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Collateral Pathways 105
Fig. A5.55 DSA, composed image, left and right selective ICA in-
jection late arterial phase, posteroanterior view. A Bilateral A1-ACA
occlusion (arrows). Note the filling of the ACA territory via LMC from
the MCA territory (arrowheads). B Bilateral A2-ACA occlusion (arrow). As in the case in A, there is filling of the ACA territory via LMC
from the MCA territory (arrowheads).
Intracranial Collateral Pathways in ICA Occlusive Processes
In extracranial ICA occlusion, involvement of the ACoA via
retrograde A1-ACA (cross flow) is seen in up to 80 % of
cases (Fig. A5.56A). Activation of the PCoA can be seen in
70 % of cases (Demchuk et al. 2000) (Fig. A5.56B). If the
diameter of both communicating arteries is too small for
the required blood flow, they will demonstrate raised flow
velocities and turbulences (functional stenosis) themselves and poststenotic flow patterns or low resistance
flow signals in the downstream intracranial vessel segments. This flow pattern is characterized by a reduced
flow velocity, a delayed systolic flow rise, and a raised
diastolic flow component, the latter attributable to a compensatory dilatation of the resistance vessels. In a TCD
study of 114 patients with a > 80 % ICA stenosis, 54 % of
patients demonstrated the above flow pattern. Interestingly, in symptomatic patients the pattern was seen significantly more often than in asymptomatic patients (80 %
vs. 37%, respectively) (Hartmann et al. 2000). Another TCD
study in 17 patients with proximal ICA occlusions found
poststenotic flow patterns in 67 % of cases (Demchuk et al.
2000). This, on the contrary, means that a third of patients
did not show any flow profile alterations within the downstream vessels indicating very good functioning of primary
collateral pathways.
Whenever a cross-flow via the ACoA is present, the A1ACA of the nonaffected side shows raised flow velocities as
it has to provide the blood supply for both ACA and in
general also for the contralateral MCA territory. If its flow
velocity is clearly higher than that of the ipsilateral MCA
and AcoA, cross-flow can be assumed even if a direct
visualization of the retrograde A1-ACA on the side of the
occlusion is difficult. The M1-MCA of the affected side
Fig. A5.56 Schematic drawing of the two main types of collateral
flow in proximal ICA occlusion. A Cross-flow from the contralateral
side via contralateral A1-ACA, ACoA, retrograde ipsilateral A1-ACA
into theipsilateral MCA territory.B Collateral flowfrom theipsilateral
P1-PCA via thePCoA into the ipsilateral MCA territory. Combinations
of both patterns are possible.
Fig. A5.57 Left proximal ICA occlusion. A DSA, selective right ICA
filling, posteroanterior view. Cross-flow via right A1-ACA, ACoA
(arrow), left A1-ACA into the left MCA territory. B TCC S, tr anstem poral approach, axial midbrain plane (left-sided insonation). Colormode image demonstrates the red-coded retrograde A1-ACA flow
(arrow). Right: Corresponding Doppler spectra of the right, contralateral A1-ACA (strong orthograde flow), the ACoA (raised flow
velocity and turbulence), the ipsilateral A1-ACA (retrograde flow)
and the ipsilateral M1-MCA (mildly reduced flow velocity). Note the
positive oscillation effect within the left MCA Doppler spectrum on
oscillation of the right extracranial ICA (arrows)
often demonstrates a reduced flow velocity (Fig. A5.57).
Baumgartner and coworkers reported in a DSA correlated
study in 78 patients with > 70 % stenosis- or occlusioninduced ACoA cross-flow, a peak systolic flow velocity of
141 ± 36cm/s within the A1-ACA contralateral to the occlusive process, and an M1-MCA velocity of 103 ± 27 cm/s
onthesameside.Incomparison,MCAflowvelocitieson
theocclusivesidewerelower(79± 24cm/s) (Baumgartner
et al. 1996). The ACoA in these circumstances becomes
5 Vascular Pathology106
Fig. A5.58 Different quality of collateral blood flow via the ACoA in
extracranial left ICA occlusion. Top: DSA, right ICA injection, posteroanterior view. Bottom: Corresponding Doppler flow profile of
the MCA ipsilateral to the occlusion. A Optimal collateral flow with
nearly simultaneous contrast filling of both MCA territories and
almost normal MCA flow profile. B Impaired collateral flow with
delayed MCA contrast filling on the side of the occlusion and poststenotic flow pattern in the MCA.
Fig. A5.59 Left proximal ICA occlusion. A DSA, selective left VA
filling, posteroanterior view: Collateral flow via left PCoA (arrow)
into the left MCA territory (arrows). B TCCS, transtemp oral ap proach, axial midbrain plane: Color-mode image demonstrates the
PCoA (arrow). Right: Corresponding Doppler spectra of the left P1PCA (raised flow velocity and turbulence), the PCoA (bidirectional
raised flow velocity and turbulence), the M1-MCA (orthograde flow
with reduced velocity and pulsatility), and the P2-PCA (normal
orthograde flow).
apparent in the form of a functional stenosis. If flow in the
retrograde A1-ACA is also turbulent, transmission of the
turbulence in the ACoA or a functional stenosis within a
hypoplastic A1-ACA itself may be the underlying cause.
The diameter of the ACoA and A1-ACA determine the MCA
flow profile on the side of the occlusion which may appear
almost normal, poststenotic, or in the worst case similar to
a venous signal (venouslike flow). The DSA correlate of this
impairment is a delayed contrast filling on the side of the
occlusion (Fig. A5.58). A DSA correlated study in 117 patients revealed a high diagnostic accuracy of cross-flow
detection by TCCS, provided that good insonation conditions were present. If the ACoA cross-flow is defined as a
retrograde A1-ACA flow on the side of the occlusion, or as a
M1-MCA flow reduction on the side of the occlusion on
contralateral CCA compression, the sensitivity, specificity,
and positive and negative predictivevalues are 98 %,100 %,
100 %, and 98 %, respectively (Baumgartner et al. 1997a). If
only a small MCA segment can be isonated on the side of
the occlusion because of an inadequate bone window,
extracranial oscillation may help to identify the collateral
flow pattern. If oscillation of the contralateral extracranial
submandibular ICA leads to a distinct oscillation effect
within the ipsilateral MCA, a cross-flow is very likely.
If a collateral flow occurs via the ipsilateral PcoA, the P1PCAdemonstratesraisedflowvelocitiesasitthenalsohas
to provide the blood supply to parts or the total ipsilateral
anterior circulation. The post-communicating PCA segments may, however, be completely normal (Figs A5.59,
A5.60). In the study by Baumgartner and coworkers
(1996), the peak systolic P1-PCA flow velocities on the
side of the occlusive process were 107 ±31 cm/s and
69 ±13 cm/s on the contralateral side. Often the PCoA is
theneasytovisualizeincolormodebecauseoftheraised
flow velocities. Functional stenoses and musical murmurs
are a frequent finding. In ICA occlusion, flow toward the
anterior circulation is expected. However, as the PCoA
oftenrunsanelongatedcourse,thisisnotalwaysevident
and a turbulent bidirectional signal can frequently be
found (Fig. A5.59). As in ACoA collateral function, the
downstream flow profiles—normal or poststenotic—depend on the caliber of the PCoA. If manual oscillation of
the extracranial VA in V3 leads to a marked effect within
the MCA on the side of the occlusion, relevant PCoA collateral function can be assumed even if the PCoA itself is
not directly accessible. The A1-ACA on the side of the
occlusion is then usually orthograde and demonstrates
identical, more or less poststenotic flow alterations, comparable with the MCA flow pattern. If the A1-ACA on the
occlusion side is not accessible despite excellent insonation conditions, both ACA territories are probably supplied
by the contralateral A1-ACA which then often shows
raised flow velocities.
Baumgartner and coworkers (1997a) also performed
comparative ultrasound and DSA analyses of the PCoA.
An active PCoA collateral was defined in case of a PCoA
presence or raised flow velocities within the P1-PCA
(> 2SD above the normal systolic blood flow velocity).
For TCCS they found sensitivity, specificity, and positive
and negative predictive values of 84 %, 94 %, 94 %, and 84 %,
respectively, which are lower than for the ACoA collateral.
However, it has to be kept in mind that every PCoA visible
on DSA is not necessarily a true collateral.
In clinical practice, a coexistence of anterior and PCoA
collaterals can sometimes be observed with the ACoA
Collateral Pathways 107
Fig. A5.60 Right proximal ICA occlusion. Left: DSA, selective left VA
filling, lateral view: Collateral flow via right PCoA (arrow) into the
right MCA territory (arrows). Right: Corresponding Doppler spectra
of the right P1-PCA (raised flow velocity and turbulence), the right
M1-MCA (poststenotic flow pattern), and the right A1-ACA (poststenotic flow pattern but orthograde flow). Note, as the ACA flow is
orthograde, the ACoA and/or left A1-ACA must be hypofunctional.
mainly providing the blood supply to the ACA territory and
the PCoA distributing blood into the MCA territory
(Fig. A5.61). In this constellation, a functional stenosis
might be detected in both communicating arteries.
Secondary collaterals, i. e., the OA and LMC, will be activated in case of insufficient primary collateral function. In
the worst instance, they may be the sole collateral pathways in extracranial vessel occlusion which usually implies an increased risk of developing hemodynamically
related cerebral ischemic infarction (for further details,
see Case 11, p. 183).The orbital collateral flow is confirmed
by retrograde flow in the OA. In ICA occlusion this can be
observed in the majority of patients. Reported incidences
byTCDvarybetween71%and77%(Demchuketal.2000,
Kluytmans et al. 1999) (Fig. A5.62). If the perfusion pressure is similar within the intra- and extracranial compartments, a watershed phenomenon—zero OA flow—may be
observed, which means that no OA flow is detected by
ultrasound. Comparison with the contralateral side will
help to differentiate between methodologic problems in
displaying the OA or a real zero-flow constellation. In a
study of patients who had a transient ischemic attack (TIA)
orminorstroke,incaseofazeroOAflow,anICAstenosisof
at least > 80 % or an ICA occlusion was found in each instance (Nuzzaci et al. 1999). Also, no case with a hemodynamically relevant ICA stenosis or occlusion demonstrated
anormalorthogradeOAflow.Asmallorthogradeflow
signal, however, was shown to be nonspecific. They were
observedinICAstenosis<60%butalsoinICAocclusion
(Nuzzaci et al. 1999). Although direct assessment of the OA
will probably suffice in most cases, an additional oscillation test may be performed. An orbital collateral can be
assumed if a slight manual oscillation of the ocular bulb
results in a visible oscillation effect within the ipsilateral
Fig. A5.61 Patient with combined ACoA and PCoA collateral in right
proximal 90 % ICA stenosis. A 3D TOF MRA, axial MIP. Note the
strong right PCoA (arrow) and the weak intracranial IC A signal
(arrowhead). B Corresponding TCCS color-mode image, transtemporal approach, axial midbrain plane (right-sided insonation). Note
the strong color-signal of the right PCoA and the retrograde right
A1-ACA flow.
Fig. A5.62 OA collateral in extracranial ICA occlusion. Left: DSA,
selective ECA filling, enlarged lateral view. Retrograde OA filling
(small arrows) and blood flow into the carotid siphon (large arrow)
and distal MCA territory. Right: Transorbital duplex ultrasound, axial
plane. Color-mode imaging reveals the blue-coded retrograde OA.
Note the brain supplying-like flow OA profile in the Doppler spectrum analysis.
MCA (Schreiber et al. 2006). Instead of the OA, its periorbital peripheral branches, e.g. the supratrochlear artery,
may be studied using a continuous-wave Doppler probe.
This approach, derived from the early days of clinical ultrasound, is also reliable in collateral assessment of the OA.
However, direct collateral assessment should be carried
out whenever possible.
LMCs can be indirectly assessed by analyzing blood flow
velocities in the feeding basal cerebral artery.For example,
if the P1- and the P2-PCA segments demonstrate equally
raised flow velocities, an LMC activation seems likely while
a velocity rise solely within the P1-PCA segment indicates
5 Vascular Pathology108
Fig. A5.63 PCA leptomeningeal collateral flow via PCA branches in
extracranial ICA occlusion. A DSA, selective left VA filling, postero-
anterior view. Collateral filling of the MCA territory via a prominent
anterior temporal artery (arrow). B Corresponding TCCS color-mode
image demonstrating a strong signal of the same PCA branch (arrow).
Tab l e A5 . 5 Synopsis of intracranial collateral pathways in extracranial ICA occlusion or > 80 % stenosis
Via ACoA Via PCoA
Ipsilateral M1 (ø)IpsilateralM1(ø)
Retrograde A1 Ipsilateral P1 ∕
Functional stenosis ACoA Ipsilateral P2 normal
Contralateral A1 ∕ Functional stenosis PCoA
Contralateral A1 > M1 Ipsilateral A1 orthograde with
flow pattern identical to ipsilateral M1
Via LMC Via OA
Ipsilateral P2 = P1 ∕ Retrograde or zero OA flow
∕ flow velocity increased
ø flow velocity decreased
a PCoA collateral function. To increase diagnostic certainty,
the right and left sides should always be compared, as flow
velocities in homologous P2-PCA segments are usually
similar. A study correlating TCCS and DSA findings regarding a PCA LMC in occlusive lesions of the carotid system a
peak-systolic flow velocity greater than 100 cm/s within
the post-communicating P2-PCA segment yielded a diagnostic sensitivity of 77 % and specificity of 83 % (Kimura et
al. 2000). If good insonation conditions are present, even
the cortical PCA branches may be detected and their flow
velocity and therefore their possible involvement in PCA
LMC can be assessed (Fig. A5.63).
Tab l e A5.5 summarizes the possible intracranial collateral patterns in extracranial ICA stenoocclusive disorder of
at least 80 % stenosis and their main ultrasound criteria
(Tab l e A5.5).
Fig. A5.64 DSA, selective ICA injection, lateral view in a patient with
bilateral extracranial VA occlusion. A Retrograde BA filling (arrows).
B Late arterial phase—retrograde BA filling extends down to one VA
(arrows) and from there into the PICA (arrow). Note, that the precondition of this flowpattern is an intact PCoA. However, the PCoA is
not clearly visible, although it is present and functional.
Intracranial Collateral Pathways in VA Occlusive Processes
In contrast with unilateral occlusive processes of the ICA, a
unilateral extracranial VA stenosis or occlusion only rarely
leads to a compromised intracranial hemodynamic constellation. This is mainly caused by the anatomic constellation of both VAs merging into the BA. In proximal VA
occlusion the PICA, originating from the distal intracranial
VA, is often supplied by the contralateral VA in a vertebrovertebral overflow pattern (for further details, see “Intracranial Posterior Circulation,” p. 99). Intracranial collateralization is only required if both VAs are functionally impaired by a bilateral occlusive process, in cases with unilateral VA occlusion and contralateral hypoplasia (incidence of unilateral hypoplasia in approximately 10%) or
in unilateral occlusion and contralateral VA terminating as
the PICA. In the worst case scenario, the total posterior
circulation, the cerebellum and brain stem are supplied via
the anterior circulation by one or both PCoAs, which requires retrograde BA and VA flow (Fig. A5.64). The main
limiting factor for this collateral pattern may be bilaterally
nonfunctionalPCoAs,which,however,arefoundonlyin
up to 16% of cases (Hoksbergen et al. 2000b).
Extracranial Collateral Pathways
Extracranial collateral pathways may also be activated to
assure sufficient intracranial perfusion. This may occur
especiallywithintheVA,whichincontrastwiththeICA
often anastomoses with primarily nonbrain-supplying arteries, even under physiologic circumstances. In hemodynamically relevant occlusive VA processes a number of
collateral patterns can be observed that result in a secondary, postocclusive VA filling (for further details, see “Ex-
Collateral Pathways 109
tracranial Posterior Circulation,” p. 91). Frequently, distal
fillingatthedistalV2-VAortheleveloftheatlasloopvia
the thyrocervical trunk anastomoses and ECA branches,
especially the occipital artery, can be observed. The latter
anastomosis is also reversely able to function in CCA occlusion and to fill the ICA via the retrograde ECA. Other,less
common, collateral patterns are a VA filling via the ladderlike spinal arteries from the contralateral VA (for further
details, see “Extracranial Posterior Circulation,” p. 91). Numerically irrelevant are the very rare collaterals from ICA
to the BA via persisting primitive embryonal vessels.
Clinical Relevance of Collateral Pathways
Although current scientific interest is mainly focused on all
aspects of revascularization, there is growing awareness of
the importance of collateral pathways, particularly as sufficient collaterals may prevent the occurrence of stroke or
at least alleviate the severity of damage. Within the acute
stroke setting the maintenance of collateral pathways is at
least as important as the therapeutic recanalization.
Within the chronic phase, the quality of the collaterals
substantially determines the future prognosis.
Data on collateral dependent clinical prognosis in patients with symptomatic extracranial ICA stenosis have
been reported from the NASCET trial. DSA images were
analyzed in 339 medically and 342 surgically treated patients for the presence of an ACoA, PCoA, and OA collateral
but not including the LMCs due to methodical reasons
(Hendersonetal.2000).Asingularcollateralflowviathe
ACoA was found in 70% of cases, an exclusively PCoA
collateral in 9 %, an exclusively OA collateral in 2 %, and a
mixed pattern in 20 %. The existence of collaterals correlated as expected with the degree of stenosis. Collateral
blood flow was found in 63.6 % of near occlusions (defined
as severe distal lumen reduction), in 42.7 % of 85–99 %
stenosis (ECST criteria > 90 %), in 25.3 % of 70–84 % stenosis
(ECST criteria 85–95 %), in 3.1 % of 50–69 % stenosis (ECST
criteria 70–82 %), and in 0.5% of stenoses < 50 % (ECST
criteria < 70 %). In the medically treated patients the stroke
risk significantly increased with the increasing degree of
stenosis except for the near occlusions. If collaterals were
present, patients with stenoses between 70–84 % and
85–99 % had a two-thirds reduced risk of stroke. If the
70–99 % stenoses were combined, the 2-year risk of hemispheric stroke with sufficient collaterals compared with
insufficient collaterals was significantly reduced (11.3% vs.
27.8 %, respectively). The likelihood of a TIA (19.1% vs.
36.1%) or a disabling stroke or fatal stroke was also significantly reduced (6.3 % vs. 13.3 %). In the operated patients, the presence of collaterals resulted in a reduced
perioperative risk (1.1 % vs. 4.9 %) and a lower 2-year risk
of hemispheric stroke (5.9% vs. 8.4 %), but both differences
did not reach statistical significance (Henderson et al.
2000).
With regard to the development of border zone infarction, collateral flow via the PCoA seems to have a protec-
tive effect. In a patient group with extracranial ICA occlusion, the incidence of a PCoA collateral was 50 % in those
without a border zone infarction compared with 12 % in
those with border zone infarction. Patients without BZI
also revealed significantly larger PCoA diameters (1.6 mm
vs. 1.3mm). On the other side, a cross-flow via the ACoA
was notprotective as a comparable prevalencewas seen in
both groups (60 % vs. 69 %) (Hendrikse et al. 2001).
The quality of the collaterals may also be evaluated
indirectly by measuring the cerebrovascular reactivity
(CVR). In a TCD study of 85 patients with asymptomatic
ICA occlusion followed over 38 ± 15 months, only 8 % of
patients with normal CVR developed a TIA. No strokes
occured. In contrast, 32 % of patients with diminished or
exhaustedCVRhadaTIAorcompletedstroke(Kleiserand
Widder 1992). The occurrence of secondary collaterals is
also suggestive of an insufficient collateral blood supply. A
TCD study of 25 patients with extracranial ICA occlusion
demonstrated significantly lower systolic MCA flow velocities on the side of the occlusion (55 ± 22 cm/s vs.
79 ±24 cm/s). Furthermore, a retrograde OA flow was associated with a low MCA flow velocity and with the absence of primary collaterals (Schneider et al. 1991). This
was further confirmed by a combined TCD and DSA study
in 70 patients with ICA occlusion and minor stroke. In
these, a retrograde OA flow or activation of LMC was
associated with a significant impairment of carbon dioxide
CVR (8 ± 14 % vs. 33 ±18 %) compared with patients with
exclusively primary collaterals such as the ACoA and PCoA
(Hofmeijer et al. 2002).
In intracranial occlusions, the LMCs are the only alternative collateral blood supply. In these circumstances their
activation does not reflect insufficient collateralization but
is the only opportunity to reduce the extent of impaired
perfusion. In a study of 97 intraarterial and 14 systemically
thrombolyzed patients with intracranial occlusions of the
anterior circulation, multivariate analysis revealed that
the most important factor for the clinical outcome was
the existence of well-developed LMCs (odds ratio 5.9,
confidence interval [CI]: 1.3 to 26.7), defined as retrograde
filling of at least three MCA branches up to the M2 segments and not a successful recanalization (odds ratio 1.9,
–6.6) (Kucinski et al. 2003). In a comparable study of
CI: 0.5
53 stroke patients the LMC quality also significantly correlated with infarct volume and clinical outcome, independent of the extent of the recanalization (Christoforidis et al.
2005).
The function of LMC in MCA occlusion can be assessed by
ultrasound techniques by detection of raised flow velocities within the ACA and PCA, also called flow diversion. In
a group of 47 patients with persisting M1-MCA occlusion
despite rt-PA thrombolysis only those patients with a TCD
assessed flow diversion demonstrated clinical improvement. After 90 minutes/24 hours of receiving the rt-PA
bolus, 22 %/29% with and 0.52 %/–25 % without flow diversion had clinically improved (Kim et al. 2005). These data
indicate that the quality of LMCs may determine the time
5 Vascular Pathology110
window of applicable thrombolysis. There seems also to be
interindividual variability in the development of these
collaterals. Moreover, their function seems to be age-dependent, the younger the patient the better the collateral
function, which has been explained by an age-dependent
increasing vessel wall rigidity (Brozici et al. 2003).
Very few data are available for the collateral flow patterns of the posterior intracranial circulation. In an angiographic study of 51 patients with BA occlusion, factors
influencing outcome were, besides vessel recanalization,
other parameters such as the initial clinical condition, the
length of the BA occlusion, and the collateral supply
(Brandt et al. 1996). Also, retrograde collateral flow within
the distal BA seems to be associated with better clinical
outcomes (Ribo et al. 2004).
The impairment of autoregulation within the ischemic
area is probably of greatest therapeutic importance as it
canbeassumedthatperfusionthendirectlydependson
blood pressure. A therapeutic increase of blood pressure
might therefore improve the brain perfusion and reduce
the extent of the ischemic area. First, clinical observations
seem to support this assumption. Reduction of blood pressure within the first 24 hours after stroke was related to a
poor clinical outcome after 3 months (Oliveira-Filho et al.
2003). The level of systolic blood pressure after acute
ischemic stroke was found to be inversely related to the
degree of vessel recanalization. In patients without recanalization, systolic blood pressure remained elevated for
longer than in those with successful recanalization (Mattle
etal.2005).Theobservationthataspontaneousblood
pressure rise is present in almost all patients with a relevant vascular occlusion favored treating ischemic stroke
patients with a drug-induced hypertension. A small clinical study analyzed the clinical outcome of 13 patients who
received phenylephrine to increase blood pressure by 20 %
or up to 200 mmHg outside the time window for thrombolysis. Seven of them demonstrated clinical improvement by two points on the National Institutes of Health
StrokeScale(NIHSS)scalewithouttheoccurrenceofany
complication (Rordorf et al. 2001). A further step was
takeninasecondpilotstudyinwhichserialMRIperfusion/diffusion images were also obtained. A significant
clinical improvement was only shown in the group with
medically raised blood pressure. Correspondingly, MRI
demonstrated a significant reduction of the hypoperfused
brain regions and a reduction of the mismatch area in
comparison with the nontreated group (Hillis et al. 2003).
Part A: Principles and
Rules
6
Angiographic Techniques in Neuroradiology
111
Digital Subtraction Angiography ................ 111
Historical Development ......................... 111
TechnicalAspects .............................. 112
Strengths andDisadvantages .................... 113
Magnetic Resonance Angiography .............. 113
Historical Development ......................... 113
TechnicalAspects .............................. 114
Strengths andDisadvantages .................... 115
Computed Tomographic Angiography ........... 116
Historical Development ......................... 116
In recent years, numerous new cross-sectional imaging
techniqueshave evolved,making the choice of the optimal
angiographic technique for a given indication increasingly
complex.
As various techniques, either single or combined, may
provide clinically relevant information, the final diagnostic
algorithms actually applied will be determined by several
factorssuchastechnicalinfrastructure(scanners,workstation), clinical pathways in current use, the hospital’s
size,andlevelofstrokecareprovided,suchastheexistence of a stroke unit or neurosurgical facility. Together
with ongoing technical developments, a specialized investigator, such as a neuroradiologist, would be best qualified
to tailor the imaging protocol to the specific clinical questions posed by the referring physician and the patient’s
needs.
In this chapter, a selection of angiographic methods in
clinical use, such as digital subtraction angiography (DSA),
magnetic resonance angiography (MRA), and computed
tomography angiography (CTA) are described, from historical development to technical aspects, with discussion of
their main advantages and disadvantages.
The chapter concludes with an overview of the current
status of neuroimaging at the Charité Hospital, Berlin. The
value of the different angiographic methods in stroke,
vessel wall pathology, and stenoses of various origin of
the extra- and intracranial brain-supplying vessels as
well as in cerebral venous thrombosis will also be discussed briefly. Further angiographic aspects are discussed
in the selected case histories. The cases presented in this
book do not reflect the current state of stroke-imaging
TechnicalAspects .............................. 116
Strengths andDisadvantages .................... 117
Current Algorithm at the Charité University
Hospital ...................................... 119
Stroke........................................ 119
IntracranialAneurysm........................... 120
Vasculitis...................................... 121
Cerebral Venous Thrombosis..................... 123
Peri-therapeutic Imaging........................ 124
algorithms. They have been chosen from a data pool collected since 2000, especially because of their suitability to
cover important aspects of neurosonology in stroke.
Digital Subtraction Angiography
Historical Development
Conventional angiography is a technique that uses X-ray
pictures to visualize the lumen of blood-filled structures,
such as the cervical and cerebral arteries. The term angiography is derived from the Greek words angeion, “vessel,”
and graphien, “to write or record.” The terms “angiograph”
or, “angiogram” denote the X-ray film or vessel image. A
radiodense intravascular contrast agent is indispensable
for outlining vessel structures. At the present time this is
usually achieved by intravenous administration of a nonionized-iodine-containing contrast medium.
E. Moniz, a Portuguese neurologist, developed cerebral
angiography in 1927 as a technique of contrasted cerebral
X-ray angiograms for the assessment of various central
nervous system (CNS) diseases of neoplastic and vascular
origin (Petit-Dutaillis 1954) and was one of the most important pioneers in this field. He was awarded the Nobel
Prize in Medicine in 1949, although this was for the introduction of frontal leukotomy. The first cerebral angiographies were performed in the late nineteenth century
using cadaveric phantoms, as there was no contrast medium suitable for use in patients available at that time.
When Moniz performed his first angiograms, the carotid
artery had to be laid open for access. In 1929 the German
6 Angiographic Techniques in Neuroradiology112
Fig. A6.1 A–B DSA and MSCTA, posteroanterior (A)andlateral(B)
projection, ICA injection. Regular findings.
physician W. Forssmann, who worked at the Charité Hos-
pital, performed the first cardiac catheterization in a selfexperiment and also received the Nobel Prize in 1956 for
this ground-breaking discovery (Forssmann 1954).
Theuseofasmallintravasculartubeaswellasthedirect
percutaneous vessel puncture, introduced by the Swedish
radiologist S.I. Seldinger in 1953, are the hallmarks of
modern angiography, as no sharp and potentially harmful
introductory devices are left inside the vessel lumen (Seldinger 1953).
DSA, introduced in 1980, permitted serial imaging while
reducing radiationexposure and contrastmedium volume
in comparison with conventional film-screen arteriography. DSA remained the gold standard technique for invasive cerebrovascular angiography until the present day
(Meaney et al. 1980, Reuter 1980). Contrast-enhanced
(ce) images are subtracted from the preceding unenhanced image, thus eliminating all unnecessary image
information and improving vessel-to-background ratio
(Fig. A6.1). For neuroangiography purposes, biplane angiography suites have become standard (Fig. A6.2)asthe
B
Fig. A6.2 A 3D rotational neuroangiography suite (Charité,CBF).
B 3D rotational DS angiogram, lateral view. An aneurysm (arrow)
of the anterior communicating artery is depicted. (Images courtesy
of A. Schilling, MD, Charité.)
morphologic depiction of aneurysms and arteriovenous
malformations (AVMs) is improved, thus reducing procedure time and obviating the need for additional angiographic views (Kleefield et al. 1987). More recently,
three-dimensional (3D) rotational angiography has been
introduced and described as being of special benefit in
neurointerventional treatment planning, such as is required for intracranial aneurysms (Anxionnat et al. 2001,
Sugahara et al. 2002).
Technical Aspects
Access is achieved by puncture of the femoral artery using
the Seldinger technique. Following the intravascular
placement of the introducer sheath, a guidewire is advanced to the level of the aortic arch, followed by a catheter. Assisted by the wire, an endhole-catheter is then
moved cranially into the internal carotid and/or vertebral
arteries for diagnostic angiographic purposes, depending
on the clinical question. If anatomic variants or significant
proximal supraaortic vascular pathology are expected, a
Magnetic Resonance Angiography 113
brachiocephalic angiogram by using the so-called pigtail
catheter may be performed first.
Although spatial resolution of DSA with a pixel size of
about 0.3 mm is closely approximated by multislice CT
(0.35 mm), contrast-to-noise ratio is superior for DSA,
thus improving delineation of tiny vessels (Villablanca et
al. 2002). This might be of special interest if a vasculitis is
included in the differential diagnosis. Primary vasculitis of
the CNS tends to affect medium-sized and smaller vessels,
making detailed vessel delineation a major task.
The total amount of iodinated, nonionic contrast medium injected depends on the procedure and whether, for
example, a brachiocephalic angiogram is required. Approximately 100 mL contrast medium (300 mg I/mL) for
a four-vessel-angiogram including brachiocephalic angiogram should be considered (Leffers and Wagner 2000).
DSA provides not only pathomorphologic information,
but allows visualization of intracerebral hemodynamics by
repeatedly acquiring multiple images per second (usually
three images/s, range from 1/s to 6/s).
Strengths and Disadvantages
DSA is considered to be the gold standard whenever significantly detailed resolution and/or assessment of cerebral hemodynamics is required. As described previously,
vascular imaging issues are constantly changing and cerebrovascular hemodynamics may now be assessed noninvasively with MRA or by using last generation 320-row
CT scanners for time-resolved whole brain CTangiography.
Yet, all these techniques at present suffer from restrictions
compared with DSA, particularly with respect to spatial
and temporal resolution. If interventional procedures may
become necessary within a short period of time, such as in
patients with presumptive basilar artery occlusion, invasive catheter angiography also remains the first line modality.
Contraindications to DSA are comparable with CTA as
they are generally related to the application of iodinated
contrast medium as well as ionizing radiation. Renal insufficiency, hyperthyroidism, and iodine allergy are commonalthoughnotabsolutecontraindicationsforDSA(as
well as CTA). Also, pregnancy is considered a contraindication for DSA if the procedure is not of vital importance
for the mother.
Procedural complications have been reported in the
region of 1–2.3 % of overall incidence of neurologic deficits
and a 0.4–0.5 % incidence of persistent deficit following
cerebral angiography (Heiserman et al. 1994, Kaufmann et
al. 2007, Leffers and Wagner 2000). Yet, non-neurologic
complications were observed in 14.7% in the study by
Leffers and Wagner and clinically silent embolisms were
encountered in up to 44% of patients undergoing DSA if
they had concurrent vascular risk factors (Bendzus et
al.1999). These figures might seem high, but in Leffers’
study the majority of non-neurologic complications were
due to minor groin hematomas. In addition, Burger et al.
(2006) in their study of DSA-related complications of pediatric neurorangiography, which is technically more demanding than in adults, showed that this is a low-risk
procedure (no intraprocedural complications in 241 consecutive pediatric cerebral angiograms) in experienced
hands (for further details, see also Case 24, p. 287).
Radiation exposure is a variable that depends on the DSA
procedure itself (two-, three-, or four-vessel angiography),
vascular anatomy (elongation, anatomic variants), investigator experience, and angiography suite used. Moreover,
various exposure parameters are used, such as effective
dose, CT dose index (CTDI) for CTA, organ dose (for example, lens dose), etc. A typical four-vessel angiogram was
found to result in a patient effective dose of 3.6 millisievert
(mSv) (Marshall et al. 1995), which is within the range for
multislice cervico-cranial CTA (2.2–4.3 mSv for 4- and 64slice CTA), as measured in our institution. The dose received during CTA has also been described as equivalent
to approximately 15 minutes of fluoroscopy time, i.e.,
somewhat greater than typically required for routine diagnostic DSA but not outside the safe limits for diagnostic
radiological assessments (Chapell et al. 2003).
Overall, the procedure is considered to be relatively safe
when performed by an experienced neuroradiologist,
though careful consideration of an noninvasive angiographictechniqueshouldbemadeineverysinglecase.
Magnetic Resonance Angiography
Historical Development
Nuclear magnetic resonance imaging (NMRI), the original
term for MRI, is a radiation-free imaging technique based
on the proton nucleus resonance to a radio-frequency
pulse, emitted (and received) by so-called coils within
the scanner. Although the basic physical principle was
described by Bloch and Purcell in 1946, P.C. Lauterbur
and P. Mansfield shared the Nobel Prize in Physiology or
Medicine in 2003 for developing in the early 1980 s the
underlying principle of an MRI technique that allowed the
generation of images of the human body.
For image generation and spatial encoding, magnetic
gradients are applied together with the radiofrequency
pulse. The resulting data are recorded in a 2 D or 3D image
matrix and the image itself then is created by applying an
algorithm called Fourier transformation. By varying the
scanning parameters, tissue contrast can be altered and
enhancedinvariouswaystoassessdifferentproperties.
With respect to MRA the introduction of FLASH sequences
(fast low angle shot) in 1985 by J. Frahm and co-workers
allowed significant shortening of MRI measuring times, by
combining a gradient echo (GE) sequence with a low-flip
angle pulse and rapid sequence repetition (Frahm et al.
1986).
6 Angiographic Techniques in Neuroradiology114
Tab l e A6 . 1 A selection of MR-based imaging techniques of the cervicocranial vasculature
Abbreviation Name Variants Vasculature Indication Contrast
TOF Time-of-Flight 3 D Arteriography Intracranial vasculopathy No
2 D Venography Cerebral venous thrombosis
PC Phase contrast Venography Cerebral venous thrombosis No
ce 3 D FLASH Fast low angle shot Arteriography
Venography
ce = contrast enhanced
Cervicocranial
vasculopathy
medium
Yes
Technical Aspects
MRA is a noninvasive tool, that is, there is no radiation
exposure and no administration of iodinated contrast medium. MRA has therefore become a widely used imaging
approach for the cervico-cranial vascular system. In the
past 10–15 years, various contrast and noncontrast-enhanced MRI techniques have been described, requiring
some background knowledge in order to tailor the MR
study design to the question raised by the referring clinician. An overview of common, currently applied MRA
techniques in clinical settings is given in Table A 6.1.Basically one has to differentiate between primary vasculature
imaging techniques with intrinsic or extrinsic contrast and
3D GE sequences with or without fat saturation (FS) providing vessel visualization as a secondary effect.
Primary vascular imaging techniques with intrinsic contrast are mainly the so-called time-of-flight (TOF) MRA
(Fig. A6.3A) and the phase-contrast (PC) MRA. The arterial-spin-labeling MRA also belongs to this group, but as
this technique is not used in a routine setting it will not be
addressed here. Intravenous contrast medium (gadolinium) application is required in 3D GE FLASH technique
(Fig. A6.3B), with or without elliptic-centric readout as
well as dynamic 2 D GE angiography.
Fig. A6.3 MR arteriography techniques. A 3D time-of-flight, axial
MIP. B Contrast-enhanced FLASH 3D GE, coronal MIP.
Time-of-Flight Magnetic Resonance Angiography
Most commonly, a GE measurement is performed, characterized by a short repetition time (TR) and slice acquisition
perpendicular to the direction of blood flow. The difference between the unsaturated and presaturated spins
leads to high intravascular signal intensity. The flowing
blood moves unsaturated spins from outside into the
imaging plane and enables signal generation, as opposed
to the stationary and saturated tissue spins. When a presaturation slab is established on one side of the imaging
plane, those spins that flow from the same side do not
deliver a signal, thus rendering this technique either arteriography or venography (direction sensitive). As only
fresh, inflowing blood will deliver maximum signal, slow