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Pial Arteriovenous Malformations
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Fig. 3.4a–j. A 42-year-old woman
presenting with two episodes of
seizures. Pre- and post-contrast CT
a, b) show a right temporal
scans (
AVM. A slightly hyperdense structure is visible before and, strongly
enhanced, after injection. Frontal
and axial T
ize the AVM within the white matter
of the right temporal lobe, but determination of the nidus border is diffi cult (
not show the nidus limits precisely
and affords poor understanding of
the AVM architecture (
angiography performed during embolization shows the arterial feeders, nidus size and venous drainage much better (
injection during embolization allows a much better understanding
of nidus arteriovenous architecture.
Distal catheterization shows immediate opacifi cation of draining veins
g). Such arteriovenous anatomy
(
allows very effi cient embolization
with easy gluing of origin of draining veins (
after second embolization, followup angiography showed complete
occlusion (
images perfectly local-
2
c, d). A 3D TOF image does
e). Digital
f). Superselective
h). Three and 18 months
i, j)
a
c
b
d
65
e
h
f
i
g
j
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C. Cognard, L. Spelle, and L. Pierot
a
c
Fig. 3.5a–d. A 63-year-old woman presenting with common headaches. Post-contrast CT scan shows an abnormal vessel
within the right temporal lobe (
depicts a very small superfi cial temporal AVM draining into a single, slightly dilated, superfi cial vein (
plied by very short “en passage” feeders. Due to patient’s age, absence of symptoms, and AVM morphology no therapy was
planned
3.4.2.2
MR
a). Axial proton density image shows enlarged fl ow void vessel (b). Digital angiography
Anatomic Analysis
b
c, d). AVM is sup-
Conventional sequences (T1, T2, T1 with gadolinium)
Patients presenting with ruptured AVMs are usually
examined in the acute phase by a CT scan. MRI is
currently used in case of unruptured AVM or to fi nd
the underlying lesion in case of lobar hematoma,
generally days or weeks after the bleeding.
Given the different sequences available in MR imaging, MRI is able to give three levels of analysis of
the AVM:
Anatomic analysis using conventional sequences
Vascular analysis using MR angiography
Functional analysis using fMRI
enable a very precise analysis of the brain AVM
(Smith et al. 1988b). On T
- and T2-weighted images,
1
circulating vessels have no signal because of the fl ow
void phenomenon (Fig. 3.5). On T
-weighted images
1
with gadolinium, vessels are enhanced.
The size and the anatomic location of the nidus
are precisely delineated by MRI (Figs. 3.4 and 3.6).
Smith et al. (1988) showed that the size of the nidus
was more precisely shown by MRI than by conventional angiography. Anatomic location was always
better defi ned by MRI than by angiography. Depic-
d
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67
a
c
b
d
e
Fig. 3.6a–f.
MR image shows a left temporopolar small brain AVM (
medial aspect of the left temporal lobe (
age (
and should be the fi rst target of embolization. Superselective catheterization of the lenticulostriate artery harboring the
aneurysm allowed gluing of both aneurysm and AVM (
incomplete obliteration of the AVM with disappearance of any nidus but persistent early venous drainage (
A 27-year-old man presenting with a small deep hematoma with ventricular hemorrhage. Axial proton density
c). An intranidal aneurysm or false aneurysm is visible; this must be considered the most likely cause of the bleeding
f
a) and the hematoma in a remote, more posterior location at the
b). Internal carotid injection shows the temporal AVM with a deep venous drain-
d). Final follow-up angiography after four embolizations showed
e, f)
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C. Cognard, L. Spelle, and L. Pierot
tion of arterial feeders and draining veins is often
incomplete with conventional sequences.
MRI is also a good tool to clearly demonstrate
parenchymal lesions caused by the AVM. Because
of the high sensibility to hemosiderin, MR is able to
depict a recent, but also an old hematoma (Fig. 3.7).
However, the presence of a recent hematoma may
mask a small AVM leading to a false-negative MR
(Fig. 3.8). In the absence of hemorrhage, perinidal
abnormalities of signal, particularly hypersignal
on T
-weighted images, can be evidence of perini-
2
dal ischemic changes or gliosis. Fluid-attenuated
inversion-recovery sequence (FLAIR) seems to
be superior to the conventional T
-weighted fast
2
spin-echo sequences in the assessment of intralesional and perilesional gliosis (Essig et al. 2000).
More precisely than CT, MR is able to depict either
Fig. 3.7a–i. A 34-year-old man who presented with a fi rst episode of
bleeding in 1985 from a deep brain AVM. The patient was treated with radiosurgery. He presented a new hemorrhage in 1987, with major clinical
consequences (right severe hemiparesis and aphasia).
performed in 1998 shows deep paraventricular AVM with old hematoma
of left striatum and posterior limb of internal capsule. Three-dimensional TOF angio-MR in sagittal and frontal views (
delineation of nidus limits and angioarchitecture evaluation. Digital
angiography by internal carotid injection in AP view (
injection in sagittal view (
nidus shape and architecture, and drainage. Very early phase of vertebral injection depicts a small intranidal aneurysm or false aneurysm of
distal thalamo-perforating artery; this was considered a weak point of
the malformation and treated fi rst (
posterolateral choroidal arteries performed immediately after thalamoperforating artery and aneurysm gluing showed intranidal wedge positioning of catheter tip (
intravent ricular hemorrhage. Glue injection was perfor med immediately
after bleeding was recognized (
intraventricular hemorrhage but no parenchymal hematoma (
nal ventricular shunting was performed just after embolization. Patient
was awakened 3 days later and showed moderate worsening of initial
symptoms. At 3-month follow-up examination he had completely recov-
a
ered his initial clinical status
morphological changes induced by the AVM itself
or its parenchymal or ventricular consequences:
parenchymal atrophy with focal dilatation of the
ventricular system; compression of the ventricular
system in case of mass effect caused by the AVM;
hydrocephalus in case of previous hemorrhage or
if the ventricular system is compressed by enlarged
draining veins of the AVM.
Vascular Analysis
Until recently, only phase-contrast and time-offl ight techniques were available to study the vascular system (Fig. 3.2). These have been demonstrated
to be of value in providing three-dimensional
representations of AVM vascular architecture
( Marchal et al. 1990). However, these techniques
a Axial T2 image
b, c) allows good
d) and vertebral
e) provide the same information about feeders,
f). Superselective catheterization of
g). Late venous phase of this injection showed
h). Post-embolization CT scan confi rmed
i). Exter-
cb
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d
69
g
e
f i
h
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C. Cognard, L. Spelle, and L. Pierot
a
d
e
b
f
Fig. 3.8a–f. A 42-year-old woman who presented with sudden headaches
and aphasia at 7 months of pregnancy. CT scan showed a left temporal
hematoma. Digital angiography was performed and considered normal
(not available). Pregnancy was carried out to term and cesarean delivery
was performed. She progressively recovered and came to our institution
3 months later. CT-scan and MR were performed at that time. CT scan
showed chronic hypodense hematoma (
showed hyperintense signal within the hematoma due to extracellular
methemoglobin (
normal (
ered not accurate enough to rule out a small AVM. Digital angiography
depicts a small left temporal micro-AVM (
tion allowed more precise understanding of nidus morphology (
distal catheterization did not obtain wedge positioning of catheter tip
c
and good control of the fl ow. Consequently, embolization was not performed and the patient was treated with radiosurgery
d). Both axial conventional images and angio-MR were consid-
b, c). Three-dimensional TOF MIP reconstruction was
a). MR T1 and T2 axial images
e). Superselective catheteriza-
f). More
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71
have limited anatomic coverage and are not able
to adequately depict the precise anatomy in a large
number of cases: The correct size of the nidus cannot be assessed (Fig. 3.4); intranidal aneurysms are
frequently not visible (Fig. 3.7); depiction of the
draining veins is inconsistent (Fig. 3.9); small-caliber vessels and regions of slow blood fl ow cannot
be consistently revealed (Fig. 3.9) (Edelman et al.
1989; Marchal et al. 1990; Nüssel et al. 1991).
Moreover, dynamic information is not provided by
these sequences.
Multiple overlapping thin-slab acquisition timeof-fl ight MR allows greater anatomic coverage and
produces better signal-to-noise ratio and higher
resolution than conventional MR angiography, but
slab boundary artifacts represent a major limitation
(Liu and Rutt 1998; Wa r re n et al. 2001).
Gadolinium-enhanced MRA techniques are currently in development which are superior to TOF MR
angiograms but still inferior to DSA images for depiction of AVM components because of limitations
in both temporal and spatial resolution ( Takano et
a
Fig. 3.9a–d. A 51-year-old woman who presented with a left
hematoma of the posterior limb of the internal and external
capsule in 1985, with subsequent slight right hemiparesis
and lateral right hemianopia. Digital angiography was performed in 1985 and 1994 and showed a sylvian fi ssure AVM.
Due to the angioarchitecture, no treatment was decided on
at that time. The patient returned in 1999 and complained
about recurrent episodes of right side hemiparesthesia. Ax-
images done at that time showed sequelae of a deep
ial T
2
hematoma and abnormal vessels along the wall of the posterior aspect of the lateral ventricle (
TOF angio-MR depicts very small abnormal vessels arising
from left middle and posterior cerebral arteries (
internal carotid injection shows an AVM extending into the
left sylvian fi ssure supplied by numerous small “en passage”
feeders coming from the branches of the middle cerebral
c). Venous drainage is very abnormal, with a large
artery (
ectatic vein draining into a single small narrowed vein to
the transverse sinus (
appropriate due to the arterial feeder anatomy. Patient was
sent to radiosurgery
d). Embolization was considered in-
a). Three-dimensional
b). Left
b
c
d
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C. Cognard, L. Spelle, and L. Pierot
al. 1999; Griffi ths et al. 2000; Wa r r en et al. 2001;
Far b et al. 2001).
Functional Analysis
Functional MRI (fMRI) includes perfusion and diffusion imaging and study of brain function.
The role of DWI has to be determined (Ducreux
et al. 2001). The nidus usually has a low signal with
a large and homogeneous increase of the apparent
diffusion coeffi cient (ADC). However, to date DWI
does not play a major role in AVMs.
Perfusion MRI is an additional tool, but its role
in brain AVMs is also still unclear. It may be possible to evaluate hemodynamic characteristics of
different AVMs, but no scientifi c data are currently
available.
Functional MRI activation has been studied
largely in patients with brain AVMs (Latchaw et
al. 1995; Maldjian et al. 1996; Schlosser et al.
1997; Vikingsta d et al. 2000; Lazar et al. 2000;
Alkadhi et al. 2000; Carpentier et al. 2001).
fMRI activation is a potentially very interesting
tool to depict functional areas of the brain, when a
brain AVM is located in an eloquent area, particularly sensorimotor, visual, and language cortex.
Bold sequences used for the performance of fMRI
activation are based primarily on the detection of
hemodynamic changes in the cortex during the performance of a task. Given the huge hemodynamic
modifi cations induced by the AVM in the perinidal
parenchyma, there is some doubt regarding fMRI
activation patterns.
In the great majority of cases, no activation is
detected inside the nidus during the performance
of a task. This could be related to the absence of
functional tissue within the nidus, but the detection of subtle and minor activation within an AVM
could also be obscured by the complex relationships between the BOLD effect and AVM circulatory patterns (Viki ngstad et al. 2000). Activation
can be observed in the cortical regions adjacent to
AVMs. In the majority of cases where brain AVMs
are located in eloquent areas, a shift of the activated
areas with a frequent interhemispheric transfer is
observed.
A tudy showed a discrepancy between the superselective Wada test and fMRI activation in a
patient with a left frontal brain AVM (Lazar et al.
2000). An area which was activated during f MRI
was not detected as a language area by the Wada
test.
Thus, fMRI activation has a potential for the
study of brain function in brain AVMs, but larger
series are necessary to evaluate the liability of this
technique.
3.4.2.3
Selective and Superselective Angiography
As shown in Section 3.3.2.1, many anatomic factors
have to be analyzed to evaluate the risk of rupture
of an AVM and to decide which treatment is appropriate. Despite recent developments, CTA and
MRA are currently not suffi cient to obtain a precise description of the AVM from an anatomic and
hemodynamic point of view. Selective angiography
is still always necessary to make a decision regarding the treatment. In summary: the diagnosis of
an AVM nowadays is usually based on CT or MR;
the exact and therapeutically relevant anatomic and
functional information still has to be obtained by
catheter angiography.
Technically, selective angiography has to be performed according to a rigorous protocol. To assess
as precisely as possible the anatomic components
of the AVM, it is important to inject selectively the
internal and external carotid arteries and vertebral
arteries. Analysis of the arterial feeders, nidus,
and venous drainage is obtained by performing
multiple projections (anteroposterior, lateral, and
oblique). Three-dimensional angiography may be
helpful.
However, even excellent angiograms are often inadequate for reaching correct therapeutic decisions
(Nakstad and Nornes 1994). The exact anatomy of
large feeding arteries may be obscure with selective
injections. Small feeding arteries are sometimes not
visible on selective angiograms. Although the size of
the nidus is generally well evaluated by selective angiography, intranidal aneurysms (Fig. 3.7) and direct intranidal AV fi stulas are often misdiagnosed.
The venous drainage of the AVM is generally well
studied by selective angiography, but the compartments of the AVM and their venous drainage are often not depicted because the AVM is injected as a
whole (Fig. 3.4).
For all these reasons, superselective angiography often gives a more detailed analysis of the
AVM and may become more important in making
the diagnosis. Superselective angiography is performed by manual injection of each separate arterial feeder. It is usually the fi rst step of embolization.
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3.4.3
Imaging Strategy
Imaging strategy is closely related to the clinical
presentation (rupture of the AVM or not) and the
clinical status of the patient.
3.4.3.1
Ruptured AVM
In this situation, the patient has the clinical presentation of a parenchymal hematoma or a subarachnoid hemorrhage or both. The fi rst examination is
the CT scan, which has a high sensibility to detect
intracranial hemorrhage in the acute phase with a
high specifi city.
Contrast-enhanced CT scan and CT angiography are becoming more useful. Small AVMs may be
mistaken by CTA and the anatomic data provided
by this technique are often not suffi cient to make a
therapeutic decision. In patients with a large spaceoccupying hematoma CTA can be performed to try
to indicate to the neurosurgeon whether a brain
AVM is the underlying cause of bleeding, before
emergency surgery is performed.
With the exception of this specifi c situation, the
next step after the diagnosis of the hemorrhage is selective a ngiography. In case of isolated subarach noid
hemorrhage or when a brain hematoma may be related to a ruptured aneurysm, it has to be performed
emergently. In other cases, the time to perform angiography is a matter of debate. When an intraparenchymal hematoma is present it can compress the
AVM, leading in some cases to a false-negative diagnosis. For the same reasons, anatomic analysis in
the acute phase may be erroneous. Therefore, selective angiography should probably be delayed. However, angiography is often performed at the acute
phase of bleeding to obtain a defi nite diagnosis
and to have all the information at hand concerning
the AVM in case the patient’s clinical status should
worsen, requiring prompt surgery. Moreover, when
the cause of bleeding is unclear (AVM or associated
aneurysm), angiography is also important to determine if an associated aneurysm is present, and in
such instances angiographic criteria combined with
CT or MR fi ndings may be helpful to determine the
site of bleeding (Fig. 3.6).
After the acute phase of bleeding, the therapeutic
approach to the AVM will be defi ned on the basis of
anatomic data provided by MRI and selective angiography (Figs. 3.2 and 3.7).
3.4.3.2
Unruptured AVM
For an unruptured AVM, CT is not indicated; the fi rst
step is MRI and MRA to obtain all the information
needed to make a therapeutic decision. In a great number of cases, clinical data, MRI, and MRA are suffi cient
to make a decision regarding therapeutic options: – in
some cases, it is clear that treatment should be conservative, and in this situation selective angiography is
not needed; in other cases, the AVM has to be treated
and the next step depends on the therapeutic strategy.
If embolization is the fi rst step of treatment, there is no
reason to perform fi rst a selective angiogram and then
superselective angiography and embolization. In this
situation, complete information has to be given to the
patient and selective, superselective angiography and
the fi rst embolization have to be performed at t he same
time. If surgery is the modality of choice, selective angiography has to be performed fi rst. If radiosurgery is
indicated as the sole treatment, selective angiography
has to be performed immediately before treatment for
stereotactic localization of the AVM.
In some cases, the therapeutic decision is not
clear after MRI and MRA, and selective angiography
is performed to make a decision.
3.4.4
Classi cation of Brain AVMs
Several systems have been designed to classify
patients with brain AVMs regarding surgical risk
(Spetzler et al. 1992) and individual hemorrhagic
risk (Nataf et al. 1998).
3.4.4.1
Classi cation of Spetzler and Martin
The Spetzler and Martin (1986) c lassifi cation was
established to grade AVMs according to their degree
of surgical diffi culty and the risk of surgical morbidity and mortality. To assign an AVM grade, the
size, the venous drainage, and the eloquence of the
adjacent brain are determined from angiography,
computed tomography, and MRI. A numerical value
is assigned for each of the categories:
1. Size of the AVM: small (< 3 cm): 1;
medium (3–6 cm): 2; large (> 6 cm): 3
2. Eloquence of adjacent brain:
non-eloquent: 0; eloquent: 1
3. Pattern of venous drainage:
superfi cial only: 0; deep: 1
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C. Cognard, L. Spelle, and L. Pierot
The grade of the lesion is obtained by summing
up the points assigned for each category. As previously outlined, the Spetzler-Martin grading system
is clearly a surgical one and is of little value for interventional neuroradiologists and radiotherapists
(Mansmann et al. 2000).
3.4.4.2
Classi cation of Nataf et al.
Based on a retrospective study of 250 consecutive
patients treated by radiotherapy, the classifi cation of
Nataf et al. (1998) was established to evaluate individually the risk of hemorrhage. Five angiographic
parameters were considered to be determinants of
the bleeding risk, leading to a four-grade classifi cation:
Grade I: No risk factor
Ia: With venous recruitment
Ib: Without venous recruitment
Grade II: Venous stenosis or venous refl ux
Grade III: Deep venous drainage only
Grade IV: Intra- or juxtanidal aneurysm
In the series mentioned, there were 13% of hemorrhages in grade Ia, 38% in grade Ib, 48% in grade II,
and 90% in grades III and IV.
3.5
Therapy
3.5.1
Neurosurgery
Neurosurgery may be indicated in emergency to
remove a large life-threatening hematoma. Only
superfi cial AVMs, more easy to control, may be removed with the hematoma. When surgery of a brain
AVM i s d i f fi cult, the hematoma may be removed
and the treatment strategy may then be decided
without hurry regarding AVM location, size, and
architecture. Treatment of AVM is then performed
later, after the patient has recovered. Very few papers
report patient outcome after early surgical treatment of intracerebral hemorrhage caused by AVMs
(Lamy et al. 1990; Jafar and Rezai 1994; Puzzilli
et al. 1998). The numbers of patients are too small
to allow any fi rm conclusions. In the largest series
of 24 operated patients there were 53% good results,
25% comatose patients, and 21% deaths (Lamy et
al. 1990).
3.5.1.1
Elective Surgery
In a non-emergent situation surgery is elective, by
the standard microsurgical technique with an operating microscope (Ogilvy et al. 2001). Usually,
the arterial feeders are attacked fi rst, followed by
the nidus, and only at the very end of treatment
the draining veins (Yasargil 1988). The goal of
surgery is complete cure, which should be proven
by intraoperative and postoperative angiography.
In case of residual AVM a new surgical approach
should be considered immediately to avoid subsequent bleeding that may be favored by subtotal occlusion of the nidus. Radiosurgery or embolization
of postoperative residual AVM may be considered
even if the fi rst carries a risk of bleeding until complete occlusion.
3.5.1.2
Outcome of Direct Surgery
A recently published meta-analysis reviewed all series of more than 50 patients published since 1990
(25 series, 2452 patients) (Castel and Kantor
2000). The clinical presentation was hemorrhage
in 57% of cases. Global mortality varied from 0%
to 15%, mean 3.3% (68 of the 2452 patients). It
was below 5% in 81% of the reported cases. Postoperative global morbidity was 1.5%–18.7%, mean
8.6%. Hamilton and Spetzler (1994) made a pro-
spective study of 120 consecutive patients who underwent complete microsurgical excision of their
AVM, with or without previous embolization, to
evaluate correlation between the Spetzler-Martin
grade and clinical complications. Permanent major morbidities were 0% for grades I–III, 21.9% for
grade IV, and 16.7% for grade V. Defi cit related
to surgery and evaluated 6 weeks after operation
was 0% in grade I, 4.2% in grade II, 2.8% in grade
III, 31% in grade IV, and 50% in grade V. Mortality directly related to surgery was 0%. Risk of
surgery is quite well estimated by the Spetzler Martin grading system, with a favorable outcome
in 92%–100% grade I, 95% grade II, 88% grade III,
73% grade IV, and 57% grade V ( Spetzler and
Martin 1986; Heros et al. 1990). Series in which
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