vessel identiﬁ cation and diﬀ erentiation of the vessel lumen might be diﬃ cult. A fresh thrombotic occlusion usually presents with hypoechoic thrombotic material. In contrast to a recent occlusion, a chronic occlusion may demonstrate a reduction or loss of vessel distensibility which deﬁ nes variation of diameter during the systolic and diastolic phase (Alexandrov 2013). B-mode insonation alone, however, is not suﬃ cient for diagnosis of occlusion. It should always be combined with colormode and Doppler spectrum analysis.

Direct Hemodynamic Assessment

Occlusions result in a complete absence of color-ﬂ ow signal, even after adjustment for very low ﬂ ow signals (lowest PRF and increased color gain settings). Doppler spectrum analysis reveals no ﬂ ow signal. In cases with a proximal vessel stump, a distinctly reduced, alternating ﬂ ow pattern with a short systolic peak and a small retrograde ﬂ ow component (“stump signal” or “to-and-fro signal”) can be found. Diagnostic certainty may be increased by using intravenously administered ultrasound contrast agents. On transcranial insonation, a missing ﬂ ow signal does not necessarily imply occlusion. For example, the P1-PCA segment might be absent due to P1 hypo- or aplasia in case of a fetal-type PCA. The A1-ACA segment might also be missing in distinct hypo- or aplasia. In these circumstances, indirect hemodynamic criteria might help to distinguish normal anatomic variants from pathologic ﬁ ndings.

Fig. A5.48 Distal ICA stenosis. Color-mode, longitudinal plane, composed image. Aliasing and lumen reduction is visible ~2 cm distal of the ICA bifurcation (arrow) indicating ICA stenosis. Doppler spectrum reveals increased velocities (top left: 265/87 cm/s). The proximal ICA itself showed low velocities (bottom right: 18/6 cm/s).

ﬂ ow proﬁ les proximal and distal to the occlusion (see also “Ultrasound Criteria of Stenoses” above). Because of the ability of collateral vessels to bypass occlusions, their detection and consideration of their capacity is of paramount importance in the acute and chronic state after stroke (for further details see also “Collateral Pathways” below).

Extracranial Pathology

Extracranial Anterior Circulation

ICA Stenosis

Auscultation with the stethoscope can be considered as an inadequate screening method as it detects only 25% of ICA stenoses and has a high number of false-positive ﬁ nd- ings: 10% are not conﬁ rmed by conventional angiography (Ziegler et al 1971).

Since a variety of alternative invasive, less invasive, and noninvasive imaging methods are available that permit visualization of vessel pathology in vivo, the evaluation of ICA pathology and grading of ICA stenosis has been and remains a matter of extensive debate. A special anatomic variant of the ICA which hinders a simple interpretation of stenoses in each modality, unlike other brain-supplying arteries, is the variable widening of the carotid bulb. ICA stenoses of atherosclerotic origin are mainly located just at this site, which is explained by the nonlinear ﬂ ow at the bifurcation. In meth- ods primarily outlining the intraluminal patency a relevant bulb stenosis may be underestimated. In particular, homogeneous noncalciﬁ ed plaques may have a smooth surface and may be completely overlooked in catheter or MR angiography (Fig. A5.47). Precise analysis of vessel lumen reduction within this region is therefore a challenge for all currently available imaging methods. ICA dissections usually alter the ICA in its more distal parts but atherosclerotic lesions may also aﬀ ect the ICA at more atypical distal sites (Fig. A5.48).

Indirect Hemodynamic Assessment

In occlusion, the same criteria as for hemodynamically relevant high-grade stenoses can be applied for the analysis of

Grading of ICA Stenosis by Digital Subtraction Angiography

Evaluation of stenoses and occlusions has so far been

126 5 Vascular Pathology

ICAECA

CCA

Fig. A5.49 Schematic of an ICA stenosis, similar to the images derived from DSA. Illustration of three angiographic methods to determine the grade of ICA stenosis. Note that the ECST method uses an “eyeball” estimate of the nonvisible outer wall of the ICA at the carotid bulb (dashed gray line). Comparative analysis of the three methods yielded a linear relationship, allowing an estimated conversion.

NASCET (D – B) / D x 100%

ECST (C – B) / C x 100%

CC (A – B) / A x 100%

Conversion NASCET (%) = (ECST – 40%) / 0.6

(CC – 40%) / 0.6%

dominated by the ﬁ rst available method: conventional angiography. Several important clinical trials have been based on angiographic data, the results of which form the basis for current treatment decisions in carotid stenosis. The European Carotid Surgery Trial (ECST Collaborative Group

1991) and the North American Symptomatic Carotid Endarterectomy Trial (NASCET Collaborators 1991) compared medical treatment and carotid endarterectomy (CEA) in patients with diﬀ erent grades of symptomatic ICA stenosis. They found that patients with stenoses between 70% and 95% signiﬁ cantly beneﬁ t from the surgical intervention. However, the two studies used diﬀ erent approaches to de- termine the grade of stenosis. The NASCET study used the diameter of the unaﬀ ected distal ICA and the narrowest stenosis diameter for calculation of stenosis (distal grade of stenosis). The ECST used the stenosis diameter and the estimated diameter of the nonvisualized outer walls of the ICA stenosis (local grade of stenosis). A third method, deﬁ ning the grade of stenosis between the stenosis diameter and the proximal unaﬀ ected CCA (CC method) has not yet been used in a large clinical trial (de Bray and Glatt 1995) (Fig. A5.49). Currently treatment decisions on whether or not to perform CEA rely on the NASCET and ECST data. Although numerically identical, a 70% NASCET ICA stenosis is not equal to a 70% ECST ICA stenosis. Rothwell and co workers compared NASCET and ECST grades of stenosis and found a linear correlation which allows an estimated conversion between the two approaches (Rothwell et al 1994):

NASCET (%) = (ECST − 40%)/0.6

The same relationship can be applied to the CC criteria:

NASCET (%) = (CC − 40%)/0.6

CBA

Fig. A5.50 DSA, selective CCA injection, lateral view. (A–C) Po- tential error in ICA stenosis estimation using the ECST method. Diﬀ erent estimates of the presumed carotid sinus will result in a calculated grade of stenosis increasing from A to C. Diameter of stenosis: 3.3 mm. Diameter of the carotid bulb, assessed by duplex ultrasound: 9.2 mm. Resulting degree of stenosis: 64%, best corresponding to the estimate in C.

(Al exa nd rov et a l 199 3) . The N AS CET a ppro ach i s una ble to account for low-grade stenosis as a 40% ECST stenosis equals 0% NASCET, and, for example, a 30% ECST stenosis translates to an absurd –17% NASCET stenosis. The ECST approach, on the other hand, relies on an “eyeball” estimation of the presumed carotid bulb diameter, which has the potential for considerable error (Fig. A5.50 and Fig. A5.51). To reduce this error some authors use the carotid stenosis index, which is largely based on a publication by Williams and Nicolaides, who found a ﬁ xed carotid bulb to proximal CCA ratio of 1.2 in 96% of 61 angiograms of presumably normal carotid bifurcations (Williams and Nicolaides 1987). Use of this ratio certainly improved the comparability between both angiographic methods but did not improve their diagnostic accuracy. In fact other studies found an ICA/CCA ratio ranging from 0.7 to 1.4 (Rothwell et al 1994). A CTA approach has questioned a ﬁ xed ICA/CCA ratio (Bartlett et al 2007).

Considering these shortcomings, it is surprising that DSA has so far remained the diagnostic gold standard with which all other methods have to compete. The relevance of extended meta-analyses which try to analyze sensitivity and speciﬁ city values for the less invasive methods (duplex ultrasound, MRA, CTA) in comparison to DSA (Patel et al 2002, Wardlaw et al 2006a) is also questionable. As with all other nonangiographic methods, the duplex ultrasound ﬁ ndings have to be “imported” into the angio graphic scales. Continuous-wave Doppler sonography, in contrast, can no longer be recommended because of its low diagnostic accuracy. For instance, in a comparative Doppler and angiographic study that aimed to identify patients with ICA stenoses >60% (NASCET criteria), the Doppler technique yielded 41% false-positive results (Qureshi et al 2001). For further details, see Case 1.

Following this conversion, a 70% ECST ICA stenosis is equivalent to a 50% NASCET stenosis. Despite this correlation and the positive ﬁ ndings in the above two clinical studies, both approaches have considerable methodological problems

Grading of ICA Stenosis by Duplex Ultrasonography

Duplex ultrasonography allows the grading of ICA stenosis according to the ECST or NASCET criteria, so ultrasound reports should always specify the classiﬁ cation system used.

127Arterial Pathology

ICA

ECA

Fig. A5.51 Extracranial duplex corresponding to the DSA in Fig. A5.50. (A) B-mode image, longitudinal plane: Large, mildly hypoechoic structure in the carotid bulb as well as at the ECA origin. (B) Color- mode, cross-sectional plane: Following the ECST criteria, the diameter of the vessel (9.2 mm) and the residual lumen (3.3 mm) are assessed, resulting in a 64% stenosis. (C) Color-mode, longitudinal plane: Clear delineation of the remaining perfused lumen and conﬁ rmation of the plaque extension. (D) Doppler spectrum analysis. Flow velocity 185/102 cm/s, indicating local stenosis, grade 60–70%.

ICA

ECA

The ultrasound technique works at its best if the local grade of stenosis is assessed, i.e., if the ECST grades are measured by direct analysis of cross-sectional area or lumen reduction. The most conﬁ dent results can be achieved in low and moderate stenoses with up to 50% lumen reduction (Fig. A5.52). The distal ICA lumen, required for NASCET grading, is usually diﬃ cult to assess. However, the NASCET criteria have become the current base for clinical decision-making worldwide. The Neurosonology Research Group of the World Federation of Neurology (NSRG) has therefore proposed adapted duplex criteria, which are able to deﬁ ne stenoses according to the NASCET system by us- ing a multiparametric approach (von Reutern et al 2012). With increasing grade of stenosis there is a shift of importance from B-mode imaging to velocity measurements and ﬁ nally hemodynamic parameters. To achieve this goal, all morphologic as well as direct (ﬂ ow velocities) and indirect hemodynamic information (collateral ﬂ ow, poststenotic ﬂ ow pattern) needs to be considered by also including orbital and intracranial ﬂ ow parameters. In the following, we present our recommendations for the grading of ICA stenoses which are mainly based on the NSRG criteria.

B-mode and color-mode imaging, especially in the cross-sectional plane, are the most important parameters in low-grade bulb stenoses <50% as usually no obvious velocity increase is present (see Fig. A5.11). Here we rec- ommend describing the lumen reduction in local grades and to start diagnosing a stenosis from a 30% narrowing onwards, stepwise in 10% steps up to a 50% stenosis. The calculated stenosis according to the NASCET criteria may additionally be reported. In a local stenosis between 50% and 60% (NASCET 15–35%), the main criterion is a velocity increase without indirect signs of collateral ﬂ ow or of poststenotic ﬂ ow pattern. In local stenoses of more than 80% (NASCET 70%), indirect hemodynamic criteria are the dominant parameters demonstrating a collateral ﬂ ow via alternative pathways (retrograde ophthalmic ﬂ ow, cross-

ECA ECA

pICA

dICA dICA

Fig. A5.52 Extracranial duplex, color-mode image, cross-sectional plane, ICA bulb stenosis. (A,B) ICA bulb with a diameter reduction from 10.8 mm to 4.6 mm leading to a 57% local stenosis (A) and an area reduction from 32.7 mm stenosis (B). (C,D) Distal ICA on the same side with a diameter of 6 mm and an area of 28.9 mm NASCET of 23%.

to 15.9 mm2 which results in a 51%

resulting in a stenosis according to

pICA

ﬂ ow via ACoA or PCoA or leptomeningeal collateral ﬂ ow), and/or a poststenotic ﬂ ow pattern characterized by a pro- longed AT and/or decreased pulsatility index (PI) in the distal ICA, and/or a prestenotic ﬂ ow pattern in the CCA with increased pulsatility. A comparison with the unaﬀ ect- ed side by eyeball estimate is necessary to prove a pre- or poststenotic ﬂ ow pattern. The ICA/CCA, ICA

or ICA

lateral

ond-line criteria. However, these are less frequently used

intrastenotic

/ICA

indices may be useful as sec-

poststenotic

ipsilateral

/ICA

contra-

in our daily routine and their importance should not be overestimated. This means, in case of conﬂ icting ﬁ ndings, ﬁ rst-line criteria (one or more signs of a hemodynamic compromise, such as collaterals or a poststenotic ﬂ ow pat- tern) overrule second-line criteria such as the above-mentioned ratios. If a collateral ﬂ ow is clearly documented, a hemodynamically relevant stenosis is proven irrespective of the measured intrastenotic ﬂ ow velocity.

For exact grading, the highest velocity within a stenosis should be identiﬁ ed. Depending on the conﬁ guration of the stenosis this point can be at its origin (most frequent location) but also more distal, as often seen in case of dissections. In most cases a direct assessment of the highest velocities is possible; however, evaluation may be hindered or may even be impossible if severe plaque calciﬁ cation and subsequent acoustic shadowing are pres- ent. The latter is found in up to 7% of cases (Polak et al

1989) (Fig. A5.53). A deeply located vessel or an angulated vessel course may also impair the visualization of a stenosis. Velocity measurements should be performed with the lowest possible angle of correction (see also Chapter 1, “Doppler Shift and Flow Velocity” under “Ultrasound Principles”), following the jet of the ﬂ ow and not the ana- tomic course of the aﬀ ected vessel (Fig. A5.54). If present, prestenotic ﬂ ow alterations in the distal CCA are easily detectable (Fig. A5.55). Extracranial measurements distal to the stenosis are often hindered if the bifurcation is near the mandible or if the stenosis extends over a

128 5 Vascular Pathology

Fig. A5.53 Extracranial duplex, color-mode image, longitudinal view. (A,B) Examples of a distinct acoustic shadowing phenomenon caused by calciﬁ ed ICA plaques impeding assessment of ICA ﬂ ow. Shortly distally a ﬂ ow signal can be detected (B).

long segment distance. In some of these cases, the distal extra cranial ICA can be assessed in the axial plane. Unfortunately in this plane the angle of insonation is not well deﬁ ned and reliable velocity measurement cannot be performed. However, spectrum analysis may still be sufﬁ cient to identify a poststenotic ﬂ ow pattern and some- times there are also perivascular color artifacts, mainly during systole, surrounding the stenotic vessel (the “confetti eﬀ ect;” see also Fig. A1.45). Alternatively, the ﬂ ow pattern of the intracranial ICA below the communicating arteries, preferably at the C6-ICA segment (Fig. A5.56, top), or the OA if anterograde and not activated as a collateral vessel itself (Fig. A5.57) may show a poststenotic ﬂ ow pattern, illustrating the hemo dynamic relevance of an extracranial ICA stenosis. The ipsilateral MCA and ACA may also be analyzed. However, in their assessment it has to be considered that collateral ﬁ lling might have already occurred via ACoA, PCoA, and/or OA, and the observed MCA and ACA waveforms might no longer reveal the poststenotic ICA ﬂ ow pattern (Fig. A5.56, bottom). In the case of a collateral ﬂ ow via the PCoA, the ACA might show a more distinct poststenotic ﬂ ow pattern compared with the MCA which can be best explained by a functioning ACoA and a patent contralateral A1-ACA ensuring ﬂ ow to both ACA territories (Fig. A5.58). A synopsis of recommended duplex ultrasound criteria for grading of a proximal ICA stenosis considering the multiparametric approach of morphology, direct and indirect ﬂ ow parameters based on the NSRG criteria (von Reutern et al 2012) is given in Fig. A5.59. Particularly important are the threshold values which deﬁ ne an ICA stenosis >50% according to the NASCET criteria. The NSRG recommended using the relatively low USA threshold values (see below). However, they also added an analysis of data from ﬁ ve DSA-correlated studies including 977 stenoses, which together revealed higher average peak systolic ﬂ ow ve- locities. Interestingly, the latter are closely equivalent to the threshold values usually used in European countries.

Fig. A5.54 Extracranial duplex, color-mode image, longitudinal plane. Image of a high-grade ICA stenosis with lumen reduction and color-aliasing at the stenosis. Direction of the ﬂ ow stream (“jet”) and vessel course is not equivalent, complicating the e x a c t p l a c e m e n t o f t h e a n g l e c o r r e c t i o n . ( A) Inappropriate angle correction placement following the vessel course (398/197 cm/s). (B) Preferred placement following the ﬂ ow jet within the stenosis resulting in a diﬀ erent velocity (270/128 cm/s).

Fig. A5.55 Assessment of pre- and poststenotic blood ﬂ ow in the CCA, proximal ICA, and distal ICA. Left: Dop pler sp ect ra in unaﬀ ect- ed vessels. Right: Flow patterns in a >80% ICA stenosis (ECST criteria): Prestenotic ﬂ ow pattern in the CCA with reduced ﬂ ow velocity and increased pulsatility (bottom), intrastenotic elevated ﬂ ow ve- locity and spectral broadening (middle), poststenotic ﬂ ow pattern in the distal ICA with reduced ﬂ ow velocity, pulsatility and delayed systolic ﬂ ow acceleration (top). Note the distal ICA collapse.

It seems therefore more reasonable to use these average velocities as threshold values for grading of ICA stenosis in addition to the indispensable indirect hemodynamic marker. The 90% grade according to NASCET (95% according to ECST) represents the speciﬁ c ﬁ ndings in near-oc- clusion. Ultrasound reports should always state the classiﬁ cation system used. This approach, including a grading in 10% steps, is used in many European centers and is well accepted as it has been shown to be a reliable approach if applied by experienced sonographers (Dippel et al 1997). In North America the intracranial and intraorbital ﬂ ow parameters are normally not analyzed and therefore the grading of ICA stenosis is mainly based on intrastenotic

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