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The anterior medullary-anterior pontomesencephalic venous system and its

bridging veins communicating to the dural sinuses: Normal anatomy and
drainage routes from dural arterioven...

Article in Neuroradiology · December 2008

DOI: 10.1007/s00234-008-0433-3 · Source: PubMed

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Neuroradiology (2008) 50:1013–1023
DOI 10.1007/s00234-008-0433-3

DIAGNOSTIC NEURORADIOLOGY

The anterior medullary–anterior pontomesencephalic venous

system and its bridging veins communicating to the dural
sinuses: normal anatomy and drainage routes from dural
arteriovenous fistulas
Hiro Kiyosue & Shuichi Tanoue & Yoshiko Sagara &
Yuzo Hori & Mika Okahara & Junji Kashiwagi &
Hirofumi Nagatomi & Hiromu Mori

Received: 1 December 2007 / Accepted: 25 June 2008 / Published online: 18 July 2008
# The Author(s) 2008

Abstract APMV end separately to the bridging vein or the transverse

Introduction We evaluated the normal venous anatomy of pontine vein. Bridging veins were identified in 34 cases,
the anterior medullary/anterior pontomesencephalic venous connecting to the cavernous sinus in 33, to the suboccipital
(AMV/APMV) system and bridging veins connected to the cavernous sinus in 11, and the inferior petrosal sinus in five
dural sinuses using magnetic resonance (MR) imaging and cases. In 80 DAVF cases, seven of 40 cavernous sinus
demonstrated cases of dural arteriovenous fistulas (DAVFs) DAVFs, two craniocervical junction DAVFs, and one
with bridging venous drainage. inferior petrosal sinus DAVF drained via bridging veins to
Materials and methods MR images obtained using a 3D the brain stem.
gradient echo sequence in 70 patients without lesions Conclusion The AMV/APMV and bridging veins showed
affecting the deep or posterior venous channels were various anatomies and frequently showed a connection to
reviewed to evaluate the normal anatomy of the AMV/ the cavernous sinus. Knowledge of the venous anatomy is
APMV system and bridging veins. MR images and digital helpful for the diagnosis and intravascular treatment of
subtraction angiography in 80 cases with intracranial or DAVFs.
craniocervical junction DAVFs were reviewed to evaluate
the bridging venous drainage from DAVFs. Keywords Dural arteriovenous fistula . Cerebral vein .
Results MR images clearly revealed AMV/APMV in 35 Angiography . MRI
cases. Fifteen cases showed a direct connection between
AMV and APMV, while 15 cases showed an indirect
communication via the transverse pontine vein or the Introduction
bridging vein. In the five remaining cases, the AMV and
The anterior pontomesencephalic–anterior medullary venous
(APM–AMV) system is an important venous channel that
H. Kiyosue (*) : S. Tanoue : Y. Sagara : M. Okahara :
J. Kashiwagi : H. Mori
drains blood from the brain stem and cerebellum. The
Department of Radiology, Oita University Faculty of Medicine, anterior pontomesencephalic vein (APMV) is connected to
1-1 Idaigaoka, Hasama, the basal vein via the peduncular vein, superiorly, which runs
Yufu City, Oita, Japan 879-5503 longitudinally in the peduncular fossa or along the anterior
e-mail: hkiyosue@med.oita-u.ac.jp
surface of the cerebral peduncle, and is often continuous with
Y. Hori the AMV, inferiorly [1]. The AMV usually runs in the
Department of Radiology, Nagatomi Neurosurgical Hospital, midline along the anterior surfaces of the pons and medulla,
Oita, Japan which connect to the anterior spinal vein, inferiorly (Fig. 1).
This longitudinal venous channel communicates with the
H. Nagatomi
Department of Neurosurgery, Nagatomi Neurosurgical Hospital, adjacent dural sinuses via the transverse pontine vein and/or
Oita, Japan bridging veins [2]. Therefore, dural arteriovenous fistulas
1014 Neuroradiology (2008) 50:1013–1023

craniocervical junction. Postcontrast images after the intrave-

nous injection of 0.1 mmol/kg gadolinium chelate (Omniscan)
were obtained for each patient.
The images were transferred to a workstation, and the
transverse images were evaluated by consensus between two
neuroradiologists (H.K. and Y.S.) for the normal anatomies
of the APM–AMV system and its bridging veins. The
vertical continuity of such veins was evaluated by paging the
transverse images on the same window (Fig. 2).
We retrospectively reviewed 80 cases of dural AVFs that
performed digital subtraction angiography (DSA) in our
institution between January 2000 and March 2007 and
evaluated DSA and MRI with regard to the draining route
via the APM–AMV system. The locations of dural AVFs
were in the cavernous sinus in 40, transverse sigmoid sinus in
17, tentorial in seven, condylar canals in five, craniocervical
junction in seven, anterior fossa in two, and others in seven
cases.
Fig. 1 Schematic diagram of the APM–AMV system. The APMV
connects to the peduncular vein superiorly, which runs longitudinally
in the peduncular fossa and is continuous with the transverse pontine Results
vein and the AMV inferiorly at the mid-pons level. The AMV usually
runs in the midline along the anterior surface of the pons and medulla,
Normal venous anatomy
which connects to the anterior spinal vein inferiorly. The transverse
pontine vein connects to the petrosal vein laterally
Among 70 patients, the APM–AMV system was entirely
(DAVFs) can drain through bridging veins into the APM– evaluated in 35 patients. In the other patients, the APMV
AMV system and may cause serious symptoms such as and/or AMV could not be identified or was scantly visible
pontine hemorrhage and venous edema [3–6]. However, when evaluating longitudinal continuity. In 35 patients, we
little attention has been paid to the venous anatomy of the observed several variations of the APM–AMV system at two
bridging veins and the APM–AMV system. In this study, levels of the pontomedullary junction and the mid-pons.
we evaluated the venous anatomy of the APM–AMV
system and its bridging veins that communicate with the Pontomedullary junction level
APM–AMV system and the dural sinuses using magnetic
resonance imaging (MRI). Cases of dural AVF draining via The patterns of the AMV at the pontomedullary junction
the venous system were also reviewed and demonstrated. were classified into six types (Fig. 3). These were type 1,
single AMV running superiorly in the midline along the
anterior surface of the pons; type 2, single AMV running
Materials and methods superior laterally; type 3, double AMVs with one running
in the midline and the other running superior laterally; type
We retrospectively evaluated MRI from consecutive 4, double AMVs both running superior laterally; type 5,
patients examined using fat-suppressed contrast-enhanced triple AMV; and type 6, absent AMV superiorly beyond the
3D fast gradient-echo MRI between March 2004 and April pontomedullary junction. Fifteen patients (43%) were
2006. Among them, patients with pathological conditions considered as type 1, five (14%) were type 2, six (17%)
potentially affecting the APM–AMV system such as were type 3, four (11%) were type 4, two (6%) were type 5,
cerebellopontine angle tumors were excluded from the study, and three (8%) were type 6.
leaving 70 participating patients (25 men and 45 women; age
range, 26–83 years; mean age, 57.6 years). The fat-suppressed Mid-pons level
contrast-enhanced 3D fast gradient-echo images using the
1.5 T MR unit (Excelart Vantage, Toshiba Medical Systems, The patterns of the APMV and the AMV at the mid-pons
Tokyo, Japan) were evaluated. The imaging parameters were level were classified into three types (Fig. 4): type A, the
as follows: repetition time/echo time, 25:5.5; flip angle, 20°; AMV directly continues to the APMV; type B, the AMV
matrix size, 224×256; section, 1 mm. The scanning area communicates with the APMV via the transverse pontine
covered between the level of the orbital roof and the vein in which there are two subtypes of unilateral
Neuroradiology (2008) 50:1013–1023 1015

Fig. 2 Normal MRI of the APM–AMV system. The anterior spinal then joins with the APMV via the transverse pontine vein (type B).
vein runs along the anterior surface of the cord and receives the The APMV continues to the peduncular vein superiorly. Note the
bridging vein [arrowhead in (a)] from the suboccipital cavernous bridging vein to the cavernous sinus [arrowheads in (e)]. Arrows
sinus at the craniocervical junction level. The AMV also runs in the indicate AMV/APMV
midline on the anterior surface of the medulla and pons (type 1) and

communication and bilateral communication; type C, the of unilateral communication and six cases of bilateral
AMV is interrupted at the APMV, at the mid-pons level. In communication.
type C, the AMV and APMV end to the cavernous sinus,
separately through the bridging veins and/or the transverse Bridging veins
pontine vein (Fig. 5) or to the petrosal vein. There were 15
patients (43%) of type A, 15 (43%) of type B, and five Bridging veins were identified in 34 of 35 patients (97%).
(14%) of type C. In the type B group, there were nine cases The bridging veins communicated with the APMV–AMV
1016 Neuroradiology (2008) 50:1013–1023

Fig. 3 Various types of the

anterior medullary vein at the
pontomedullary junction level.
Type 1 single AMV running
superiorly in the midline along
the anterior surface of the pons.
Type 2 single AMV running
superior laterally. Type 3 double
AMVs, one running in the
midline and the other running
superior laterally. Type 4 double
AMVs, both running superior
laterally. Type 5 triple AMVs.
Type 6 absent AMV beyond the
pontomedullary junction,
superiorly
Neuroradiology (2008) 50:1013–1023 1017

Fig. 4 Variations of the APMV

and the AMV at the mid-pons
level. Type A the AMV directly
continues to the APMV. Type B
the AMV communicates with
the APMV via the transverse
pontine vein in which there are
two subtypes of communication
(unilateral communication: B1
and bilateral communication:
B2). Type C the AMV interrupts
the APMV at the mid-pons
level. The AMV and APMV end
at the cavernous sinus separately
through the bridging veins

and cavernous sinus, inferior petrosal sinus, suboccipital in seven, at the craniocervical junction in two, and at the
cavernous sinus, marginal sinus, and jugular bulb (Fig. 6). inferior petrosal sinus in one case (Figs. 7, 8, 9 and 10).
Bridging veins communicating with the APMV–AMV (via Two cases of dural AVFs were located on one craniocervical
the transverse pontine vein) to the posterior aspect of the junction and one inferior petrosal sinus showing symptoms
cavernous sinus were observed in 33 patients (94%) in due to edema of brainstem or spinal cord (Fig. 8). In one case
which bilateral bridging veins to both cavernous sinuses of cavernous dural AVF, transient worsening of symptoms
were seen in 15 patients. Bridging veins to the suboccipital occurred after incomplete transvenous embolization with
cavernous sinus were observed in 11 patients (31%). Five residual bridging venous drainage due to brainstem edema
patients (14%) showed that the veins were bridged to the (Fig. 9).
inferior petrosal sinus while three patients showed bridging
to the marginal sinus, and bridging to the jugular bulb was
seen in one patient. Discussion

Dural arteriovenous fistulas The APMV and the AMV are the longitudinal venous
channels that run along the anterior surface of the brain
Among the 81 cases of intracranial or craniocervical stem. The APM–AMV runs more closely to the brain stem
junction dural AVFs, bridging venous drainage to the than the basilar artery; thus, the APM–AMV can exactly
APM–AMV system was found in ten cases. The locations define the anterior outline of the brainstem on lateral view
of dural AVFs in the ten cases were in the cavernous sinus of angiography [7, 8]. This information has been used in
1018 Neuroradiology (2008) 50:1013–1023

Fig. 5 MRI of the type 1 and type C APM–AMV system. The AMV cavernous sinus via the bridging vein (type C). The APMV (arrow-
(arrows) runs along the anterior surface of the medulla and pons (type heads) also ends at the left cavernous sinus via a different bridging
1), then runs superolaterally at the mid-pons level and ends at the left vein

Fig. 6 Types and frequencies of

bridging veins. a Bridging vein
to the cavernous sinus.
b Bridging vein to the inferior
petrosal sinus, c Bridging vein
to the marginal sinus,
d Bridging vein to the
suboccipital cavernous sinus
Neuroradiology (2008) 50:1013–1023 1019

Fig. 7 Craniocervical junction DAVF draining via bridging vein and sinus. MRI (e–i) show that the dural AVF draining into the anterior
AMV/APMV system (type 1 and type C). A 70-year-old woman with medullary vein continuing superiorly in the midline along the anterior
a dural AVF located at the craniocervical junction. The AVF was surface of the medulla and pons. The AMV (arrows) runs right
incidentally found on angiography when evaluating for a cerebral laterally at the mid-pons level and joins the right cavernous sinus via
aneurysm at the left internal carotid artery (not shown). Bilateral the bridging vein (arrowheads). Because the AVF showed no
vertebral angiography (a–d) showed that the AVF drained via the symptoms, and MRI showed no brainstem edema; the AVF was
anterior medullary vein, and the bridging vein into the right cavernous treated by stereotactic radiosurgery

diagnostic neuroradiology. However, the recent advances in During the fourth stage of embryonic development,
technology of less invasive modalities including MRI and numerous primary transverse (pial-arachnoid) veins first
multidetector-low computed tomography (CT) can directly become identified on the surface of the neural tube, which
depict the brain stem and lesions. Only little attention has been connect to the dural plexus. Between these primary transverse
paid to the APM–AMV system in diagnostic neuroradiology. veins, secondary longitudinal anastomoses soon develop
1020 Neuroradiology (2008) 50:1013–1023

Fig. 8 Craniocervical junction DAVF draining via bridging vein and occipital artery shows that the AVF drains into the AMV and backward
AMV (type 6). A 77-year-old man with symptoms of spinal cord inferiorly to the spinal vein, probably due to hypoplasty of the AMV at
edema. Angiography showed that the AVF was located at the the pontomedullary junction (arrow; type 6). CT (b) after embolization
cervicocranial junction and was fed by the meningeal branches from with glue shows glue cast (white arrow) in the fistulous point at the
the left occipital artery and the left vertebral artery. Selective right suboccipital cavernous sinus
angiography (a) via microcatheter positioned at a branch of the right

Fig. 9 Cavernous sinus DAVF

with bridging venous drainage.
A 42-year-old woman with oc-
ular symptoms. Bilateral carotid
angiography showed a dural
AVF at the cavernous sinus,
which drained into the superior
orbital vein, the superficial mid-
dle cerebral vein, and the basal
vein via the bridging venous
system (a, b). Transvenous em-
bolization was performed, but
unfortunately, the procedure was
interrupted because the catheter
was accidentally pulled back to
the inferior petrosal sinus and
never advanced into the CS. The
final angiogram showed occlu-
sion of most of the AVF, but the
residual AVF drained via the
bridging vein into the transverse
pontine vein (arrows) and to the
APMV (c, d). Transient wors-
ening of the symptoms due to
pontine edema that developed
after embolization
Neuroradiology (2008) 50:1013–1023 1021

Fig. 10 Cavernous sinus DAVF

with bridging venous drainage
A 48-year-old woman with
ocular symptoms. Bilateral in-
ternal and external carotid
angiograms showing a dural
AVF at the left cavernous sinus,
which drained into the superior
orbital vein, the superficial mid-
dle cerebral vein, and the basal
vein (a). Three-dimensional
DSA image (b) well demon-
strated the AVF draining via the
bridging vein (white arrow-
heads) into the APMV and the
AMV (white arrows). Selective
venogram (c) via a microcath-
eter positioned at the outlet to
the bridging vein clearly dem-
onstrate the bridging venous
drainage to the APMV (arrows).
With special attention to the
bridging venous drainage, the
AVF was completely occluded
without any complications (d)

parallel to the basilar artery. Then, most of the primary cavernous sinus would play an important role for brain
transverse veins are reduced according to the enlargement of stem venous drainage.
the brain. In this way, the venous net and the main pial veins of To the best of our knowledge, only one anatomical study
the medulla and pons are formed [9]. Therefore, several has been reported in the English literature on the bridging
variations of the APMV–AMV system can occur depending veins connecting the brain stem venous system with the
on the degree of the regression and the development of the adjacent dural sinus. Matsushima et al. [2] mentioned that
primary transverse and secondary longitudinal veins. there were several bridging veins connecting the APM–
In our results, there were several variations in the course AMV system to the adjacent dural sinuses, in an excellent
of the APM–AMV system. The variations of the AMV were anatomical study. They reported that the bridging veins run
frequently found at the pontomedullary junction level. The from the APMV or transverse pontine vein to the posterior
AMV communicates with the vein of the pontomedullary portion of the cavernous sinus just below the Meckel’s
sulcus at the pontomedullary sulcus and is contiguous to the cave; from the vein of the pontomedullary sulcus or
median anterior medullary vein (type 1), one or two anterior anterior, lateral, and transverse medullary veins to the
lateral (ponto)medullary veins (type 2 or 4), both the median inferior petrous sinus, the sigmoid sinus, the marginal sinus,
and lateral anterior (ponto)medullary vein (type 3 or 5), or is or the anterior condylar vein. According to their results, in
discontinued superiorly (type 6). 25 adult cadavers, bridging veins to the cavernous sinus
At the mid-pons level, the AMV often communicates were identified in 12.5%, to the inferior petrosal sinus in
with the APMV directly (type A) or indirectly via the 8.3%, to the sigmoid sinus in 37.5%, and to the marginal
transverse pontine vein (type B). However, there was no sinus around the foramen in 41.7%. In our study, bridging
communication between the APMV and AMV in 14% of veins to the cavernous sinus were more frequently observed
cases (type C). In the type C group, the bridging vein to the in 94% of patients (of 35 cases). Although we cannot
1022 Neuroradiology (2008) 50:1013–1023

clearly explain why we obtained such a difference in the quate embolization for such cases can lead to serious
frequency of visibility of the bridging veins, we hypothe- complications such as brain stem edema due to venous
size that the differences may be the results of different congestion (Fig. 9). Kim et al. [11] demonstrated the
methodologies between a cadaver-based anatomical study transvenous embolization of cavernous dural AVFs in 57
and a clinical MR evaluation. patients. In their study series, venous congestion of the
For the cases of dural AVFs potentially draining via the posterior fossa after transvenous embolization developed in
APM–AMV system, the development of the APM–AMV two patients. One patient showed permanent deficits, and the
system and its bridging veins would be related to the other improved after additional treatments. Angiography
symptoms. In our series, both cases of dural AVFs at the after embolization in one patient showed remarkable residual
craniocervical junction drained via the AMV superiorly. shunt draining into the APMV suggesting bridging venous
One case without symptoms showed the AMV directly drainage. Therefore, it is very important for the treatment of
connected to the APMV (type 1), and the AVF drained into cavernous dural AVFs to assess deep venous drainage
the cavernous sinus via the developed bridging vein including bridging venous drainage before and during
without venous stasis. In contrast, another case with spinal transvenous embolization.
cord edema showed that the AMV was interrupted at the Our study has several limitations. Spatial resolution of
pontomedullary junction (type 6) and the AVF drained via MRI was limited in evaluating the normal venous anatomy
the vein of the pontomedullary sulcus and backward into the of the APM–AMV system. Although we evaluated 70
spinal veins. Kai et al. [10] reported six cases of AVF at the cases, the APM–AMV system could have been entirely
cervicomedullary junction including four cases of dural evaluated in only 35 cases. It is possible that the APM–
AVFs. All four cases of dural AVFs presented with AMV system was too small to be identified on MRI in
subsrachnoid hemorrhage, and the AVFs drained ascending some cases. Some variations of the venous system, which
into the cavernous sinus, the superior petrosal sinus, or the could not be evaluated by MRI, may be presented. Our
inferior petrosal sinus. Several cases of intracranial dural work may scratch only the surface of the great variability of
AVFs draining into the APM–AMV system have been the normal venous anatomy of the AMV/APMV system
reported, and the majority of the reported cases showed and its bridging veins. However, we believe that the
brain stem injury due to venous congestion and/or knowledge of the venous anatomy would be helpful for
hemorrhage [3–6]. Two potential drainage routes to the the diagnosis and interventional treatment of dural AVFs.
APM–AMV system of the petrosal venous route and the
bridging venous routes exist. The petrosal venous route is
commonly seen in dural AVFs at the superior petrosal
Conflict of interest statement We declare that we have no conflict
sinus, tentorium, and rarely in cavernous dural AVFs. The of interest.
AVF drains via the petrosal vein contiguous with the
transverse pontine vein into the AMV–APMV system [5].
To the best of our knowledge, only one case has been Open Access This article is distributed under the terms of the
reported for the bridging venous drainage in the English Creative Commons Attribution Noncommercial License which per-
mits any noncommercial use, distribution, and reproduction in any
literature [6]. Although we found some additional cases of medium, provided the original author(s) and source are credited.
angiography suggesting bridging venous drainage to the
APM–AMV in previously published papers, none showed
specific descriptions of the drainage route to the brain stem
[4, 5, 11]. In our review of cases of cavernous dural AVFs, References
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