Добавил:
Sekretar
kiopkiopkiop18@yandex.ru
t.me/Prokururor I Вовсе не секретарь, но почту проверяю
Опубликованный материал нарушает ваши авторские права? Сообщите нам.
Вуз:
Предмет:
Файл:Ординатура / Хирургия / Библиотека им академика М.И. Перельмана / Книга_5773_Библиотеки_им_академика_М_И_Перельмана.pdf
Intracranial Pathology 95
Tab l e A5 .3 Ultrasound grading of intracranial stenoses (modified from Baumgartner et al. 1999). Flow velocities are given in cm/s. In high-
grade stenosis, the opportunity to analyze pre- and/or poststenotic signals strongly depends on the localization (proximal or distal) of the
stenosis and might not always be obtainable
Stenosis < 50 % mild 50–80 % moderate > 80 % high
Middle cerebral artery ≥ 155 ≥ 220 distal M1 / M2-MCA poststenotic fp
Anterior cerebral artery ≥120 ≥ 155 A2-ACA poststenotic fp
Posterior cerebral artery ≥ 100 ≥ 145 distal PCA poststenotic fp
Basilar artery ≥ 100 ≥ 140 distal BA/PCA poststenotic fp
Vertebral artery ≥ 90 ≥ 120 distal VA/BA poststenotic fp
Fp = flow pattern; ∕ increased flow velocity as collateral sign
A1-ACA and/or P1/P2-PCA ∕
ipsilateral M1-MCA and/or contralat. A1 ∕
ipsilateral M1-MCA ∕
VA/proximal BA prestenotic fp
VA extracranial prestenotic fp
Occlusions
Occlusions are characterized by missing color and Doppler
flow signals at the site of the occlusion or reduced flow
signals in vessel segments proximal to the occlusion. The
reduced flow signals are usually caused by the remaining
blood flow into small perforating arteries or vessel
branches located proximal to the occlusion. The finding
of a residual flow may cause confusion to the sonographer
as to whether or not and at which site an occlusion is
present.
Most evaluations concerning intracranial occlusions are
reported in patients with acute stroke. The DIAS I (Duplex
Sonography In Acute Stroke) study analyzed the ability of
duplex ultrasound to diagnose main stem arterial occlusions within the anterior circulation within a 6-hour time
window. Diagnostic certainty of the sonographers varied
from 50 % to 60 % of studied vessels in unenhanced TCCS
but reached 80–90 % after intravenous contrast administration (Gerriets et al. 2002). These findings suggest that
thequalityofthebonewindow,i.e.,theinsonationconditions, determine whether a sufficient transcranial evaluation can be achieved. For Doppler spectrum analysis in
occlusion and evaluation of reperfusion patterns after
thrombolysis, a grading system similar to the TIMI criteria
(Thrombolysis In Myocardial Ischemia)—the TIBI grading
system (Thrombolysis In Brain Ischemia) has been developedforuseinacutestroke(Demchuketal.2001).Itdifferentiates the following grades of ischemia (Fig. A5.43):
Fig. A5.42 Schematic drawing of stenosis locations where efficient
collateral pathways may prevent the development of raised flow
velocities (VA, P1-PCA, A1-ACA) and which might therefore be
underestimated or even overlooked (arrows). At other locations
(ICA,M1-MCA,M2-MCA,A2-ACA,P2-PCA,P3-PCA),astenosis
will always result in raised flow velocities, provided that a sufficient
prestenotic perfusion pressure exists (circles)
• Grade 0: absent flow.
• Grade 1: minimal flow.
• Grade 2: blunted flow.
• Grade 3: dampened flow.
• Grade 4: stenotic flow.
• Grade 5: normal flow.
(TIBI 0 and 1 refer to proximal occlusion, TIBI 2 and 3 to
distal occlusion and TIBI 4 to recanalization.)
Applying these criteria in acute stroke the TIBI classification correlates with initial stroke severity, clinical recovery, and mortality in patients treated with recombinant
tissue plasminogen activator (rt-PA) (Demchuk et al.
2001). Also, the grading system can be used to analyze
5 Vascular Pathology96
Fig. A5.43 Ultrasound Thrombolysis In BrainIschemia (TIBI) grading
system according to Demchuk et al. (2001).
Intracranial Anterior Circulation
ICA—Stenosis
A grading system for intracranial ICA stenoses does not yet
exist. This is mainly due to the complex and tortuous
anatomic course of the artery and the unfavorable insonation angle via the transtemporal bone window, which
hinder optimal vessel visualization as well as exact placement of an angle correction. It is important to insonate all
transcranially accessible segments to avoid overlooking a
stenosis which might be also found in its most proximal
location at the C5 and C6 segments (Fig. A5.44). For steno-
sis identification in this region we recommend looking not
only for differences in velocity between the two sides but
also for differences in turbulence. Stenoses > 70–80 % will
result in the activation of collaterals (ACoA or PCoA) which
can be depicted. Depending on the grade and the location
of the stenosis (infra- or supraophthalmic) the proximal
extracranial ICA flow may show more or less prestenotic
flow alterations. Problems may arise in intra- and extracranial ICA tandem stenoses. In case of a hemodynamically
relevant extracranial stenosis, flow in the distal intracranial stenosis may be so reduced that the distal stenosis
might be underestimated. If the distal stenosis dominates,
the proximal stenosis will also be underestimated. For
further details about intracranial ICA stenosis see Cases 9
(p.171), 14 (p. 210), and 30 (p. 338).
Fig. A5.44 Left: DSA, selective CCA injection, lateral view. C6-ICA
stenosis (arrow). Right: TCCS, transtemporal approach, axial lower
pontine plane. Color-mode visualization of the horizontal C6-ICA
segment revealing a turbulent flow with raised velocity (199/
50 cm/s).
recanalization patterns, for example, during thrombolysis,
where it has been shown that the duration of recanalization correlates with the clinical outcome (Alexandrov et al.
2001). For further details, see Case 10 (p. 176).
ICA—Occlusion
Long segmental intracranial ICA occlusions are usually
characterized by an absent color signal. In proximal occlusion, however, filling of the carotid siphon may occur via
the OA or PCoA. In distal ICA occlusion an orthograde flow
from the proximal C6-ICA segment to the carotid siphon—
further draining into the OA—may be seen. However, more
easily demonstrated are the indirect pre- and poststenotic
signs of ICA occlusion, which may vary depending on the
location of the occlusion. Extracranial ICA analysis is of
great importance as a reduced flow velocity, and an increased pulsatility can be expected in most cases. This also
facilitates differentiation between infraophthalmic (below
the origin of the OA), which usually leads to a flow signal
without a diastolic flow component, and supraophthalmic
(above the origin of the OA) ICA occlusion. The latter is
characterized by a remaining diastolic flow component,
resembling OA flow. In the rare occasion of a prominent
PCoA the extracranial ICA flow signal may appear only
mildly reduced, despite a distal occlusion above the origin
of the PCoA (Ta b l e A5.4).
MCA—Stenosis
Stenoses of the M1-MCA can be graded according to flow
velocity, turbulence, and asymmetry into mild, moderate,
and high-grade stenoses (Table A 5 . 3). The latter requires
Intracranial Pathology 97
Tab l e A5 . 4 Synopsis of hemodynamic effects of ICA and MCA occlusions depending on the localization of the occlusion. A–EFindingsina
normally developed circle of Willis. F Variant with a strong early temporal MCA branch. G–HFindingsinfetal-typePCA
ICA extracranial A1-ACA M1-MCA P1/2-PCA
Normal Normal Normal or reduced Normal
A
Normal or reduced Normal or raised Reduced Normal or raised
B
Reduced Raised or normal No flow Raised or normal
C
OA-like flow No flow No flow Raised or normal
D
Stump signal or no flow Retrograde or
E
Normal or reduced Normal or raised Reduced or normal Normal or raised
F
Normal or reduced Raised or normal No flow Raised or normal
G
Reduced Noflow Noflow Raised
H
the analysis of available pre- and poststenotic vessel segments. If the stenosis is located within the M1-MCA segment signals should be obtained from the M2 segment
which in high-grade stenosis might show a poststenotic
flow pattern, sometimes even with a venouslike flow signal. In high-grade proximal MCA stenosis, activation of
collaterals (ipsilateral A1-ACA, and P1-PCA via leptomeningeal collaterals (LMC) may be observed (for collateral
activation, see “Collateral Pathways,” p.101). TCCS analysis
of the MCA should, however, not only be carried out to
analyze potential poststenotic flow patterns but primarily
reduced
Reducedornormal Raisedornormal
to search for a stenosis itself. Therefore, all available, i. e.,
detectable MCA segments, should be insonated. A frequently overlooked location of stenosis by all diagnostic
modalities is the transitional region between M1- and M2MCA or a proximal MCA branch itself (Fig. A5.45). There
are no normal values or cut-off velocity criteria for the M2MCA. If a turbulent flow is detected with a flow velocity
higher than in the main stem of MCA a stenosis seems very
likely. M1-MCA near occlusion has not been reported of
but similar findings compared to extracranial ICA near
occlusion can be expected. For further details about MCA
5 Vascular Pathology98
Fig. A5.45 TCCS, transtemporal approach, axial midbrain plane.
A Normal Doppler signal fromthe mid-M1-MCA segment in a depth
of 50mm (flow velocity: 73/39 cm/s). B Doppler signal from a prominent M2-MCA branch of the same case with turbulent flow and
raised flow velocities in a depth of 43 mm (flow velocity: 225/
122 cm/s) indicating a proximal M2-MCA branch stenosis.
Sometimes a hyperechogenic B-mode signal can be observed which might correspond to MCA main stem occlusion (Kadimi et al. 2000) (Fig. A5.46). In occlusions of the
middle part of the MCA, a small orthograde flow with
increased pulsatility may be present depending on a residual blood flow into lenticulostriate perforating arteries.
In distal M1-MCA occlusion a distinctly reduced flow velocity is present with variable pulsatility depending on the
presence and the diameter of an early temporal branch. In
this special anatomical situation the analysis of flow distribution and the assessment of vessel pathology may be
difficult. Distal MCA occlusion, e. g., of a relevant M2-MCA
branch or more than one M2 branch, will result in a reduced flow with low velocities and a marked bilateral
asymmetry (Zanette asymmetry index) (for further reading see also case 13). Raised flow velocities in the A1-ACA
or P2- and P3-PCA segments indicate flow diversion with
leptomeningeal flow toward the MCA territory (for further
details about LMC flow, see “Intracranial Collateral Pathways in ICA Occlusive Processes,” p.105). In most cases the
occlusion of a single M2-MCA branch will not cause detectable flow alterations in the proximal vessel segments
and may therefore be overlooked but is also often missed
by the other diagnostic modalities. A special situation
arises in distal M1-MCA occlusion if a prominent early
temporal branch is present—which complicates the analysis of flow distribution and the assessment of vessel
pathology. The hemodynamic effects of MCA occlusion in
relation to its location are presented in Table A 5 . 4 .For
further details about MCA occlusion, see Cases 10
(p.176), 17 (p. 231), and 25 (p. 297) and for MCA occlusion
and early temporal branch see Case 22 (p. 269).
Fig. A5.46 A, C CTA, axial MIP. B, D TCCS, transtemporal approach,
axial midbrain plane, color-mode. A Left M1-MCA occlusion with
absent contrast filling (arrows) and prominent PCA (arrow).
B Corresponding TCCS color-mode image. Absent MCA color signal.
Instead, a slight B-mode hyperechogenic area indicates MCA occlusion (“hyperechogenic media sign”)(arrows).Strongcolor-flowsignal within the P2-PCA (arrow). C CTA of the same patient flipped
horizontally in analogy to the TCCS image in (D). Note the present
contralateral MCA signal as well as a normal PCA (arrow).
D Corresponding TCCS color-mode image of the right side with
normalMCAandPCA(arrow).
stenosis, see Cases 5 (p.149),17(p. 231), 24 (p. 287), and 30
(p. 338), and for MCA near occlusion, see Cases 25 (p. 297)
and 30 (p. 338).
MCA—Occlusion
Depending on the location of the occlusion, the Doppler
spectrum may be completely absent or reduced. In case of
a proximal M1-MCA occlusion no flow signal is seen.
ACA—Stenosis
For evaluation of the A1-ACA segment, differences between the right and left sides cannot be used as criteria
of stenosis as physiologic diameter differences are a frequentfinding(forACAanatomy,seeChapter2,“Intracranial Arteries,” p. 24). Furthermore, a unilateral A1-ACA
stenosis may not cause raised flow velocities because of
asufficient collateral compensation via the contralateral
A1-ACA segment and ACoA and may therefore be difficult
to detect. In any other instance A1-ACA stenoses may also
be evaluated according to flow velocity and the presence of
turbulences (Tabl e A 5 .3). Using modern ultrasound systems, distal assessment of the A2-ACA segment is possible
in some cases, allowing to search for poststenotic flow
alterations or stenoses of the A2-ACA segment itself. For
further details about ACA stenosis, see Case 9 (p. 171).
ACA—Occlusion
The variability of ACA anatomy may also hinder a clear
differentiation between aplasia and occlusion. In such
cases all available clinical information should be taken
into account. If the patient has an acute leg paresis con-
tralateral to the missing A1-ACA segment and ipsilateral
M1-MCA flow velocities are slightly raised (indicating leptomeningeal activation), then an A1-ACA occlusion seems
rather likely. Direct TCCS assessment of A2-ACA occlusions
has not yet been reported.
Intracranial Posterior Circulation
PCA—Stenosis
PCA stenosesmay be graded according to the magnitude of
observed flow velocities and the presence of turbulence
(Tab l e A 5 .3). As the P2- and P3-PCA segments are usually
symmetrically developed, differences between the right
andleftsidesmayalsobeconsideredinthesesegments.
Although there are no extensive data regarding the latter,
similar to MCA pathology the same criteria of at least
30 cm/s flow velocity difference as a cut-off can be used
to differentiate between physiologic and pathologic differences. A turbulent flow may further contribute to diagnose
a stenosis. An asymmetry analysis cannot be applied to the
P1-PCA segment because of the rather frequently seen
variation of a fetal-type PCA (see “Intracranial Collateral
Pathways,” p.101). Furthermore, indirect hemodynamic
criteria also apply to the PCA. Hemodynamically relevant
stenoses will cause a proximal prestenotic flow pattern
(except for a P1-PCA stenosis) and distal poststenotic flow
patterns. For further discussion on PCA stenosis, see Case 6
(p.156).
Intracranial Pathology 99
Fig. A5.47 TCCS, transtemporal approach, axial midbrain/thalamic
plane. A Normal color-mode and Doppler spectrum of the proximal
right P3-PCA which is accompanied by the basal vein of Rosenthal
signal (BVR) (flow velocity artery: 81/29 cm/s, vein: 20/10 cm/s).
B Contralateral right PCA Doppler spectrum with markedly reduced
flow velocity (22/13 cm/s) indicating a distal PCA occlusion. C Signal
of the right basal vein of Rosenthal located lateral to the PCA (flow
velocity: 20/10 cm/s)
PCA—Occlusion
Again, guidelines for MCA occlusion can also be applied in
PCA occlusion. Direct sign of a proximal PCA occlusion is an
absent color-mode signal. Doppler spectrum analysis may
show an absent flow signal. In more distal occlusion, e. g.,
within the P3-PCA segment a dampened flow signal (corresponding to TIBI grade 3) may proximally be observed
(Fig. A5.47). A P1-PCA occlusion may escape detection if a
large PCoA is present as this constellation then appears to
be a physiologic fetal-type PCA or if a well-developed SCA
is mistaken for the P1-PCA segment. Otherwise, raised
flow velocities within the A1-ACA or M1-MCA segments
indicating leptomeningeal flow to the PCA territory may
be present. Such a flow diversion may also occur in the case
of P2- and P3-PCA occlusion. Distal PCA branch occlusion
might not have any hemodynamic effect and is therefore
often overlooked.
BA—Stenosis
The combined transforaminal (proximal two-thirds of the
BA) andcoronal transtemporal insonationapproach (distal
one-third of the BA) allows assessment of the BA over its
full length, provided that the insonation conditions are
good (Fig. A5.48). Velocity cut-off values for >50 % and
< 50% stenosis are given in Ta b l e A 5 . 3 . Detectionof indirect
Fig. A5.48 A 3D TOF MRA, coronal MIP. BA stenosis within the distal
third of the BA (arrow). B TCCS, transforaminal approach. Distal BA
stenosis (flow velocity: 210/95 cm/s). C TCCS, transtempora l ap proach, coronal plane. Distal BA stenosis (angle-corrected flow velocity: 226/98 cm/s).
signs of high-grade stenosisdepends on the location of the
stenosis. Prestenotic flow alterations are absent in distal
stenosis but may be present in both VAs in proximal highgrade BA stenosis. A distal indirect sign is the activation of
one or both PCoAs.
5 Vascular Pathology100
Fig. A5.49 Synopsis of VA and BA flow patterns in intracranial pos-
terior circulation occlusion depending on the location of the occlusion. Both VAs are well developed. A P1-PCA occlusion—no flow
alteration. B Top of the basilar artery occlusion—no significant VA
flow alterations. No or only mild BA flow reduction. C Midbasilar
occlusion—distinct prestenotic flow alteration in both VAs and even
more in the BA, if detectable. D Unilateral V4-VA occlusion distal of
the PICA origin—only moderate ipsilateral prestenotic VA flow alter-
ation asthe blood flow into thePICA is preserved. Note that a normal
flow signal may also be present. Normal BA flow. E Unilateral V4-VA
occlusion proximal to the PICA origin—severe prestenotic VA profile
alteration without diastolic flow. Sightly increased contralateral VA
flow which may also be observed in D.
BA—Occlusion
Occlusions are difficult to assess and diagnostic certainty
depends on the site of the occlusion. In general, the diagnostic specificity is high but the sensitivity low. A proximal
BA occlusion will always result in prestenotic flow alterations of both extracranial VAs. Transtemporal insonation
of the distal segment may then show a retrograde BA flow
derived from one or both P1-PCA and PCoA segments.
OcclusionofthetopoftheBA,however,mayleaveboth
VA profiles and even the proximal BA signal almost unchanged (Fig. A5.49). This is explained by the numerous
arteries that originate from the proximal and midbasilar
artery (AICA, SCA, branch and perforator arteries) which
may result in a nearly unchanged peripheral flow resistance. Therefore, apparently normal VA and proximal BA
profiles are not sufficient to exclude top of the basilar
occlusion. Additional coronar transtemporal insonation
may help to overcome this problem if the distal BA can
be visualized. In case of a proximal occlusion, uni- or
bilateral PCoA collateral activation will be seen. Oscillation
of VAs and ICAs under simultaneous PCA flow analysis
might additionally help to identify the intracranial flow
pattern. Complete BA occlusion can be excluded if VA
oscillation at the atlas loop leads to a visible oscillation
effect within the PCA. However, as this cannot exclude the
presence of, for example, a fragmented thrombus, ultrasoundshouldalwaysbeusedtogetherwithotherdiagnostictoolssuchasCTA,MRA,orDSAinpresumedBA
pathology. For further details, see Case 21 (p. 261).
VA—Stenosis
The intracranial V4-VA segment—is generally easily accessibleviathetransforaminalapproach.Stenosescanbe
assessed by analyzing flow velocity, profile disturbances,
and pre- and poststenotic flow patterns. Velocity cut-off
values for >50 % and <50 % stenosis are given in Tab l e A5 . 3.
For further details about VA stenosis, see Cases 8 (p.165)
and 16 (p. 225).
VA—Occlusion
Flow signals in VA occlusion strongly depend on the site of
the occlusion, mainly on their relation to the origin of the
PICA (proximal or distal). Similar to the distal extracranial
VA occlusion a proximal intracranial occlusion below the
origin of the PICA results in a prestenotic extracranial VA
flow pattern mainly without an end-diastolic flow component. In this case a retrograde intracranial VA flow may be
found indicating a retrograde filling of the ipsilateral PICA.
An important differential diagnosis of this extracranial
finding is a hypoplastic VA which can usually be ruled
out by measuring the vessel diameter within the V2-VA
segment. Furthermore, even in a hypoplastic VA a residual
diastolic flow component should be present.
Occlusions distal to the PICA origin will result in mild to
moderate flow alterations of the extracranial VA, mainly
depending on its own diameter and the former relevance
in posterior circulation. It is important to note that an enddiastolic flow is always present which underlines the brain
supplying character of this flow signal. In case of a PICA
ending, the VA signal often shows a slightly increased
pulsatility which might resemble the flow signal that can
be found in an VA occlusion distal of the PICA origin. Such a
constellation may hinder a distinction between a distal VA
pathology and a physiological PICA ending of the VA (Fig.
53). A VA ending in the PICA however, usually reveals a
small vessel diameter reflecting its reduced flow territory.
A lumen diameter > 2.8 cm and a diameter-ratio (diameter
of contralateral VA divided by diameter of target VA) < 1.4
strongly argue in favor of VA occlusion distal of the PICA
and against a VA ending as the PICA (Saito et al. 2004) (for
further reading see also case 19).
Collateral Pathways
Recanalization along with the activation of collateral pathways has, along with recanalization, the greatest prognostic importance in acute ischemic stroke. The main underlying mechanism for the development of collateral function is the change in perfusion pressure, caused by blood
vessel obstruction. As the arterial vascular system is free of
valves, the blood stream may follow the direction of need,
only limited by the individual anatomic situation. The
more proximal an occlusion occurs, the easier it will be
for collaterals to compensate for it. Therefore, a major
intracranial occlusion will only rarely occur without clinical manifestation of stroke. Extracranial occlusions are
less likely to endanger the patient, at least from a hemodynamic point of view. In the following sections we explain potential intracranial collateral pathways and the
pattern of collateral flow in extra- and intracranial occlusive processes. Finally we discuss the clinical relevance of
collateral circulations.
Intracranial Collateral Pathways
Primary Collaterals (ACoA and PCoA)
The circle of Willis is the main intracranial distributor of
blood. Until the introduction of dynamic diagnostic tests in
vivo, the analysisof its importance and regulatory function
was rather limited and restricted to postmortem analysis
of anatomy and vessel diameter.
The unpaired ACoA and bilateral PCoAs are the most
important circle of Willis control variables, also called
first-order collaterals. If normally developed, together
they form a closed and therefore functional circle of Willis.
Ideally their diameter approximates the diameters of the
other basal cerebral arteries (see Chapter 2, Fig. A2.10,
p.17). Only then a proximal arterial occlusion can result
in collateral flow without blood flow impairment. Even in a
constellation of a three-vessel occlusion, for example, involvement of one VA and both ICAs (Wróblewski et al.
1997) and even of one VA and both CCAs (Karaköse et al.
2002),theremainingVAmaybeabletoprovidetheblood
supply for the whole brain via the circle of Willis, provided
that a normal heart function is present. The abovecases are
exceptionally rare, however, more frequently we observe,
for instance, bilateral ICA occlusions which are also often
well compensated (for further details, see Case 12, p.194).
InmostcaseswiththisconstellationoneorbothPCoAsare
activated to maintain a sufficient cerebral perfusion. A
collateral flow via the ACoA will then only occur if only
one PCoA provides the blood supply for both sides of the
anterior circulation. A predominantly PCoA derived blood
flow into the MCA and ACA mayalso occur in unilateral ICA
occlusion. More often, however, a so-called “cross-flow”
from the contralateral ICA via contralateral A1-ACA, AcoA,
and retrograde A1-ACA or combinations of both collateral
Collateral Pathways 101
Fig. A5.50 Right extracranial ICA occlusion. A DSA, selective left
ICA filling, posteroanterior view. Cross-flow from the left ICA via
A1-ACA, ACoA (arrow) and retrograderightA1-ACAintotheright
MCA. B DSA, selective left VA filling, posteroanterior view. Collateral
flow viathe PCoA (arrow) into the MCA territory.Note theretrograde
filling of the right VA, merely induced by the pressure injection of the
contrast agent during DSA.
twomechanismsisnotonlytheexistenceoffunctioning
collaterals but also of regularly developed P1-PCA and A1ACA segments. However, the latter show—in contrast to
the M1-MCA, A2-ACA and P2-PCA segments— considerable variations of vessel diameter.
Since the introduction of diagnostic catheter angiography in the 1950s, the circle of Willis and collateral pathways in extra- and intracranial occlusive processes as well
as the regulatory circle of Willis function can be evaluated
in vivo (Fig. A5.50). The advancement to DSA and the
selective vessel imaging further improved our understanding about the functional relevance of collaterals.
However, even in the advanced DSA techniques, a considerable amount of contrast has to be administered intraarterially under high pressure, which may alter the physiologic intracranial perfusion pressure balance. Also, with
the selective vessel imaging technique only parts of the
cerebral circulation can be displayed at a time, restricting
the evaluation and permitting only assumptions with regard to the real flow direction or the strength of the blood
flow.
The noninvasive techniques currently used to assess
these issues are MRI and ultrasound. In MRI, the phasecontrastMRAwasshowntobeabletodepictflowdirections, for example in the A1-ACA or the PCoA in cases with
an ipsilateral ICA occlusion (Kluytmans et al. 1999). The
technique, however, does not provide information regarding the quantity or quality of collateral flow and is not, for
methodologic reasons also, part of current diagnostic routines. The second frequently used TOF MRA sequence does
not display flow direction. TOF MRA also has its methodologic limitations, for instance in case of a turbulent flow
within the communicating arteries which are then often
5 Vascular Pathology102
Fig. A5.51 Bilateral TCD Doppler monitoring of the MCA during a
CCA compression test. Flow velocity of the right (green) and left
(red) MCA are given as maximal time-averaged velocity values (TAV).
Note the sharp drop in MCA flow at beginning of the compression.
Over a time period of 2 minutes of compression, blood flow of the
left MCA recovers gradually which can be explained by a gradually
improving collateral recruitment. Notethe physiological “overshoot”
in left MCA flow on release of the compression.
not depicted. In a comparative study of DSA and TOF MRA
in a mixed group of patients with and without arterial
occlusions, the PCoA was visualized with the MRI technique in 81% of cases only (Patrux et al. 1994).
Incontrast,ultrasoundpermits,comparabletotheDSA
technique, a direct and real-time evaluation of the intracranial hemodynamic effects of an extracranial arterial
occlusion. Provided that good insonation conditions are
present, flow profiles and flow velocities within the ACoA
and PCoA in combination with the analysis of distal vessel
segments allow assessment of the hemodynamic relevance of the communicating arteries. In healthy individuals they are often difficult to assess. The ACoA is too short
to be directly depicted by current ultrasound systems
under physiologicconditions. The PCoA is often very small
and its diameter in 53 % of cases reported to be less than
1 mm (Lang 2001). This, together with a frequently tortuous and basal course as well as the poor insonation angle
hinders insonation under physiologic conditions. To assess
patency and function of both vessels in absence of an
occlusive process, a CCA compression test may be performed. Artificial CCA occlusion over three to five heart
cycles will, in the case of a functional AcoA, result in
retrograde ipsilateral A1-ACA flow. A functional PCoA
under compression will result in an ipsilateral flow rise
oftheP1-PCA.Iftheabovecriteriaareappliedtoanelderly
population, a closed and therefore functional circle of Willis can be detected in up to 29 % of cases (Hoksbergen et al.
2000b). A hypofunctional ACoA was found in 4 %, a hypofunctional PCoA in 61 % of studied vessels, the latter in 45 %
unilateral and 16 % bilaterally (see Chapter 2, Fig.A2.9,
p.16). A later study comparing stroke patients with controls, however, demonstrated higher incidences of ACoA
(33 % vs. 6 %) and PCoA functional impairment (57 % vs.
43 %) (Hoksbergen et al. 2003a). This indicates that a patent circle of Willis is not only of hemodynamic importance
in extracranial vessel occlusions but might also be relevant
for the recanalization of embolic occlusions. Although an
elegant functional paradigm, the above compression test is
also not free from interpretation problems. The definition
of a functioning PCoA particularly has to be questioned
because of the arbitrary chosen cut-off of a > 20% P1-PCA
flow rise. In addition, it has to be kept in mind that the
ultrasound detection of the P1-PCA may be difficult, particularly if TCD is applied. The P1-PCA is a short vessel
segment (mean 6 mm, range 3–9mm) and might easily
be confused with the nearby SCA or the P2-PCA segment.
Furthermore, a relatively short compression does not automatically allow drawing conclusions regarding function
after prolonged occlusion. It seems obvious that first-order
collaterals will immediately respond to the altered pressure gradient, however, a collateral pathway via the communicatingarteries mayalso startafter more than three to
five heart cycles, minutes, or possibly even after a longer
period (Fig.A5.51) (Widder et al. 1994). Considering this,
the prevalence of functional communication arteries
mightbeexpectedtobeevenhigherthanreportedabove.
Although functional characteristics of the communicating arteries are easy to assess by ultrasound, no morphologic information can be obtained. The same research
group of Hoksbergen and coworkers therefore compared
functional TCCS and post-mortem anatomic vessel findings. They found a threshold diameter for first-order collaterals of 0.4–0.6 mm, i. e., considerably lower than the
previously assumed 1 mm, which mainly derives from
anatomical observations. The lower cut-off of 0.4 mm is
probably more valid for the ACoA, and the higher one of
0.6 mm for the PCoA as its length and the resulting increased resistance have to be taken into consideration
(Hoksbergen et al. 2000a).
Vessels of this size cannot usually be visualized by anyof
the current angiologic methods, particularly under physiologic circumstances in which the net flow in these vessels is rather low or even undulating. As soon as they serve
as collaterals a mismatch between vessel diameter and
required blood volume flow develops which leads to a
subsequent rise in flow velocity (so-called “functional
stenosis”),whichthenisrathereasytodetectbyultrasound techniques.
Fetal-type Posterior Cerebral Artery
As already stated above, the communicating arteries can
only effectively activate if the downstream A1-ACA or upstream P1-PCA are equally patent. A functionally relevant
A1-ACA hypoplasiaoccurs in only approximately 1 % and is
therefore rare. However variants of the P1-PCA are common, especially comprising the fetal-type (FT)-PCA in
which the PCA directly originates from the ICA without
apparent connection to the BA (full type). However, a small
vessel bridge, i. e., a hypoplastic P1-PCA, can generally be
found in anatomic studies (partial type) (Saeki et al. 1977).
The discrimination from a FT-PCA with a strong PCoA is
inconsistent. From a morphologic point of view the best
way is to define a FT-PCA if the PCoA diameter exceeds the
P1-PCA diameter which has been reported in about 20 % of
hemispheres (Saeki et al 1977; Lang 2001). Of the radiologic techniques, DSA is the best method to demonstrate
potential connections between the anterior and posterior
circulation. In a panangiographic study by Jongen and
coworkers an exclusive PCA contrast filling from the ICA
was observed in 11 % of hemispheres. In another 46 % of
hemispheres a combined supply via ICA and BA was found
(Jongen et al. 2002). An almost identical prevalence of 10%
of full fetal-type PCA was reported in a DSA-correlated CTA
study (van der Lugt et al. 2004). MRAdefined full fetal-type
PCA ranges from 3 % to 30 % and for partial fetal-type-PCA
from 13 % to 26 % indicating differences in definitions and
study populations and methodologic limitations (van
Raamt et al. 2006). In a population of healthy adults a
prevalence of 17 % per hemisphere was reported in a TOF
MRA study (Jongen et al. 2004).
Fetal-type-PCA is also difficult to define with ultrasound
methods. TCCS might, for example, fail to detect a small
hypoplastic P1-PCA segment because of its low net flow.
Also a differentiation from the nearby located SCA might
be problematic. Applying the CCA compression test, defining FT-PCA as a flow reduction or cessation in the PCA a
prevalence of 13 % of hemispheres and 6.5 % of subjects has
been reported, as all studied subjects were unilaterally
affected (Hoksbergen et al. 2000b). Alternatively, an ultrasound-derived differentiation between normal and fetaltype PCA can also be achieved by a simple oscillation test
(for further details, see PCoA anatomy in Chapter 2, “Intracranial Arteries,” p. 101). Applying the latter technique, a
similar prevalence of 17 % FT-PCA has been reported (Siemieniec 2006). From a clinical point of view it has to be
noted that a differentiation between a strong PCoA and a
FT-PCA is usually not of relevance.
Secondary Collaterals (Ophthalmic Artery
and Leptomeningeal Collaterals)
Second order collaterals are the OA and the leptomeningeal vessels. They are considered to be reserve systems
that are only activated if the anterior and PCoAs are not or
insufficiently developed to compensate a relevant proximal vessel occlusion.The OAconnects the extra- and intracranial anterior circulation. Under physiologic conditions,
in the normal type its blood supply mainly derives from
the ICA, in 2.4 % of cases however, a partial blood supply
occursfromthemiddlemeningealartery,in1.2%even
exclusively from the middle meningeal artery—aperipheral ECA branch (Hayreh and Dass 1962). In both circumstances the blood flow is centrifugal. In the case of an OA
collateral activation, which is only possible in a OA with
ICA origin, the flow direction reverses and the OAbecomes
Collateral Pathways 103
Fig. A5.52 DSA. A Selective CCA injection, lateral view. ICA occlu-
sion (arrow). Collateral filling of the carotid siphon (arrowhead) via
the retrograde OA and middle meningeal artery (arrows) from the
ECA. B Selective right VA injection, posteroanterior view. Left ICA
occlusion. Collateral filling of the MCA territory via PCA leptomeningeal collaterals (arrows). Note the prominent cortical PCA branch
also distributing blood into the MCA territory.
a brain-supplying artery. Typically the blood flow then
comes from the superficial temporal artery or facial artery
via the supratrochlear artery to the OA. However, vessel
filling may also occur via the maxillary artery and ethmoidal arteries.
The presence of an activated OA collateral is often easily
depicted by DSA during selective ECA main stem or branch
contrast injection (Fig. A5.52A). However, if the contrast is
injected proximally, i. e., at the aortic arch or the CCA, an
OA collateral may be missed because of contrast dilution.
CTA and MRA usually fail to detect the OA while TCCS and
TCD are optimally suited as they allow direct insonation of
thevesselviathetransorbitalaswellasthetranstemporal
approach. The assessment of flow profile and flow direction in particular allows evaluation of its relevance as a
collateral vessel (for further details see OA anatomy in
Chapter 2, “Intracranial Arteries”, p. 24).
Other important potential collaterals are the leptomeningealorpialarteries,thefinalsegmentsoftheMCA,
ACA, and PCA (see Chapter 2, Fig. A2.8). In case of need
they are able to build anastomosis between all three vascular territories of the cerebrum and form the LMCs. The
involved regulatory mechanisms and temporal patterns of
development are currently not well understood (Liebeskind 2003). Anatomically, they may reach a diameter of up
to 1 mm, the size of the normal pial arteries over the
cerebral hemispheres (Brozici et al. 2003). Their distribution, number, and size is variable. They are best developed
between the MCA and ACA territory, less developed between the MCA and PCA, and only weakly developed
between the ACA and PCA. Their activation represents a
shifting of the vascular territories account of the MCA,
ACA, or PCA territory. It is important to note that the
LMCs are secondary collaterals. For example, in extracranial ICA occlusion—the prototype of extracranial occlu-
5 Vascular Pathology104
Fig. A5.53 A Schematic drawing of the normal distribution of vas-
cular territories, coronal plane. B Schematic drawing of shifted vascular territories caused by MCA occlusion toward the ACA and PCA.
C DSA, selective left ICA filling, posteroanterior view: M1-MCA occlusion (arrow). Note thenormal borders of the ACA territory on the
right side (thin dashed line) and the shifting of the left ACA territory
(thick dashed line) corresponding to the theoretical considerations
shown under B.
sion—first-line collaterals are the anterior and posterior
communicating arteries. Only if these fail are the LMCs
from the PCA and OA activated, i. e., they are a sign of
insufficient primary collateral capacity (Hofmeijer et al.
2002). In intracranial MCA occlusion—the prototype of
intracranial occlusions—the primary collaterals as well as
the OA cannot, for anatomic reasons, be activated. Under
these circumstances the ACA and PCA LMCs are the only
vessels that may compensate for the occlusion. In the best
case, they are able to maintain the perfusion of the whole
MCA territory as has been shown in an autopsy case report
with MCA main stem occlusion (Nishida et al. 2000). This,
however, requires rapid LMC activation, which finally determines the extent of the hypoperfusion and subsequently the area of infarction (Fig. A5.53). Within the posterior circulation LMC may also be activated between the
three cerebellar arteries, however, their mechanisms of
activation are even less understood.
Imaging of LMCs is easily achieved by DSA and notably
within the early arterial, late arterial, and capillary phases
of the contrast passage. The early arterial phase directly
visualizes the feeding vessels, which may be particularly
prominent in the PCA as strong cortical branches
(Fig. A5.52B). The late arterial and capillary phases usually
allow a clear mapping of the territories supplied by the
LMCs. In addition, the late arterial phase demonstrates the
extent of the centripetal collateral filling. Under optimal
circumstances even a proximal main stem vessel, for example the distal M1-MCA, might be filled retrogradely via
the LMC (Fig. A5.54). The magnitude of centripetal filling
may be graded between 1 and 5. A scoreof 5 meanslittle or
no significant reconstitution of the occluded vessel territory; score 1 indicates the distal portion of the occluded
vessel is refilled (Christoforidis et al. 2005).
Fig. A5.54 DSA and schematic drawing of collaterals in MCA occlusion. A, B DSA, selective ICA filling, posteroanterior view: A Early
arterial phase: M1-MCA occlusion (arrow). B Late arterial/capillar y
phase: Note the retrograde filling of insular MCA branches (arrows)
via ACA leptomeningeal collaterals (curved arrow). C Schematic
drawing summarizing findings of the case in A and B.
In MRAanalysis, LMCare only indirectly indicated.Using
theflow-sensitiveTOFMRA,thesignalintensityofthe
vessels involved in leptomeningeal collateralization appear slightly stronger (Uemura et al. 2004). However, the
functionality of LMCs can be evaluated well by assessment
of the MRI perfusion sequences. For example, in MCA
occlusion, the size of the perfusion deficit indirectly correlates with the quality of LMC from the ACA and PCA. In case
of well-functioning collaterals, MTT values are low and the
cerebral blood volume is only slightly raised (Kluytmans et
al. 1999). Comparable information can be gathered from
the perfusion CT technique.
Ultrasound is only indirectly ableto assess LMC function.
In case of LMC activation, flow velocities within the supplying main stem arteries will be raised. In case of an MCA
occlusion, these are the ipsilateral A1-ACA, P2- and P3-PCA
segments,incaseofanA1-ACAocclusiontheipsilateral
M1-MCA, P2- and P3-PCA segments as well as the contralateral A1-ACA segment, respectively (Fig.A5.55). The
latter may be possible if an anastomosis between both A2ACA segments crossing the interhemispheric fissure is
present. Finally, in PCA occlusion, flow velocities within
the ipsilateral M1-MCA as well as the ipsilateral A1-ACA
may be increased.
In general, cortical branches may be analyzed by ultrasound techniques, however, their analysis is not yet part of
routine TCCS. From our own experience, however, some
branches, for instance the temporal PCA branches (anterior temporal artery and occipitotemporal artery) may be
particularly strong and easily depicted in MCA occlusion
(for further details about anatomy and imaging techniques
of PCA branches, see Chapter 2, “Intracranial Arteries,”
p.101).