(Stroke. 2001;32:1430.)
© 2001 American Heart Association, Inc.
Comments, Opinions, and Reviews |
Reporting Terminology for Brain Arteriovenous Malformation Clinical and Radiographic Features for Use in Clinical Trials
Correspondence to W.L. Young, MD, Center for Cerebrovascular Research, University of California, San Francisco, San Francisco General Hospital, 1001 Potrero Ave, Room 3C-38, San Francisco, CA 94110. E-mail YoungW{at}anesthesia.ucsf.edu
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Abstract |
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 Top Abstract IntroductionA. General DefinitionsB. Location and SizeC. Venous DrainageD. Arterial SupplyReferences |
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"If you wish to converse with me," said Voltaire, "define your terms." How many a debate would have been deflated into a paragraph if the disputants had dared to define their terms!
Will Durant: The Story of Philosophy
Key Words: cerebrovascular disorders • clinical trials • vascular malformations
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Introduction |
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TopAbstractIntroductionA. General DefinitionsB. Location and SizeC. Venous DrainageD. Arterial SupplyReferences |
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The goal of this writing group is to provide guidelines for use in the design of clinical trials, that can aid in providing sufficient uniformity of definitions for appropriate selection and stratification of patients, as well as analysis of data. We emphasize that this document is not to be construed as a standard-of-care or intended for current routine clinical grading or classification, such as the Spetzler-Martin surgical scoring system.1 The reporting standards presented in this document represent an "ideal" and are intended for use in research protocols rather than in quality assessment of individual practice. The definitions represent one set of possible guidelines for constructing a reportable research data set; they are not intended to represent the only ones of importance or interest to collect in clinical trials, ie, they are not proposed as a minimally acceptable set of data.
Rather, our intent is to facilitate the production of scientifically rigorous results that are capable of being reliably compared between related studies. In some cases, the definitions used are arbitrary or operational but have been recommended by consensus of the writing group for the sake of consistency in reporting.
Evaluation and treatment of brain arteriovenous malformations (BAVMs) is often a multidisciplinary exercise involving neurosurgeons, neurologists, neuroradiologists, radiotherapists, and numerous other medical specialists. A recent review by an AHA writing group2 has surveyed the literature to develop current guidelines for the clinical management of BAVMs. Despite these tremendous efforts to synthesize existing knowledge on this topic, there remain inconsistencies with nomenclature and definitions of terms for research purposes.
This lack of consistency in data reporting by investigators is a major challenge for progress in treatment of BAVMs. A set of well-considered definitions can allow different investigators to publish results that are directly comparable. The intent of this writing group is to formulate a set of definitions based on current practice and imaging technology that may serve as a frame of reference for future reports and of future clinical trials.
One of the major challenges to research of BAVMs is the lack
of widely accepted prognostic systems other than the Spetzler-Martin
scale for estimating surgical treatment
risk.1 Systems are just being
developed for radiosurgery.3
Design of definitive clinical trials would be aided by better
understanding of the natural history and treatment risks associated
with BAVMs. Careful definitions of prognostic variables and
outcomes will be required in this effort. A recent study suggested a
poor interobserver agreement on basic morphological
attributes,4 emphasizing the
importance of clear, simple, and reproducible definitions of terms for
risk or prognostication variables. These definitions should include
categories or ratings detailed enough to distinguish clinically
important differences. In addition to providing some basic points of
agreement between investigators, these definitions are meant to
stimulate critical discussion of a set of difficult issues with regard
to the anatomic and clinical classification of BAVMs.
Table 1
shows an overview of the
definitions.
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Use of the terms that are self-referential or that presuppose mechanism, such as "cerebral steal," are discouraged. Neurological signs or symptoms and angioarchitectural descriptions are preferred that are nonjudgmental in terms of mode of presentation, mechanism, or structure.
Whenever possible, we have recommended reporting continuous data rather than categorical data. For example, we recommend that BAVM sizes be reported in millimeters rather than some categorical grouping of small, medium, and large. It is always possible to go from continuous to categorical data, but it is not possible in the other direction. Many of the responses require multiple attributes, which is denoted as "choose all applicable."
It is not currently known how the rare occurrence of multiple BAVMs in a single patient influences the natural history of the disease. Therefore, each lesion should be characterized separately.
Each section of clinical and radiographic
features below (A1 through D6) is listed, in corresponding outline
format, in Table 1
. A summary of the fields and their ranges is given in
Table 2.
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A. General Definitions |
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TopAbstractIntroductionA. General DefinitionsB. Location and SizeC. Venous DrainageD. Arterial SupplyReferences |
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An operational definition of BAVM is an abnormal tangle of vessels that results in arteriovenous shunting (nonnutritive blood flow) demonstrated by 4-vessel cerebral contrast angiography, which is generally considered the diagnostic gold standard. BAVM may coexist with other vascular disorders, such as moyamoya disease5 or hereditary hemorrhagic telangectasia.6 BAVM does not include pure vein of Galen AVMs,7 cavernous malformations, dural arteriovenous fistulas (DAVF), venous malformations, venous varices, or any of the other rarer types of cerebrovascular anomalies.8 9 BAVM is the preferred and more precise term than cerebral, which excludes more caudal structures, and older and imprecise terminology such as "true" AVM or "pial" AVM (some BAVMs do not reach any pial surface). Further, "cerebral" AVM might be abbreviated as CAVM, which might lead to confusion with cavernous malformation. It is not the purpose of this writing group to make the definitive definition of BAVM (a set of attributes that all BAVMs and only BAVMs possess), and there will continue to be cases of mixed lesions, which defy classification into a simple scheme.10 11
A.1. Clinical Presentation
Comment
Clinical presentation is obtained
from the neurological history. It is the clinical picture of the event
that brought the patient to a medical encounter that directly led to
the discovery of the BAVM. The clinical presentation should
be temporally related to the imaging study (see below), which confirms
the presence or absence of bleeding. Each component can be answered in
either a yes or no fashion. It should always be clear in reporting
whether hemorrhage was part of the initial
presentation, whether or not other signs and symptoms were
present. For this reason, each of the presentation
categories should have a response.
Incidental
Presentation would refer to a
clinical presentation that was clearly unrelated to the
BAVM regarding the indication for imaging, eg, blunt head trauma after
a motor vehicle accident.
Hemorrhage refers to
bleeding into the brain or its surrounding spaces.
Seizure refers to any type of
partial or generalized seizure activity.
Focal neurological deficit
refers to a deficit that may or may not be related to seizure or
hemorrhage. Other would
refer to other precipitating signs or symptoms leading to the discovery
of the BAVM that may be related to the presence of the lesion, such as
a bruit.
Of all of the presenting signs and symptoms, headache is the most subjective. It deserves some special mention because it is not at all clear what percentage of headaches are actually related to the BAVM. It may be worthwhile detailing the nature of the headache in terms of sudden, new-onset, change in frequency or character as opposed to chronic, unchanged headaches.
Rationale
Because hemorrhage is the most important
presentation of AVMs, both in terms of occurrence as well
as morbidity,12 a clear
dichotomy between hemorrhagic and nonhemorrhagic
presentations should be made. Evidence
exists that prior bleeding increases the risk of subsequent
hemorrhage,13 14
but this has not been incontrovertibly demonstrated, and there are data
that suggest no influence of initial presentation on
subsequent hemorrhage rate.15 Incidental
presentation is also particularly important, as there may
be a trend toward detecting more asymptotic lesions with the increasing
availability of tomographic brain imaging.16
A.2. Date of Presentation
Comment
The date of presentation (DOP) is defined
as the date on which the patient experienced signs or symptoms that
led, as a proximate cause or instigation, to medical evaluation
resulting in definitive diagnosis of BAVM. DOP may not be synonymous
with date of evaluation but should be logically and temporally
related.
Example
Patient presents with a grand mal seizure on
January 1. Evaluation by primary care physician on January 8 leads to
CT scan, which confirms a structural lesion. MRI on January 9 strongly
suggests the presence of BAVM.
Four-vessel cerebral contrast angiography on January 23 confirms
diagnosis. DOP is January 1.
Related concepts would include "index date" and "diagnosis date." The index date would be the medical encounter through which the "date of presentation" was learned (January 8 in the example above). The diagnosis date would be January 23.
Rationale
Date of presentation is necessary to assess
natural history aspects of lesion. It is also used to calculate age at
presentation, which may be associated with both natural
history14 17 and
treatment risks.18 There is
commonly a time lag between the date of presentation and
definitive diagnosis of BAVM.
A.3. Imaging Source and Date
Comment
The imaging source and date (IS&D) of the CT, MRI, MRA,
4-vessel diagnostic cerebral angiography, superselective
cerebral angiography, etc, nearest in time to the patient’s
presentation should be reviewed.
Rationale
Anatomic information may be dependent on the imaging
modality used to obtain it. The most obvious example would be BAVM size
that can be estimated by angiography or MRI. MRI will tend to
overestimate size of the nidus because adjacent arterial
and venous structures may not be adequately delineated from the true
nidus (BAVM size is broken out into both because of its central
importance to risk assessment; see below).
The source of the data collected can introduce other bias, possibly unknown, into the interpretation. IS&D is important to note because there may be significant differences in the times of obtaining multiple imaging modalities.
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B. Location and Size |
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TopAbstractIntroductionA. General DefinitionsB. Location and SizeC. Venous DrainageD. Arterial SupplyReferences |
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B.1. Lesion Side
Comment
Side refers to BAVM location in the brain when the lesion is located exclusively on one side or other. If the BAVM involves a midline structure bilaterally, it would be classified as midline. If there were multiple AVMs, each one would be described separately.
Rationale
Side of lesion will influence treatment risk in some
cases with lesions in the dominant
hemisphere.
B.2. Handedness
Comment
Handedness is obtained from the neurological
history.
Rationale
An estimation of hemispheric dominance can be gleaned,
potentially influencing treatment
risk.
B.3. BAVM Size
Comment
Size, measured in millimeters, is ideally
recorded from 2 sources: both MRI and angiography
(Figures 1 and 2). The size, in 3 dimensions, is
measured on the pretreatment MRI in sagittal, coronal, and axial views,
which includes the BAVM’s largest diameter. If the 3-dimensional
geometry is such that the longest axis is misrepresented by
LxWxH measurements in the standard projections, then the
dimensions can be inferred from the slice thickness and "stacking"
multiple levels in the standard projections
(Figure 3).
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The size in 3 dimensions is measured on the pretreatment angiogram in lateral and anteroposterior projections, or in whatever additional projections are available that include the BAVM’s largest diameter. Sizing markers can be placed on both sides of the head during angiography, but magnification errors with angiography must be carefully considered.
From these dimensions, a calculation can be made to estimate BAVM volume in milliliters with the ABC/2 formula.19
Rationale
BAVM size may be an important element of risk
assessment for natural history
risk.20 21 22 23
Largest dimension is especially important because it appears to have
the strongest correlation with hemorrhagic presentation,
given multiple
dimensions.20 24
It is definitely a risk factor or treatment risk, both for surgery1 and radiosurgery.18 Although BAVM can usually be estimated from standard views on MRI and angiography, if the longest axis cannot be obtained, then the dimensions can be estimated as described above.
B.4. BAVM Location
Comment
Anatomic locations are for general grouping purposes.
The brain location (topographic location) may be distinct from the
vascular supply location. There is considerable overlap with
"eloquence." Multiple sites are possible.
Rationale
Certain areas may have different treatment risk (also
covered under "eloquence") and natural history
risk.3 13 25 26
B.5. BAVM Eloquence
Comment
Language cortex is defined as left hemisphere unless
additional clinical data suggest otherwise. The locations listed are
primarily as per the Spetzler-Martin
score,1 the only difference
being the addition of "thalamus/hypothalamus/basal ganglia" and
"other eloquence." Multiple sites are possible. Although we have
not added it to the list, the question was raised of whether
nondominant parietal lobe should be considered eloquent, as
visuospatial deficits may be underrecognized but
disabling.
Rationale
Eloquence of adjacent tissue is a critical piece of
information for treatment planning. The Spetzler-Martin score is the
most widely used system in current practice. Unfortunately, it reflects
anatomic considerations only. Ideally, there would be some validated
sensitive and specific indicator of eloquence, ie, functional MRI
testing or positron emission tomography. Until such means are routinely
available, the anatomic method is simple and reproducible at the
expense of precision and accuracy.
The operational definition proposed above is recommended despite the fact that true function can only be known by some type of pharmacological, physiological, or neurological provocative testing. Particularly in the case of AVMs, function may reside in nonclassic locations.27 28 29 If eloquence has been determined physiologically by functional MRI, Wada testing, or brain mapping, this information can be reported whenever possible. The same would apply to clues to altered functional anatomy that may have become apparent from either the natural history or response to treatment, eg, a bleed or a resection resulting in an unexpected neurological deficit.
B.6. BAVM Border With Adjacent Brain
Comment
MRI islands or peninsula of normal brain tissue within
the BAVM nidus protruding into what is surgically or radiosurgically
treatable BAVM nidus, as opposed to sharply demarcated border with
neighboring parenchyma
(Figure 4).
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Rationale
The border with adjacent brain may have implications
for surgical resection20 and response to
radiosurgery.13
B.7. BAVM Hemorrhage
B.7.1. Evidence of NEW BAVM Hemorrhage
Comment
Evidence of NEW BAVM hemorrhage is noted if
there appears to be blood products on MR or CT likely to be
associated with BAVM presentation.
B.7.2. Age of NEW BAVM Hemorrhage
Comment
The age of the hemorrhage is estimated in
number of days.
B.7.3. Is NEW BAVM Hemorrhage Symptomatic?
Comment
The imaging evidence should be consistent with
the patient’s clinical presentation. The main criterion
for symptomatic is a direct temporal relationship to the
indication for imaging.
B.7.4. Evidence of OLD BAVM Hemorrhage
Comment
Evidence of OLD BAVM hemorrhage includes all
instances of CT or MR evidence of bleeding that is NOT temporally
related to imaging for current signs and symptoms. In addition to such
blood of indeterminate age, it would also include indirect evidence of
old hemorrhage, ie, encephalomalacia adjacent to the lesion
consistent with a prior hematoma, as well as
hemosiderin found incidentally at microsurgical
resection.12
B.7.5. Age of OLD BAVM Hemorrhage
Comment
Estimate age of hemorrhage in months; if >1
year, choose "12."
B.7.6. Was OLD BAVM Hemorrhage Symptomatic?
Comment
Is the imaging evidence of old BAVM hemorrhage
consistent with any prior symptoms (transient focal
neurological abnormalities, prior seizure of any type with no other
known precipitating causes) or not related to any known prior symptoms
or events?
Rationale
The writing group recognizes that the relationship of
imaging signs of hemorrhage may be a difficult judgment, as
many lesions have bled silently as evidenced by
hemosiderin deposits seen during microsurgical
resection.12 Nonetheless, it
is a judgment that investigators must make in order to define the
clinical behavior of a class of lesions that may be at higher natural
history risk. "Unknown" may be appropriate to this
categorization.
B.7.7. Hemorrhage Location
B.7.8. Hemorrhage Size
Comment
The hemorrhage size is recorded in
millimeters using the same guidelines as for BAVM size. From these
dimensions, a calculation can be made to estimate intraparenchymal
hemorrhage size in ml using the ABC/2 formula of Rashmi et
al.30
Rationale
The anatomic site of bleeding may be important for the
pathophysiologic consequences of the blood products that remain
extravascular, ie, subarachnoid; or in terms of potential for
interruption of tissue function, ie, parenchymal versus
intraventricular.
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C. Venous Drainage |
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TopAbstractIntroductionA. General DefinitionsB. Location and SizeC. Venous DrainageD. Arterial SupplyReferences |
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Comment
The writing group recognizes that descriptions of the complex venous drainage of many BAVMs may defy simple rules. A large number of systems have been proposed, especially in terms of hemorrhagic risk, but it is clear that abnormalities in venous drainage are strongly associated with hemorrhagic events.20 24 31 32 33 34 35 36
C.1. Superficial Versus Deep Venous Drainage
Comment
The definition proposed by Spetzler and
Martin1 is recommended
(Figure 5, panel A). Superficial drainage is considered present "if all the drainage from the BAVM is through the
cortical venous system. The venous pattern is considered deep if any or
all of the drainage is through deep veins (such as the internal
cerebral veins, basal veins, or precentral cerebral vein). In the
posterior fossa, only cerebellar hemispheric veins that drain directly
into the straight sinus, torcula, or transverse sinus are considered to
be superficial."1
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Rationale
Abnormalities of venous drainage directly affect the
propensity for spontaneous rupture and relate to
surgical12 37 and radiosurgical
risk.13 18
Whereas any deep venous drainage appears to increase risk for microsurgical resection,37 there is evidence that exclusively deep venous drainage may increase risk of spontaneous hemorrhage in the natural course.13 24 31 33 Therefore, identifying the separate components (deep versus superficial) may have utility in differentiating treatment versus natural history risks.
C.2. Periventricular Drainage
Comment
Sometimes termed subependymal,
periventricular venous drainage refers to venous drainage
that is distinct from other deep venous drainage into the Galenic
system; internal cerebral vein; basal vein of Rosenthal; superficial
cerebellar veins (Figure 5, panel B). In the rare instance where
periventricular draining veins egress into a superficial
sinus, this should still be a "yes" response.
Rationale
Periventricular drainage may
represent a lower risk in the natural history if bleeding can
egress into the ventricular system. It may, however, also
increase risk if these structures are more fragile or under higher
pressure.20 Presence of
periventricular drainage may indicate increased surgical
risk because these lesions may be larger and transcortical.
Periventricular location of the nidus may also be important
for natural history.31 33
C.3. Number of Draining Veins Leaving Nidus
Comment
The number of discrete venous channels that actually
leave the nidus should be reported (Figure 5, panel C).
Rationale
The number of draining veins appears to be inversely
related to venous pressure.20 32 34 38 39 40
C.4. Number of Veins Reaching Sinus
Comment
The number of draining veins are counted which reach
any of the following sinuses: superior sagittal, straight, transverse,
sigmoid, cavernous, superior petrosal or inferior petrosal
(Figure 5, panel C). Veins draining into any parasitized
sinuses such as occipital or marginal sinuses may be included in this
count.
Rationale
Counting the number of veins reaching any venous sinus
is a method to simplify the complex venous anatomy, and appears
to be correlated with hemorrhagic risk,20 similar to "number
of draining veins leaving nidus."
C.5. Venous Stenosis/Occlusion
Comment
Venous stenosis/occlusion is defined as
narrowing of any draining vein outflow pathway in two angiographic
views (Figure 5, panel D). The venous outflow tract immediately
proximal is used as the denominator in this relative index. If there is
nonuniformity of venous caliber, the draining vein’s diameter at the
exit from the nidus should be used. Percent stenosis is
therefore equal to the narrowest diameter of the vein (measured in
millimeters) divided by the largest diameter of the vein just proximal
to the stenosis (measured in
millimeters).
Rationale
Venous stenosis/occlusion appear to be associated with hemorrhagic presentation.41
C.6. Venous Ectasia (Dilatation)
Comment
Because "venous stenosis/occlusion" may
miss various patterns of venous caliber change, an additional relative
index is proposed
(Figure 5, panel D). "Venous ectasia" is any change in
venous caliber in the venous runoff or drainage from the BAVM, with a
>2-fold caliber change in any draining venous
channel.
Rationale
Venous ectasia may be associated with hemorrhagic
presentation.31 This general marker of venous irregularity will identify lesions that might be difficult to quantitate in terms of stenosis because of nonuniformity of draining vein caliber.
C.7. Venous Reflux
Comment
Reversal of flow in any venous outflow pathway in a
direction other than the normal pathway, which is defined as toward the
closest venous sinus (Figure 5, panel E).
Rationale
Venous Reflux may be associated with hemorrhagic
presentation.31
C.8. Sinus Thrombosis/Occlusion
Comment
Defined as a filling defect in a dural venous sinus
that could be thrombosis or occlusion and excludes arachnoid
granulations.
Rationale
Abnormalities in venous drainage appear to be
associated with hemorrhagic presentation and venous hypertension.
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D. Arterial Supply |
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TopAbstractIntroductionA. General DefinitionsB. Location and SizeC. Venous DrainageD. Arterial SupplyReferences |
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D.1 Feeding Arteries
Comment
A feeding vessel is defined as an arterial structure that angiographically demonstrates a contribution of flow (as evidenced by contrast opacification) to the arteriovenous shunt. Feeding arteries may be parent arteries that give rise to vessels that directly or indirectly supply flow to the BAVM. Multiple vessels are possible. Penetrators (perforators) refer to vessels that are normally end arteries; branches refer to other named or unnamed branches that normally go on to divide further.
Rationale
The arterial anatomy may be
associated with several aspects of natural history risk (many
territories suggesting recruitment of new inflow and low
pressure)25 or increased
treatment risk (involvement of deep perforating arteries that increase
risk of microsurgical resection).
D.2 Arterial Aneurysms
Comment
Flow-related is
an operational term describing an aneurysm which lies on an
pathway that carries nonnutritive blood flow (contrast) supplying the
BAVM shunt
(Figure 6, panels A and B). Aneurysms are
defined as saccular luminal dilatations of the parent feeding vessel.
"Nidal" is defined as contiguous with the vascular mass included in
the BAVM size measurement
(Figure 1), but the aneurysm may extend past the
margin of the actual measured BAVM mass
(Figure 6, panel C).
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For location, "proximal" versus "distal" refers to the circle of Willis. "Proximal" aneurysms would be located on the vessel or branch points of the circle of Willis or proximal to it, and include the internal carotid arteries; anterior and posterior communicating arteries; first portions of the anterior (A1) or posterior cerebral (P1) arteries; basilar arteries; or vertebral arteries (panel C). "Distal" refers to other more distal locations that are beyond the circle of Willis (panel D).
D.2.1. Number of Arterial Aneurysms
D.2.2. Arterial Aneurysms Location
Rationale
Arterial aneurysms are recognized
to have the propensity to rupture and bleed, including those associated
with BAVMs.21 25 33 42
There is some controversy whether the initial presentation
or rebleeding rate is affected by the presence of
aneurysms42 and
there is still an evolving understanding of unruptured
aneurysms.43 The
main distinction is between arteries which are
presumably exposed to higher
flow rates than normal (termed
flow-related aneurysms)
and those that are
not.
D.2.3. Arterial Aneurysms Hemorrhagic History
Comment
Has the patient has ever bled from any of the
aneurysms that could be localized as a source of
hemorrhage other than the BAVM?
Rationale
Although with distal and nidal aneurysms
it may not be possible to differentiate the source of BAVM versus
aneurysmal hemorrhage, it may be possible with
locations that are more distant from the nidus (more proximal or in a
different, neighboring circulation). This item is recommended to be
recorded because it addresses the question of whether a BAVM that
presents with an aneurysmal subarachnoid
hemorrhage is incidental or not. If the aneurysm is
intranidal, then most would agree that it would
NOT be incidental. If the
aneurysm was in the contralateral hemisphere, one might
consider the discovery of the BAVM to be incidental. The closer a
symptomatic aneurysm is to the BAVM nidus, the less
clear this "incidental" versus "hemorrhagic" distinction
becomes. Hence, by recording this information, future studies
might determine more precisely how the natural history of associated
aneurysmal bleeds is related to the natural history of BAVM
bleeds.
D.2.4. Arterial Aneurysms Hemorrhagic Date
Comment
If the patient has ever bled from any of the
aneurysms, give first and subsequent
dates.
D.3 Number of Vessels to Be Embolized
Comment
This is a priori assessment of how many
arterial pedicles will be cannulated and then
embolized
(Figure 7).
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Rationale
The type of endovascular therapy may vary with the
embolic agent and may influence the choice of number of vessels to be
treated. Nevertheless, risk of treatment-related complications may be
related to the degree of instrumentation and navigation of the cerebral
vasculature. By estimating the number of feeding vessels to be treated,
some prospective index of procedure-related risk may be
obtained.
D.4 Moyamoya-Type Changes
Not exclusively moymoya disease, rather this is a
pattern of angiographic changes that suggest occlusion or near-complete
stenosis of associated feeding arteries. This pattern includes
recruitment of collateral supply to compensate for the occluded or
stenotic arterial
segment.44 A more precise
but unwieldy nomenclature would be "collateral small vessel
recruitment due to distal feeding vessel arteriopathy with
stenosis or occlusion."
Rationale
This angiographic pattern suggests a unique vascular
biologic response that might be intuitively associated with a differing
type of clinical behavior.
D.5 Pial-to-Pial Collateralization
Comment
Recruitment of neighboring pial-to-pial collaterals not
considered part of the BAVM nidus (target for radiosurgery, resection
or embolization;
Figure 8). This may be either between or within long
circumferential territories. For example, it might be collateral
recruitment at a borderzone between branches of the middle cerebral
artery (MCA) and posterior cerebral artery (PCA) or between adjacent
territories of one artery, such as between parietal branches of
MCA.
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Rationale
Pial-to-pial collateralization is associated with
decreased pressure in feeding
arteries,45 and there is
evidence that size and pressure are
related.22 24 The
distinction is made for "between territories" and "within
territories" because it may be related to the degree of pressure
reduction in the nidus and, for example, may be an indirect indicator
of hemorrhagic risk.20
D.6 Intravascular Pressure Measurements
Comment
Some groups have used intravascular cerebral pressure
measurements for both research and clinical purposes. Pressure
measurements, however, should not be construed as a standard of
clinical care.
If pressures are measured in a particular practice or protocol, it is probably most meaningfully obtained during the patient’s initial superselective angiography session, the first embolization prior to the injection of any embolic material or during surgery if no previous embolization has been performed. In this way the physiological measurement will be more indicative of the natural history before any treatment effect may interact with the hemodynamic state of the BAVM.
Pressure measurement has been described for both intraoperative direct puncture of vessels22 35 46 and endovascular measurement through microcatheters.20 47 48 The reader is referred to these references for technical details but a few points can be mentioned in brief.
The pressure transducer system should be zeroed and
calibrated taking into account any difference between the height of the
head above the right
atrium.46 This is primarily
an issue for microcatheter rather than direct needle punctures. For
example, during transfemoral angiography, a calibration pressure can be
obtained as the microcatheter is passed through the coaxial or guiding
catheter in the neck
(Figure 9, panel A). Simultaneous pressures
can be recorded with the tip of the microcatheter visualized
approximately 1 cm past the orifice of the guiding catheter. This
should give equivalent pressures in both the guiding catheter and
microcatheter, thus verifying the integrity of the transducer
system.
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Feeding artery pressure can be measured at a point distal to which there are no nutritive vessels (panel B). For example, this might be the point at which embolic material would be injected. Free flow of contrast should indicate that the catheter tip is not wedged. Pressures are recorded in millimeters of mercury, relative to the right atrium as the zero level for atmospheric pressure.
Rationale
Increased feeding artery pressure has been associated
with hemorrhagic
presentation.20 22 24 35
If and when it is validated as a predictor of
future hemorrhagic risk,
intravascular pressure measurement may be an attractive variable to
use as a risk factor because, like BAVM size, it is theoretically
obtainable in all patients as a continuous value, making generation of
statistical models more effective.
There are several unresolved issues related to pressure measurements that suggest their use primarily for research purposes, rather than patient-specific clinical use. For example, if there are several measurements possible, which pressure should be reported? These will have to be worked out in future studies. Most previous studies that have examined hemorrhagic risk and pressure measurement have looked at either the lowest, initial pretreatment pressure from endovascular procedures20 24 or the first and presumably only intraoperative arterial puncture that was available.22 35
A surrogate for intravascular pressure, intravascular contrast transit time, has also been described.49 Transit-time methods, for both contrast angiography50 and MR techniques, may offer a means of estimating distal cerebral pressures without the need for intracranial catheter navigation. Further validation of such noninvasive methodologies may make intravascular pressure estimation more widely applicable.
Summary
We wish to emphasize that these definitions span a
broad range of possibly
relevant clinical and radiographic parameters
to be considered in research studies. We do
not endorse these guidelines as
"minimal criteria" for all reporting of research data related to
BAVMs. For example, some of the angioarchitectural features described
herein are based on reasoned speculation. Additionally, some features
may be relevant to a given research question, but not relevant to
others.
These operational definitions have been chosen by consensus of the writing group for the sake of consistency in reporting clinical trials and observational studies. They are intended for use in research protocols. These definitions can allow different groups to publish results that are directly comparable.
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Acknowledgments |
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This work was supported in part by PHS grant RO1 NS34949. Nancy J. Quinine, RN, and John Bennett assisted with technical aspects of the manuscript preparation. Illustrations were kindly provided by Adel Malek, MD, PhD.
The writing group consisted of the following contributors: Richard P. Atkinson, MD (Mercy Healthcare, Sacramento, Calif); Issam A. Awad, MD (Yale University School of Medicine, New Haven, Conn); H. Hunt Batjer, MD (Northwestern University, Chicago, Ill); Christopher F. Dowd, MD (University of California, San Francisco); Anthony Furlan, MD (The Cleveland Clinic [Ohio]); Steven L. Giannotta, MD (University of Southern California, Los Angeles, Calif); Camilo R. Gomez, MD (University of Alabama, Birmingham); Daryl Gress, MD (University of California, San Francisco); George Hademenos, PhD (The American Heart Association National Center, Dallas, Tex); Van Halbach, MD (University of California, San Francisco); J. Claude Hemphill, MD (University of California, San Francisco); Randall T. Higashida, MD (University of California, San Francisco); L. Nelson Hopkins, MD (State University of New York at Buffalo); Michael B. Horowitz, MD (University of Pittsburgh [Pa]); S. Claiborne Johnston, MD, MPH (University of California, San Francisco); Michael T. Lawton, MD (University of California, San Francisco); Michael W. McDermott, MD (University of California, San Francisco); Adel M. Malek, MD, PhD (Brigham and Women’s Hospital, Boston, Mass); J.P. Mohr, MD (Columbia University, New York, NY); Adnan I. Qureshi, MD (State University of New York at Buffalo); Howard Riina, MD (Barrow Neurological Institute, Phoenix, Ariz); Wade S. Smith, MD, PhD (University of California, San Francisco); John Pile-Spellman, MD (Columbia University, New York, NY); Robert F. Spetzler, MD, F.A.C.S. (Barrow Neurological Institute, Phoenix, Ariz); Thomas A. Tomsick, MD (University of Cincinnati [Ohio]); and William L. Young, MD (University of California, San Francisco).
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Footnotes |
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A complete list of the members of the joint writing group appears in the Appendix.
Received December 15, 2000; revision received March 30, 2001; accepted April 2, 2001.
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References |
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TopAbstractIntroductionA. General DefinitionsB. Location and SizeC. Venous DrainageD. Arterial SupplyReferences |
|---|
1. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 1986;65:476–483.[Medline] [Order article via Infotrieve]
2.
Ogilvy CS,
Stieg PE, Awad IA, Brown RD Jr, Kondziolka D, Rosenwasser RH, Young WL,
Hademenos G. Recommendations for the management of intracranial
arteriovenous malformations: a statement for health care professionals
from a special writing group of the Stroke Council, American Stroke
Association. Stroke.. 2001;32:1458–1471.
3. Flickinger JC, Kondziolka D, Lunsford LD, Kassam A, Phuong LK, Liscak R, Pollock B. Development of a model to predict permanent symptomatic postradiosurgery injury for arteriovenous malformation patients. Arteriovenous Malformation Radiosurgery Study Group. Int J Radiat Oncol Biol Phys. 2000;46:1143–1148.[Medline] [Order article via Infotrieve]
4. Stapf C, Hofmeister C, Mast H, Pile-Spellman J, Young WL, Mohr JP. The feasibility of an internet web-based, international study on brain arteriovenous malformations (The AVM World Study). Stroke. 2000;31:322. Abstract.
5. Enam SA, Malik GM. Association of cerebral arteriovenous malformations and spontaneous occlusion of major feeding arteries: clinical and therapeutic implications. Neurosurgery. 1999;45:1105–1111; discussion 1111–1112.[Medline] [Order article via Infotrieve]
6. Putman CM, Chaloupka JC, Fulbright RK, Awad IA, White RI Jr, Fayad PB. Exceptional multiplicity of cerebral arteriovenous malformations associated with hereditary hemorrhagic telangiectasia (Osler-Weber-Rendu syndrome). AJNR Am J Neuroradiol. 1996;17:1733–1742.[Abstract]
7. Chiang V, Awad I, Berenstein A, Scott M, Spetzler R, Alexander MJ. Neonatal galenic arteriovenous malformation [clinical conference]. Neurosurgery. 1999;44:847–54.[Medline] [Order article via Infotrieve]
8. McCormick WF. Pathology of vascular malformations of the brain. In: Wilson CB, Stein BM, eds. Intracranial Arteriovenous Malformations. Baltimore, Md: Williams & Wilkins; 1984:44–63.
9. Jafar JJ, Awad IA, Robert H, Rosenwasser E. Vascular Malformations of the Central Nervous System. New York, NY: Lippincott Williams & Wilkins; 1999:1–540.
10. Awad IA, Robinson JR, Mohanty S, Estes ML. Mixed vascular malformations of the brain: clinical and pathogenetic considerations. Neurosurgery. 1993;33:179–188.[Medline] [Order article via Infotrieve]
11. Tomlinson FH, Houser OW, Scheithauer BW, Sundt TM Jr, Okazaki H, Parisi JE. Angiographically occult vascular malformations: a correlative study of features on magnetic resonance imaging and histological examination. Neurosurgery. 1994;34:792–9; discussion 799–800.[Medline] [Order article via Infotrieve]
12. Stein BM, Kader A. Intracranial arteriovenous malformations [review]. Clin Neurosurg. 1992;39:76–113.[Medline] [Order article via Infotrieve]
13.
Pollock BE,
Flickinger JC, Lunsford LD, Bissonette DJ, Kondziolka D. Factors that
predict the bleeding risk of cerebral arteriovenous malformations.
Stroke. 1996;27:1–6.
14. Mast H, Young WL, Koennecke H-C, Sciacca RR, Osipov A, Pile-Spellman J, Hacein-Bey L, Duong H, Stein BM, Mohr JP. Risk of spontaneous haemorrhage after diagnosis of cerebral arteriovenous malformation. Lancet. 1997;350:1065–1068.[Medline] [Order article via Infotrieve]
15. Ondra SL, Troupp H, George ED, Schwab K. The natural history of symptomatic arteriovenous malformations of the brain: a 24-year follow-up assessment. J Neurosurg. 1990;73:387–391.[Medline] [Order article via Infotrieve]
16. Singh V, Young WL, Ko NK, Sidney S, Johnston SC. Increased detection of cerebral vascular malformations in a large health maintenance organization. Ann Neurol.. 2000;48:4. Abstract.
17. Karlsson B, Lindquist C, Johansson A, Steiner L. Annual risk for the first hemorrhage from untreated cerebral arteriovenous malformations. Minim Invasive Neurosurg. 1997;40:40–46.[Medline] [Order article via Infotrieve]
18. Pollock BE, Flickinger JC, Lunsford LD, Maitz A, Kondziolka D. Factors associated with successful arteriovenous malformation radiosurgery. Neurosurgery. 1998;42:1239–1244; discussion 1244–1247.[Medline] [Order article via Infotrieve]
19. Pasqualin A, Barone G, Cioffi F, Rosta L, Scienza R, Pian RD. The relevance of anatomic and hemodynamic factors to a classification of cerebral arteriovenous malformations. Neurosurgery. 1991;28:370–379.[Medline] [Order article via Infotrieve]
20.
Duong
DH, Young WL, Vang MC, Sciacca RR, Mast H, Koennecke H-C, Hartmann A,
Joshi S, Mohr JP, Pile-Spellman J. Feeding artery pressure and venous
drainage pattern are primary determinants of hemorrhage from
cerebral arteriovenous malformations.
Stroke. 1998;29:1167–1176.
21. Graf CJ, Perret GE, Torner JC. Bleeding from cerebral arteriovenous malformations as part of their natural history. J Neurosurg. 1983;58:331–337.[Medline] [Order article via Infotrieve]
22. Spetzler RF, Hargraves RW, McCormick PW, Zabramski JM, Flom RA, Zimmerman RS. Relationship of perfusion pressure and size to risk of hemorrhage from arteriovenous malformations [comments in J Neurosurg.. 1993;78:156–158 and J Neurosurg. 1993;78:850–853]. J Neurosurg. 1992;76:918–923.[Medline] [Order article via Infotrieve]
23. Langer DJ, Lasner TM, Hurst RW, Flamm ES, Zager EL, King JT Jr. Hypertension, small size, and deep venous drainage are associated with risk of hemorrhagic presentation of cerebral arteriovenous malformations. Neurosurgery. 1998;42:481–486; discussion 487–489.[Medline] [Order article via Infotrieve]
24. Kader A, Young WL, Pile-Spellman J, Mast H, Sciacca RR, Mohr JP, Stein BM, The Columbia University AVM Study Project. The influence of hemodynamic and anatomic factors on hemorrhage from cerebral arteriovenous malformations. Neurosurgery.. 1994;34:801–807; discussion 807–808.[Medline] [Order article via Infotrieve]
25. Turjman F, Massoud TF, Vinuela F, Sayre JW, Guglielmi G, Duckwiler G. Correlation of the angioarchitectural features of cerebral arteriovenous malformations with clinical presentation of hemorrhage. Neurosurgery. 1995;37:856–862.[Medline] [Order article via Infotrieve]
26. Sasaki T, Kurita H, Saito I, Kawamoto S, Nemoto S, Terahara A, Kirino T, Takakura K. Arteriovenous malformations in the basal ganglia and thalamus: management and results in 101 cases. J Neurosurg. 1998;88:285–292.[Medline] [Order article via Infotrieve]
27.
Lazar RM,
Marshall RS, Pile-Spellman J, Hacein-Bey L, Young WL, Mohr JP, Stein
BM. Anterior translocation of language in patients with left cerebral
arteriovenous malformations.
Neurology. 1997;49:802–808.
28. Maldjian J, Atlas SW, Howard RS, II, Greenstein E, Alsop D, Detre JA, Listerud J, D’Esposito M, Flamm ES. Functional magnetic resonance imaging of regional brain activity in patients with intracerebral arteriovenous malformations before surgical or endovascular therapy. J Neurosurg. 1996;84:477–483.[Medline] [Order article via Infotrieve]
29.
Schlosser
MJ, McCarthy G, Fulbright RK, Gore JC, Awad IA. Cerebral vascular
malformations adjacent to sensorimotor and visual cortex: functional
magnetic resonance imaging studies before and after therapeutic
intervention. Stroke. 1997;28:1130–1137.
30.
Kothari RU,
Brott T, Broderick JP, Barsan WG, Sauerbeck LR, Zuccarello M,
Khoury J. The ABCs of measuring intracerebral
hemorrhage volumes. Stroke. 1996;27:1304–1305.
31. Nataf E, Meder JF, Roux FX, Blustajn J, Merienne L, Merland JJ, Schlienger M, Chodkiewicz JP. Angioarchitecture associated with haemorrhage in cerebral arteriovenous malformations: a prognostic statistical model. Neuroradiology. 1997;39:52–58.[Medline] [Order article via Infotrieve]
32. Miyasaka Y, Kurata A, Tokiwa K, Tanaka R, Yada K, Ohwada T. Draining vein pressure increases and hemorrhage in patients with arteriovenous malformation. Stroke. 1994;25:504–507.[Abstract]
33.
Marks MP,
Lane B, Steinberg GK, Chang PJ. Hemorrhage in
intracerebral arteriovenous malformations: angiographic
determinants. Radiology. 1990;176:807–813.
34. Miyasaka Y, Yada K, Ohwada T, Kitahara T, Kurata A, Irikura K. An analysis of the venous drainage system as a factor in hemorrhage from arteriovenous malformations [comments in J Neurosurg.. 1992;77:652–654 and J Neurosurg. 1992;77:822–823]. J Neurosurg. 1992;76:239–243.
35. Miyasaka Y, Kurata A, Irikura K, Tanaka R, Fujii K. The influence of vascular pressure and angiographic characteristics on haemorrhage from arteriovenous malformations. Acta Neurochir (Wien). 2000;142:39–43.[Medline] [Order article via Infotrieve]
36. Mansmann U, Meisel J, Brock M, Rodesch G, Alvarez H, Lasjaunias P. Factors associated with intracranial hemorrhage in cases of cerebral arteriovenous malformation. Neurosurgery.. 2000;46:272–279; discussion 279–281.[Medline] [Order article via Infotrieve]
37. Hamilton MG, Spetzler RF. The prospective application of a grading system for arteriovenous malformations. Neurosurgery.. 1994;34:2–6; discussion 6–7.[Medline] [Order article via Infotrieve]
38. Miyasaka Y, Yada K, Kurata A, Tokiwa K, Irikura K, Tanaka R, Ohwada T, Kitahara T. Correlation between intravascular pressure and risk of hemorrhage due to arteriovenous malformations. Surg Neurol. 1993;39:370–373.[Medline] [Order article via Infotrieve]
39. Hollerhage H-G. Comment on "An analysis of the venous drainage system as a factor in hemorrhage from arteriovenous malformations." J Neurosurg. 1992;77:652–654.
40. Hollerhage H-G. Venous drainage system and risk of hemorrhage from AVMs [letter, with response, on "An analysis of the venous drainage system as a factor in hemorrhage from arteriovenous malformations." J Neurosurg.. 1992;76:239–242.] J Neurosurg. 1992;77:651–654.[Medline] [Order article via Infotrieve]
41. Vinuela F, Nombela L, Roach MR, Fox AJ, Pelz DM. Stenotic and occlusive disease of the venous drainage system of deep brain AVMs. J Neurosurg. 1985;63:180–184.[Medline] [Order article via Infotrieve]
42. Meisel HJ, Mansmann U, Alvarez H, Rodesch G, Brock M, Lasjaunias P. Cerebral arteriovenous malformations and associated aneurysms: analysis of 305 cases from a series of 662 patients. Neurosurgery. 2000;46:793–800; discussion 800–802.[Medline] [Order article via Infotrieve]
43.
ISUIA
Investigators. Unruptured intracranial aneurysms: risk of
rupture and risks of surgical intervention [see comments] [published
erratum appears in N Engl J
Med. 1999;340:744]. N
Engl J Med.
1998;339:1725–1733.
44. Regli L, Murphy KJ, Tribolet ND, Uske A, Rufenacht DA, Guimarens L, Numaguchi Y, Chang J. Moyamoya disease with arteriovenous malformation: an angiogenetic hypothesis. J Neurosurg. 1998;88:201A (paper #35). Abstract.
45. Norbash AM, Marks MP, Lane B. Correlation of pressure measurements with angiographic characteristics predisposing to hemorrhage and steal in cerebral arteriovenous malformations. AJNR Am J Neuroradiol. 1994;15:809–813.[Abstract]
46. Young WL, Kader A, Pile-Spellman J, Ornstein E, Stein BM, Columbia University AVM Study Project. Arteriovenous malformation draining vein physiology and determinants of transnidal pressure gradients. Neurosurgery. 1994;35:389–395; discussion 395–396.[Medline] [Order article via Infotrieve]
47. Jungreis CA, Horton JA, Hecht ST. Blood pressure changes in feeders to cerebral arteriovenous malformations during therapeutic embolization. AJNR Am J Neuroradiol. 1989;10:575–578.[Abstract]
48. Duckwiler G, Dion J, Vinuela F, Jabour B, Martin N, Bentson J. Intravascular microcatheter pressure monitoring: experimental results and early clinical evaluation. AJNR Am J Neuroradiol. 1990;11:169–175.[Abstract]
49. Norris JS, Valiante TA, Wallace MC, Willinsky RA, Montanera WJ, terBrugge KG, Tymianski M. A simple relationship between radiological arteriovenous malformation hemodynamics and clinical presentation: a prospective, blinded analysis of 31 cases. J Neurosurg. 1999;90:673–679.[Medline] [Order article via Infotrieve]
50. Wakhloo AK, Lieber BB, Rudin S, Fronckowiak MD, Mericle RA, Hopkins LN. A novel approach to flow quantification in brain arteriovenous malformations prior to enbucrilate embolization: use of insoluble contrast (Ethiodol droplet) angiography. J Neurosurg. 1998;89:395–404.[Medline] [Order article via Infotrieve]
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