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Dural Arteriovenous Shunts

A New Classification of Craniospinal Epidural Venous


Anatomical Bases and Clinical Correlations
Sasikhan Geibprasert, MD; Vitor Pereira, MD; Timo Krings, MD, PhD; Pakorn Jiarakongmun, MD;
Frederique Toulgoat, MD; Sirintara Pongpech, MD; Pierre Lasjaunias, MD, PhD

Background and Purpose—The craniospinal epidural spaces can be categorized into 3 different compartments related to
their specific drainage role of the bone and central nervous system, the ventral epidural, dorsal epidural, and lateral
epidural groups. We propose this new classification system for dural arteriovenous shunts and compare demographic,
angiographic, and clinical characteristics of dural arteriovenous shunts that develop in these 3 different locations.
Methods—Three hundred consecutive cases (159 females, 141 males; mean age: 47 years; range, 0 to 87 years) were
reviewed for patient demographics, clinical presentation, multiplicity, presence of cortical and spinal venous reflux, and
outflow restrictions and classified into the 3 mentioned groups.
Results—The ventral epidural group (n⫽150) showed a female predominance, more benign clinical presentations, lower
rate of cortical and spinal venous reflux, and no cortical and spinal venous reflux without restriction of the venous
outflow. The dorsal epidural group (n⫽67) had a lower mean age and a higher rate of multiplicity. The lateral epidural
group (n⫽63) presented later in life with a male predominance, more aggressive clinical presentations, and cortical and
spinal venous reflux without evidence of venous outflow restriction. All differences were statistically significant
(P⬍0.001).
Conclusion—Dural arteriovenous shunts predictably drain either in pial veins or craniofugally depending on the
compartment involved by the dural arteriovenous shunt. Associated conditions (outflow restrictions, high-flow shunts)
may change that draining pattern. The significant differences between the groups of the new classification support the
hypothesis of biological and/or developmental differences in each epidural region and suggest that dural arteriovenous
shunts are a heterogeneous group of diseases. (Stroke. 2008;39:2783-2794.)
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Key Words: classification 䡲 cranial dural arteriovenous fistula 䡲 epidemiology 䡲 epidural veins, clinical aspects
䡲 spinal dural arteriovenous fistula

D ural arteriovenous shunts or fistulas (DAVSs or


DAVFs) are a group of diseases that share involvement
of the epidural space and adjacent dura mater and bony
gies or classic sex dominance in some localizations were not
specifically addressed.
The basis for the new classification of DAVSs proposed in
structures. this study relies on the characteristics of venous afferent
Different classifications have been proposed for these patterns of the various epidural spaces according to the
lesions,1–3 but the most widely used are those that focus on evolution and embryological development of the venous
the presence or absence of cortical venous reflux; it is drainage of the central nervous system and surrounding
generally accepted that this angiographic finding constitutes structures (vertebra, skull base, calvarium) by which 3 dif-
the major clinical consideration regarding the natural history ferent epidural spaces can be differentiated as outlined
and, therefore, the therapeutic strategies for these lesions.4 subsequently.
Until now, the classification systems, being based on the
various topographies, arterial feeders, and the drainage pat- Developmental Considerations of the Venous
tern, have been mainly descriptive. The different role played System of the Brain, Spine, and Adjacent
by each epidural area involved, as revealed during develop- Bony Structures
ment and embryology of the venous system, were not The notochord forms within the mesoderm in the third week
considered. Issues concerning spinal versus cranial homolo- and is considered a “patterning” embryonic structure of the

Received February 5, 2008; accepted March 3, 2008.


From the Department of Radiology (S.G., P.J., S.P.), Ramathibodi Hospital, Mahidol University, Bangkok, Thailand; the Service de Neuroradiologie
Diagnostique et Thérapeutique (V.P., T.K., F.T., P.L.), Hôpital de Bicêtre, Le Kremlin-Bicêtre, Paris, France; and the Departments of Neuroradiology
and Neurosurgery (T.K.), University Hospital Aachen, Germany.
Correspondence to Timo Krings, MD, PhD, Department of Neuroradiology, University Hospital Aachen, Pauwelsstr 30, 52057 Aachen, Germany.
E-mail tkrings@ukaachen.de
© 2008 American Heart Association, Inc.
Stroke is available at http://stroke.ahajournals.org DOI: 10.1161/STROKEAHA.108.516757

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neural tube that regulates the development of the surrounding system. During development, the earliest venous outlet of the
structures (such as nerves, blood vessels, and somites). anastomotic circle corresponds to the lateromesencephalic
Among other roles, it also controls the arterial versus venous vein opening into the petrous vein and in the superior petrosal
identification of the major axial blood vessels and specifies a sinus as illustrated in the epsilon-shaped drainage in aneu-
variety of cell types in forming primitive segments. It extends rysmal malformations of the vein of Galen.12 Posteriorly, the
from the level of the sacrum to the basisphenoid and adjacent great cerebral vein (Galen vein) and anteriorly the deep
portion of the sphenoid wings; it will contribute to the future sylvian vein openings correspond to phylogenetically more
development of the vertebral bodies and bony structures recent pathways as, respectively, shown by their late or
within these regions.5 postnatal development in humans.
During the third week, angioblasts initially form small cell During development, the draining veins of the archicere-
clusters (blood islands) within the embryonic and extraem- bellum (flocculonodular and lateral recess veins) and archice-
bryonic mesoderm. Recent studies have shown that arteries rebrum (anterior cerebral, uncate, and olfactory veins) will
and veins are in part genetically determined by their endo- open into these older (previously existing) venous systems
thelial types before the blood starts to flow inside the lumen.6 (basal vein, lateromesencephalic vein, pontine vein, and
The neural tube starts to develop into the ventricular spaces medullary vein) and thereafter through the petrosal vein or
at the fourth week.7 In the same period (corresponding to medullary emissary-bridging vein to the superior petrosal
Paget’s 5-mm stage embryo), the blood traversing the capil- sinus or condyloid vein.
lary network at the surface of the brain is drained on either As the intrinsic venous system of the cortex further
side by 3 “meningeal” (leptomeningeal) venous plexuses develops with its increase in cerebral territory (volume), it
arranged craniocaudally (anterior, middle, and posterior); tends to be directed laterally to drain into the primitive
cranially, these open into a corresponding “primary head tentorial sinus.9 The embryonic “tentorial sinus” at that point
sinus” (epidural) and which will further develop by coales- is likely to represent the most cranial portion of the lateral
cence into “primitive sinuses.”8,9 epidural venous system of the spine. Subsequently, the
The development of the choroid plexus starts at Paget’s 8- Breschet sinus, superior petrosal sinus, and straight sinuses
to 11-mm stage embryo10 with venous drainage into the are also included in that group. In short, the basal vein
median prosencephalic vein, which functions as the venous anastomotic circle; its afferent veins; and its mesencephalic,
drainage route for the early immature brain and choroid cavernous, and galenic (telencephalic and diencephalic) out-
plexuses. Secondarily, it may collect the deep cerebral venous lets are the cranial homologs of the emissary-bridging veins
afferents and basal vein, thereafter becoming the great cere- of the hindbrain and spinal cord.11
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bral vein or vein of Galen. Considering the volume increase of the cerebrum and
Development of the intrinsic venous drainage of the spinal cerebellum (paleo- and neopallium) observed throughout
cord starts after closure of the neural tube. Two longitudinal phylogeny, the venous drainage will finally require additional
collector systems form in the subarachnoid space at the dorsal outlets, which will be illustrated by the appearance of new
and ventral surface of the cord, later joining the epidural dorsal pathways, like the superior sagittal (for the brain) and
space laterally through numerous emissary-bridging veins. transverse sinuses (for the cerebellum) that are not present at
Contrary to arteries, these veins are not embryologically the spinal level.
(metamerically) linked with the spinal nerves and thus do not The development of the cranial vault sinuses into the
follow a nerve root nor do they exit the subarachnoid space epidural space results from the coalescence of the leptomen-
with them. Up to 40% of them exit through a separate dural ingeal vein contribution from the central nervous system with
foramen between the spinal nerves8; thus, they should not be the osseous venous drainage. The secondary modeling into
confused with the minute radicular veins draining the roots. the adult-type sinuses is largely dependent on the growth
They may instead be named emissary-bridging veins (trans- of the skull.8,9 At the spine and skull, 2 types of bone can be
dural) to differentiate them from the so-called emissary veins distinguished, the endochondral type (cartilaginous bone–
(transosseous), which drain the intracranial venous sinuses vertebral bodies, basioccipital, basisphenoid, and the petro-
outside of the skull. mastoid bone) and the intramembranous type (membranous
The spinal venous system, being the basic one, will exhibit bone–spinous process, laminae, and cranial vault).13–15 The
homologous features at its cranial counterpart for the 3 creation of the dorsal midline-located sinuses and conflu-
cephalic vesicles. However, the volume of developing brain ences is, nevertheless, linked to the falces (cerebri and
will progressively alter the simple pattern of the spinal and cerebelli) and the tentorium cerebelli16; both are associated
spinal cord venous drainage. The emissary-bridging vein of with an epidural confluence and coalescence of the venous
the rhombencephalon is the medullary vein opening laterally vascular spaces at their bony attachment later to become the
into the condyloid vein at the level of the foramen magnum. superior sagittal sinus, medial occipital sinus, and transverse
For the mesencephalon, it is the petrous vein that drains the sinuses.17 Their role in the venous drainage of the paleo- and
middle and upper brainstem. Longitudinal pial veins anasto- neocerebrum and paleo- and neocerebellum is a recent
moses will allow significant additional cranial contributions phylogenetic acquisition; they will further evolve postnatally
from the basal vein system. At the prosencephalic level, the after regression of the medial occipital sinus and maturation
base of the brain venous circle (interbasal venous anastomotic of the jugular bulbs.
circle)11 and its outlets will represent the most cranial The sigmoid sinuses and jugular bulbs are dependent on
equivalent of the basic spinal and hindbrain pial venous the growth of the petrous bone and skull base as they collect
Geibprasert et al Dural Arteriovenous Shunts 2785

Figure 1. Location of the 3 groups of DAVSs of the new classification in relation to the bony structures. The blue area depicts the ven-
tral epidural group that includes the basioccipital bone, the petrous pyramid, the basisphenoid with its adjacent sphenoid wings, and
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their related dural structures. The orange area relates to the dorsal epidural group, which includes the superior sagittal sinus (SSS), tor-
cular, transverse sinus, medial occipital sinus, and posterior marginal sinus. The green area relates to the lateral epidural group. Intra-
cranial locations are DAVS draining into emissary-bridging veins of the brainstem and their homologs draining deep cerebral structures
such as the condyloid vein at the foramen magnum, the superior petrosal vein, the basal vein, the vein of Galen, the veins of the ante-
rior cranial fossa, and the orbit. Modified with permission from Lasjaunias P, Berenstein A, ter Brugge KG. Surgical Neuroangiography.
1. Clinical Vascular Anatomy and Variations. Berlin: Springer; 2001.

petromastoid veins and do not receive any direct afferent spongiosus bony structures and has no primary role in
from the leptomeningeal space. Thus, they are rather behav- the drainage of the central nervous system.
ing like a conduit to bring the transverse and medial occipital 2. The dorsal epidural venous space is normally poorly
sinus blood to the jugular vein. developed at the spinal level. Presence of dorsally located
The cavernous plexus at birth and the basilar venous plexus dural sinuses intracranially is therefore the major differ-
do not drain any cerebral vein either. After birth, the so-called ence between the venous systems of the brain and spine.
cavernous capture may bring the remnant of the tentorial Their formation is linked to the appearance, during
evolution, of the dural falces and tentorium and associ-
sinus or the deep sylvian vein to open into the cavernous
ated with the development of the paleo- and neopallial
plexus.12 The sigmoid sinus and cavernous and basilar plex-
structures. These sinuses result from the confluence in
uses therefore correspond to the ventrally located venous the epidural space of 2 different venous systems: the
plexus of the spine. They share large midline communications osseous system draining the cranial vault and the
as well as their unique role in draining the spongiosus parts of leptomeningeal system draining the brain.
the related bones. Because the cranial sutures serve as 3. The veins draining the central nervous system (both
intramembranous growth sites,18 the evolution of the dorsal spinal and cranial) are not related to the peripheral
dural sinuses closely follows development of the adjacent nerves, as are the arteries; these “emissary-bridging
sutures. veins” join the lateral epidural venous spaces as con-
In summary, 3 main observations of the venous develop- necting drainage system. This leptomeningeal venous
ment of the brain and spinal cord during embryology there- drainage has no direct confluent communication with
fore contribute to the generation of the new classification: the ventral and dorsal epidural venous plexuses, which
drain the skull and spine.
1. The venous system of the notochord and corresponding
sclerotome extends from the basisphenoid (cavernous Although the epidural space changes its configuration,
plexus) to the sacrum and gives rise to the ventral from the spinal to the intracranial regions at the level of
epidural drainage group. It collects the blood from magnum foramen, it keeps the same analogous characteris-
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Figure 2. Spinal VE DAVSs (A). Lateral sacral artery angiogram. Anteroposterior view reveals spinal VE DAVSs at the sacrum (B) for-
merly known as “epidural arteriovenous fistula.” Venous drainage is related to the bone and therefore typically drains through the epi-
dural plexus of the vertebral body without perimedullary reflux.

tics. All 3 epidural venous spaces remain compartmented and system (Figure 1): the ventral epidural (VE) or
converge secondarily to join the jugular, azygos, lumbar, or osteo(cartilaginous)-epidural group, the dorsal epidural (DE)
sacral, paraspinal venous collectors. We suggest that DAVSs or osteo(membranous)-epidural group, and the lateral epi-
in these 3 different areas will drain according to the specific dural (LE) or leptomeningeal– epidural group. Based on these
role of the venous system of each region, unless there are spaces, DAVSs are therefore classified into the following 3
associated conditions such as constraint placed on the venous groups.
outlet or high-flow arteriovenous shunts. These venous outlet
restrictions (ie, occlusion or stenosis) can be either adjacent to Ventral Epidural Shunts
the shunting area, most commonly from thrombosis rather (osteo[cartilaginous]-epidural)
than endothelial proliferation, and/or remote from the shunt Dural arteriovenous shunts in these regions involve mainly
such as seen in jugular bulb dysmaturation in pediatric the epidural space and are in direct contact with the adjacent
patients. osseous structures that they may invade or recruit the blood
supply from (Figures 2 and 3). The venous afferents of these
New Classification regions are closely related to the bony structures and they
As pointed out previously, there are 3 venous subgroups drain outside the bony limits, thus resulting in no subarach-
according to the relationship of the epidural venous spaces noid (spinal or cortical) venous reflux (CVR). However,
with the afferent veins from the bone and central nervous some factors may precipitate development of CVR in these
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Figure 3. A, Internal carotid artery and (B) external carotid artery angiograms in lateral views reveal cranial VE DAVSs at the cavernous
sinus in 2 different patients. Venous drainage is related to the bone at the skull base and therefore no CVR occurs as seen in the first
patient (A) unless there is associated outflow restriction (B), ie, thrombosis of the jugular bulb in the second patient (*) causing severe
CVR through the superficial middle cerebral vein.

regions such as thrombosis within the epidural space sur- epidural sinus, distal restriction of the sinus opening will
rounding, remote, or distal to the shunt. This will produce rapidly produce CVR. In this group, the following DAVS
reflux in the lateral epidural space as seen in rare cases of locations are encountered: “dorsal spinal epidural DAVS,”
ventral epidural spinal shunts with perimedullary venous marginal sinus (dorsal portion), medial occipital sinus, torcu-
reflux.19,20 CVR can also be encountered in high-flow shunts lar, transverse and accessory epidural sinuses, and superior
forcing the emissary-bridging vein opening after reflux in the sagittal sinus.
lateral epidural space.21 In this group, the following locations
are encountered: “vertebral body,” basioccipital, sigmoid Lateral Epidural Shunts
sinus, petrous pyramid, basisphenoid and adjacent sphenoid At the spinal level, these shunts correspond to the typical
wings, and related dural structures. spinal DAVFs and are located lateral where the pial emissary
bridging vein pierces the dura (Figures 6 and 7). Intracranial
Dorsal Epidural Shunts locations include DAVS draining into emissary-bridging
(osteo[membranous]-epidural) veins of the brainstem and their homologs draining deep
At the spinal level, they are exceptional and clinically present cerebral structures. The drainage is always directed to the
with epidural hematoma (Figures 4 and 5). The venous cortical or perimedullary veins; therefore, the DAVS devel-
pressure within the dural sinuses is usually low, thus ante- oping there are always considered to be aggressive.22–24 In
grade, craniofugal flow of the shunts is normally observed. this group, the following locations are encountered: spinal
CVR may occur after associated venous outflow restriction, dural arteriovenous shunts, marginal sinus (lateral portion-
or with high-flow shunts; in case of variations of the venous foramen magnum) with the emissary-bridging vein to the
opening into this system such as presence of an accessory condyloid vein, falcotentorial (vein of Galen), petrosal and
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Figure 4. Spinal DE DAVSs (A). Reconstructed CT angiography (B) and right cervical artery angiogram in anteroposterior (C) and lateral
(D) views reveal a spinal DE DAVS at the cervical level. Note the relationship of the posterior epidural space with the lamina and spi-
nous process (*). Spinal DE shunts are uncommon and lesions within this space often present with spontaneous epidural hematomas.

basitentorial, Breschet sinus, paracavernous region (embryonic Bangkok, Thailand, during July 1998 to December 2006 and Bicêtre
tentorial sinus remnants), intraorbital shunts, and lamina Hospital, Paris, France, during September 1992 to December 2006)
for patient demographics, clinical symptoms, shunt localization,
cribriformis.
multiplicity, presence of CVR, and outflow modifications (stenosis/
The goal of our study was to compare in 300 consecutive occlusion). The study was approved by the local ethics committees
patients the demographic, angiographic, and clinical aspects of of both hospitals.
DAVSs that develop in these 3 different epidural spaces and to The clinical symptoms were separated into 2 groups, benign and
assess whether they truly present according to the predicted role aggressive.25 The benign group consists of incidental diagnosis,
nonspecific headaches, cranial nerve deficits, chemosis/proptosis,
of each epidural space in the venous drainage of the central
midline bruit, mass lesions, and cardiac insufficiency. Aggressive
nervous system and adjacent bony structures. Although the latter symptoms included seizures, intracranial hemorrhage, motor or
would confirm the validity of the classification system, the sensory deficits, visual field defects, aphasia, global neurological
former may demonstrate that the 3 different DAVSs also deficits (dementia, delayed psychomotor development, macrocra-
constitute separate clinical entities with possible different age nia), and other nonhemorrhagic neurological deficits such as
incontinence.
and sex distributions and pathomechanisms.
On angiographic terms, benign and aggressive lesions were
defined by absence or presence of CVR, respectively,26 and were
Materials and Methods grouped also using the classification systems of Borden2 and
This is a retrospective review of 300 consecutive patients, 150 Cognard.3 Borden 1 (sinus drainage only), Cognard I (antegrade
patients each from 2 different institutions (Ramathibodi Hospital, sinus drainage) and IIa (antegrade and retrograde sinus drainage)
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Figure 5. External carotid artery angiograms in lateral views in 2 patients reveal cranial DE DAVSs at the superior sagittal sinus without
(A) and with (B) thrombosis. Drainage is mainly outside the cranial cavity due to relatively low pressure of the dural sinuses and jugular
bulb unless there is a high flow shunt (A) or there is restriction of the venous system (B). Under these circumstances, CVR into the
frontal cortical veins (*) and frontoparietal cortical veins (arrows) are demonstrated.

were considered as “benign” DAVSs, whereas all the higher grades (50%) who had lesions classified to the VE group, 67 patients
(which have cortical and spinal drainage with or without sinus (22,3%) in the DE group, and 63 patients (21%) in the LE
drainage) were grouped as “aggressive” DAVSs.27
group. There were 20 (6.7%) patients with multiplicity of
Venous outflow restrictions (stenosis/occlusion) were defined as
adjacent to the shunt, remote from it, or both (mixed). In addition, we lesions: 16 had both a VE and a distant DE DAVF, one had
evaluated whether the restriction occurred proximal or distal to the VE ⫹ LE types, and 3 patients had DE ⫹ LE types. When
shunt or both. The cavernous sinus lesions were excluded from this calculating the statistics to evaluate the differences for each
item, because nonvisualization of the outflow pathways could mean of the 3 groups (VE, DE, LE), the patients having multiplicity
either thrombosis or compartmentalization of the cavernous sinus.
However, if there was stenosis or occlusion of the venous system of lesions were excluded. Refer to supplemental Table I for
elsewhere, they were added and classified as a remote type. The details of the Borden and Cognard classification and presence
spinal lesions were also excluded because nonvisualization of the of CVR.
draining spinal cord veins is part of the diagnosis of this location and
reflects the spinal cord venous congestion leading to neurological
symptoms.28 In addition, thrombosis or fibrosis of pial emissary-
Male versus Female
bridging veins of the cord occur with normal aging.8 There was a female predominance in patients having VE
The DAVSs were classified into the 3 groups of the new lesions (117 of 167 [70%]; P⬍0.001) and a strong male
classification. Crosstabulations with the sex, age groups, clinical predominance in patients with LE-type lesions (54 of 67
symptoms, presence of CVR, and types of venous outflow modifi- [81%]; P⬍0.001). There was no definite sex predominance
cations were performed.
Statistical significance was calculated for each group using ␹2 and
(female:male⫽41:46; P⫽0.225) for the DE lesions.
one-way analysis of variance tests.
Age
Results The mean consultation ages of patients with only VE, DE,
Of the 300 patients included in this article, the general patient and LE lesions were 51, 28, and 56 years, respectively. The
data are summarized in Table 1. There were 150 patients mean age in the DE group was significantly lower than the
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Figure 6. Spinal LE DAVSs (A). T8 intercostal artery angiogram in anteroposterior view reveals a spinal LE DAVSs at the thoracic level,
also known as a “typical spinal DAVF” (B) supplied by a radiculomeningeal artery draining directly into a pial emissary bridging vein and
subsequently retrogradely into perimedullary veins (asterisk).

VE and LE lesions (P⬍0.001) with 31 of 67 (46.3%) being in lesions are dominant in terms of risks for the patient, whereas
the pediatric population. Patients with LE-type lesions also in only 7 of 16 patients who had both VE and DE shunts,
presented later in life with no patients presenting before the aggressive clinical symptoms were present.
age of 30.
Multiplicity
Benign Versus Aggressive Clinical Symptoms The DE shunts had a higher rate of multiple lesions, 31 of 86
In 150 patients of the VE group, 139 (92%) had benign (36%), whereas only 20 of 167 (12%) shunts of the VE type
clinical symptoms, whereas in the LE group, 54 of 63 (86%) and 6 of 67 (9%) shunts of the LE type had multiple lesions
patients had aggressive clinical symptoms (P⬍0.001). There (P⬍0.001).
was a slight trend to more aggressive symptoms in the DE
group (42 of 67 [63%]) without statistical significance at 99% Comparison With Cognard/Borden
CI (P⫽0.038). Concerning the patients with multiplicity of Because the LE lesions are located within the laterally located
DAVS, whenever a LE lesion was present in these patients, epidural space, which drains primarily into the cortical or
the symptoms were aggressive, demonstrating that these spinal veins, all of them were classified as aggressive and,
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Figure 7. Internal carotid artery angiogram (A) and occipital artery angiogram (B) reveal cranial LE DAVSs in 2 patients at the anterior
cranial fossa (A) and tentorium (B), respectively. In these locations, CVR is always present. Branches of the ophthalmic artery (A) supply
the ethmoidal LE DAVSs with drainage into ectatic venous pouches of the frontal cortical vein before entering the superior sagittal
sinus (arrows). Stylomastoid branches of the occipital artery (B) supply the tentorial LE DAVSs and drain into the basal vein group,
which joins the vein of Galen (arrowheads).

subsequently, had classifications of Types III, IV, and V (64%) of the only DE shunts and all (100%) of the LE shunts
according to Cognard and Type 3 according to Borden. If (P⬍0.001). In the multiple type of VE⫹DE lesions, CVR
multiplicity of shunts was present, the lateral epidural loca- was present in 13 of 16 (81%) cases.
tion always determined the aggressiveness and could there-
fore be determined as the primary risk factor. Drainage Venous Outflow Restriction
pattern of the cranial VE and DE type of DAVSs was In the noncavernous VE lesions, 39 of 52 cases (75%) had
primarily through the sinuses, resulting in Types I, IIa, IIb, evidence of venous outflow restriction, which occurred sur-
and IIab according to the Cognard classification and Type 1 rounding the shunt in 30 of 39 cases (77%; P⬍0.001). Sixty
and Type 2 according to the Borden classification depending of 67 cases (90%) with only DE lesions had stenosis/
on outflow restrictions. Refer to supplemental Tables II and occlusion of the venous outflow and the majority (35 of 60
III, available online at http://stroke.ahajournals.org, for a [58%]) were of the multiple type that had thrombosis sur-
detailed comparison of the Cognard and Borden classifica- rounding and remote to the shunt location (P⬍0.001). In the
tions with the new classification scheme. 35 patients with nonspinal LE type of DAVSs, only 6 patients
(17%) had restrictions of venous outflow, being remote from
Cortical/Spinal Venous Reflux the shunt location in 4 of those (P⬍0.001).
Cortical/spinal venous reflux was less common in patients In the VE group, no cortical or spinal reflux was present
with only VE shunts, being present in only 45 of 150 (30%) when there was no modification of the venous outflow pattern
of the patients, all of the noncavernous shunts having steno- (13 of 13 [100%]). In the remaining patients in the VE group,
sis/thrombosis of the venous outflow. The percentage of CVR the venous outflow restriction usually occurred surrounding
increased in patients with DE and LE shunts, being 43 of 67 the shunt and most of the patients with this type did not have
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Table 1. General Data of the 300 Patients Table 3. Dorsal Epidural Shunts (osteo关membranous兴-epidural)
Demographics/Characteristics No. of Patients No sex predominance
Sex Lower mean age (pediatric group)
Female 159 (53%) Multiplicity
Male 141 (47%) Usually no CVR unless
Age, mean years (range) 47.2 (0–7) years Extensive thrombosis (of the mixed type, both proximal and distal)
Clinical symptoms High-flow shunts
Benign 183 (61%) Special anatomic variations; compartmentalization of the sinusal space if
full coalescence of the venous lumen does not occur
Aggressive 117 (39%)
History of procoagulatory states, sinus thrombosis 21 (7%)
Multiple shunts 57 (19%) same regions such as cavernous aneurysms.29 The characteristics
are summarized in Table 2. Cranial lesions usually present with
Adjacent 19 (6.3%)
benign clinical symptoms attributed to the low rate of CVR. In
Separate 18 (6%)
the spine, these shunts are usually asymptomatic; there have
Bilateral cavernous lesions 20 (6.7%) been only few case reports describing associated perimedullary
CVR 168 (56%) reflux causing congestive myelopathy and stimulated consider-
Venous outflow restriction (VOR) (excluded 93 129/179 (72%) ations about a possible valve-like mechanisms normally imped-
cavernous and 28 spinal lesions) ing retrograde flow from the epidural plexus to perimedullary
Type of VOR veins; however, in our opinion, it is more likely an extensive
Adjacent (surrounding) to the shunt 47 thrombosis of the normal epidural outlets that leads to retrograde
drainage to perimedullary veins as a seldom variant of spinal VE
Remote to the shunt 27
arteriovenous shunts.
Mixed (both) 49
Location of VOR Dorsal Epidural Shunts
Upstream to the shunt 11 There was no significant sex predominance. The characteris-
Distal to the shunt 68 tics are summarized in Table 3. The infantile type and dural
Both 48 sinus malformations of the pediatric DAVSs are within this
group,30,31 therefore significantly reducing the average age of
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patients compared with the other groups in which children are


CVR (27 of 30 [90%]; P⫽0.001). There was also a higher poorly represented. CVR is more frequently observed in
chance of CVR when the restriction occurred surrounding the patients who have venous outflow restriction; the more
shunting zone (5 of 8 [63%]) or in mixed type patterns (31 of extensive the thrombosis or venous occlusion, the higher the
35 [89%]) in this group than when the restriction occurred percentage of CVR.
remote to the shunt (6 of 17 [35%]; P⬍0.001). All of the LE Multiplicity of the shunts was more commonly found in the
lesions drained directly into the cerebral or spinal cord veins DE group (36% increasing up to 46% with the pediatric group
with CVR and in the majority (29 of 35 [83%]) of the nonspinal excluded), frequently being within adjacent regions of the
patients, there was no venous outflow restriction. Refer to same epidural type. Multifocality of dural arteriovenous
supplemental Table IV for tabulation of the data concerning the lesions in children has already been reported previously.32
type of thrombosis in relation to CVR in each group. Although the etiology of these shunts is not known, there
In the DE shunts, the venous stenosis was usually distal to seems to be clinical and radiological evidence that they are
the shunt or of the mixed type with the rate of CVR being evolutionary lesions and it has been suggested that they may
higher in the mixed type group (20 of 35 [57%] versus 22 of have been induced by venous sump from the sinus draining
25 [88%]; P⫽0.001). No statistical significance was found in the DAVSs.32 In the adult population, multifocality may be
the other groups. Refer to supplemental Table V for tabula- due to venous hypertension, typically from sinus thrombo-
tion of the data concerning the location of thrombosis in sis,33 although the exact pathomechanism is as yet unclear. In
relation to CVR in each group. the literature, it has been reported that the subgroup with
multiple DAVFs had a 3 times higher rate of hemorrhagic
Discussion presentation compared with a single DAVFs due to a higher
rate of CVR.34
Ventral Epidural Shunts
There was an approximately 2.3:1 female predominance in Lateral Epidural Shunts
this group, which is also seen in other lesions involving the There was a strong male predominance, approximately 4:1,
within this group. The characteristics are summarized in
Table 2. Ventral Epidural Shunts (osteo关cartilaginous兴-epidural)
Female predominance Table 4. Lateral Epidural Shunts
No reflux unless Male predominance
Extensive thrombosis of epidural drainage Present at later age
High-flow shunts Always aggressive lesion; CVR always present
Geibprasert et al Dural Arteriovenous Shunts 2793

Table 4. The patients also present at a later age compared References


with the other groups. As previously described in patients 1. Barrow DL, Spector RH, Braun IF, Landman JA, Tindall SC, Tindall GT.
with spinal DAVFs, these shunts most likely manifest them- Classification and treatment of spontaneous carotid– cavernous sinus
fistulas. J Neurosurg. 1985;62:248 –256.
selves after spinal cord draining veins have been obliterated 2. Borden JA, Wu JK, Shucart WA. A proposed classification for spinal and
by fibrosis from aging.35,36 The drainage into the cortical or cranial dural arteriovenous fistulous malformations and implications for
perimedullary spinal cord veins results in increased pial treatment. J Neurosurg. 1995;82:166 –179.
venous pressure with a high rate of neurological symptoms 3. Cognard C, Gobin YP, Pierot L, Bailly AL, Houdart E, Casasco A, Chiras
J, Merland JJ. Cerebral dural arteriovenous fistulas: clinical and angio-
ranging from venous infarctions, global neurological deficits graphic correlation with a revised classification of venous drainage.
to hemorrhage in the brain or congestive venous myelopathy Radiology. 1995;194:671– 680.
in the cord.37,38 Due to the role played by veins in cranial 4. van Dijk JM, ter Brugge KG, Willinsky RA, Wallace MC. Clinical course
locations, the shunts will involve the subarachnoid portion of of cranial dural arteriovenous fistulas with long-term persistent cortical
venous reflux. Stroke. 2002;33:1233–1236.
the draining cortical vein causing venous ectasias that may be 5. Fleming A, Keynes RJ, Tannahill D. The role of the notochord in
associated with hemorrhage from rupture of the venous vertebral column formation. J Anat. 2001;199:177–180.
pouches.22–24 6. Eichmann A, Yuan L, Moyon D, Lenoble F, Pardanaud L, Breant C.
Vascular development: from precursor cells to branched arterial and
venous networks. Int J Dev Biol. 2005;49:259 –267.
Treatment Considerations 7. O’Rahilly R, Muller F. Neurulation in the normal human embryo. Ciba
The decision to treat or not to treat still depends on the Found Symp. 1994;181:70 – 82; discussion 82– 89.
presence of cortical or spinal venous reflux regardless of the 8. Lasjaunias P, Berenstein A, ter Brugge KG. Surgical Neuroangiography.
1. Clinical Vascular Anatomy and Variations. Berlin: Springer; 2001.
symptoms present.26 As multiple other previous reports have 9. Padget DH. The cranial venous system in man in reference to devel-
already emphasized, the presence of cerebral or spinal venous opment, adult configuration, and relation to the arteries. Am J Anat.
reflux should prompt immediate treatment, because their 1956;98:307–355.
natural history is always aggressive with a high rate of 10. O’Rahilly R, Muller F. Ventricular system and choroid plexuses of the
human brain during the embryonic period proper. Am J Anat. 1990;189:
morbidity and mortality.4,27,39 285–302.
11. Cullen S, Ozanne A, Alvarez H, Mercier PH, Brassier G, Lasjaunias P.
Conclusions The anastomotic venous circle of the base of the brain. Interv Neuro-
The roles of venous afferents of the 3 epidural spaces radiol. 2005;11:325–332.
12. Alvarez H, Garcia Monaco R, Rodesch G, Sachet M, Krings T,
established during embryological development of the central Lasjaunias P. Vein of Galen aneurysmal malformations. Neuroimaging
nervous system and craniospinal structures are different. This Clin N Am. 2007;17:189 –206.
reference to embryology allows analyzing both cranial and 13. Friede H. Normal development and growth of the human neurocranium
Downloaded from http://ahajournals.org by on October 7, 2019

and cranial base. Scand J Plast Reconstr Surg. 1981;15:163–169.


spinal homologs and, therefore, is the basis for a classifica-
14. Labrom RD. Growth and maturation of the spine from birth to ado-
tion system that can be applied to all types of lesions lescence. J Bone Joint Surg Am. 2007;89(suppl 1):3–7.
developing in these spaces. 15. Wilson DB. Embryonic development of the head and neck: part 5, the
This new classification has the ability to predict the brain and cranium. Head Neck Surg. 1980;2:312–320.
16. Lasjaunias P, Kwok R, Goh P, Yeong KY, Lim W, Chng SM. A devel-
drainage of shunts located in different locations based on the opmental theory of the superior sagittal sinus(es) in craniopagus. Childs
craniospinal venous anatomy and the presence of associated Nerv Syst. 2004;20:526 –537.
venous outflow restriction (stenosis/occlusion), usually 17. Piske RL, Lasjaunias P. Extrasinusal dural arteriovenous malformations.
thrombosis, which could be either an etiology or comorbidity Report of three cases. Neuroradiology. 1988;30:426 – 432.
18. Opperman LA. Cranial sutures as intramembranous bone growth sites.
of the disease. Because venous thrombosis is uncommon in Dev Dyn. 2000;219:472– 485.
the general population, it may reflect an underlying biological 19. Krings T, Mull M, Bostroem A, Otto J, Hans FJ, Thron A. Spinal epidural
disorder in these patients with possible different geographic arteriovenous fistula with perimedullary drainage. Case report and patho-
(population) impact. mechanical considerations. J Neurosurg Spine. 2006;5:353–358.
20. Pirouzmand F, Wallace MC, Willinsky R. Spinal epidural arteriovenous
The significant difference of the patient characteristics (sex fistula with intramedullary reflux. Case report. J Neurosurg. 1997;87:
and age) between the groups of the new classification 633– 635.
suggests biological/hormonal differences within the epidural 21. Goyal M, Willinsky R, Montanera W, terBrugge K. Paravertebral arte-
riovenous malformations with epidural drainage: clinical spectrum,
venous system in each region and may point toward a
imaging features, and results of treatment. AJNR Am J Neuroradiol.
different etiology of the 3 different groups of arteriovenous 1999;20:749 –755.
shunts. Grouping DAVFs into a single entity may hide the 22. Kai Y, Hamada J, Morioka M, Yano S, Mizuno T, Kuratsu J. Arterio-
fundamental differences existing in each location. We pre- venous fistulas at the cervicomedullary junction presenting with sub-
arachnoid hemorrhage: six case reports with special reference to the
sume that the new classification proposed in this study will angiographic pattern of venous drainage. AJNR Am J Neuroradiol. 2005;
contribute to a better understanding of these lesions and to 26:1949 –1954.
their respective disease mechanisms. 23. Komotar RJ, Connolly ES Jr, Lignelli AA, Mack WJ, Mocco J, Harbaugh
RE. Clinicoradiological review: bilateral ethmoidal artery dural arterio-
venous fistulas. Neurosurgery. 2007;60:131–135; discussion 135–136.
Source of Funding 24. Kothbauer K, Huber P. Dural arteriovenous fistula in the falx cerebri.
SG received a Research Grant of the World Federation of Interven- Neuroradiology. 1994;36:616 – 618.
tional Neuroradiology (WFITN). 25. Lasjaunias P, Chiu M, ter Brugge K, Tolia A, Hurth M, Bernstein M.
Neurological manifestations of intracranial dural arteriovenous malfor-
mations. J Neurosurg. 1986;64:724 –730.
Disclosures 26. Lasjaunias P, ter Brugge K, Chiu M. Dural AVM. Dural AVM.
None. Neurosurgery. 1985;16:435– 436.
2794 Stroke October 2008

27. Davies MA, ter Brugge K, Willinsky R, Coyne T, Saleh J, Wallace MC. riovenous fistulas: a case report of multiple fistulas remote from sinus
The validity of classification for the clinical presentation of intracranial thrombosis. Neuroradiology. 2001;43:980 –984.
dural arteriovenous fistulas. J Neurosurg. 1996;85:830 – 837. 34. van Dijk JM, ter Brugge KG, Willinsky RA, Wallace MC. Multiplicity of
28. Krings T, Mull M, Gilsbach JM, Thron A. Spinal vascular malformations. dural arteriovenous fistulas. J Neurosurg. 2002;96:76 –78.
Eur Radiol. 2005;15:267–278. 35. Andersson T, van Dijk JM, Willinsky RA. Venous manifestations of
29. Stiebel-Kalish H, Kalish Y, Bar-On RH, Setton A, Niimi Y, Berenstein A, spinal arteriovenous fistulas. Neuroimaging Clin N Am. 2003;13:73–93.
Kupersmith MJ. Presentation, natural history, and management of carotid 36. Van Dijk JM, ter Brugge KG, Willinsky RA, Farb RI, Wallace MC.
cavernous aneurysms. Neurosurgery. 2005;57:850 – 857; discussion Multidisciplinary management of spinal dural arteriovenous fistulas:
850 – 857. clinical presentation and long-term follow-up in 49 patients. Stroke.
30. Barbosa M, Mahadevan J, Weon YC, Yoshida Y, Rodesch G, Alvarez H,
2002;33:1578 –1583.
Lasjaunias P. Dural sinus malformations (DSM) with giant lakes, in
37. Awad IA, Little JR, Akarawi WP, Ahl J. Intracranial dural arteriovenous
neonates and infants: review of 30 consecutive cases. Interv Neuroradiol.
2003;9:407– 417. malformations: factors predisposing to an aggressive neurological course.
31. Lasjaunias P, ter Brugge K, Berenstein A. Surgical Neuroangiography. 3: J Neurosurg. 1990;72:839 – 850.
Clinical and Interventional Aspects in Children, II Edition. Berlin: 38. Willinsky R, ter brugge K, Montanera W, Mikulis D, Wallace MC.
Springer; 2006. Venous congestion: an MR finding in dural arteriovenous malformations
32. Garcia-Monaco R, Rodesch G, Terbrugge K, Burrows P, Lasjaunias P. with cortical venous drainage. AJNR Am J Neuroradiol. 1994;15:
Multifocal dural arteriovenous shunts in children. Childs Nerv Syst. 1991; 1501–1507.
7:425– 431. 39. van Dijk JM, ter Brugge KG, Willinsky RA, Wallace MC. Selective
33. Kusaka N, Sugiu K, Katsumata A, Nakashima H, Tamiya T, Ohmoto T. disconnection of cortical venous reflux as treatment for cranial dural
The importance of venous hypertension in the formation of dural arte- arteriovenous fistulas. J Neurosurg. 2004;101:31–35.
Downloaded from http://ahajournals.org by on October 7, 2019

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