Original Paper
Eur Neurol 2017;78:154–160
DOI: 10.1159/000478980
Venous Stasis and Cerebrovascular
Complications in Cerebral Venous
Sinus Thrombosis
Takeo Sato a Yuka Terasawa a Hidetaka Mitsumura a Teppei Komatsu a
Kenichi Sakuta a Kenichiro Sakai a Satoshi Matsushima b Yasuyuki Iguchi a
a
Department of Neurology, The Jikei University School of Medicine, Tokyo, Japan; b Department of Radiology,
The Jikei University School of Medicine, Tokyo, Japan
Keywords
Cerebral venous thrombosis · Complications · Magnetic
resonance imaging · Seizures · Susceptibility-weighted
imaging · Venous stasis
Abstract
Background/Aims: The factors related to cerebrovascular
complications in cerebral venous sinus thrombosis (CVST) are
controversial. We focused on venous stasis and investigated
its relationship with cerebrovascular complications in CVST.
Methods: CVST patients between June 2013 and October
2016 were enrolled. Relationships between cerebrovascular
complications, defined as cerebral venous infarction, intrace-
rebral hemorrhage, or subarachnoid hemorrhage, and cere-
brum venous stasis and other clinical information were retro-
spectively analyzed. Venous stasis was evaluated by the
prominence of the veins on susceptibility-weighted imaging
(SWI). The cerebrum was divided into 10 regions according to
the venous drainage territories, and venous stasis was quan-
tified by adding one point for venous prominence on SWI for
each region (CVST SWI score). Results: All 5 cases in the non-
complicated group had a CVST SWI score of 0. The 3 patients
with CVST SWI scores higher than 0 had cerebrovascular com-
© 2017 S. Karger AG, Basel
E-Mail karger@karger.com
www.karger.com/ene
Received: April 13, 2017
Accepted: June 21, 2017
Published online: August 16, 2017
plications. The CVST SWI scores were higher in the compli-
cated group than in the noncomplicated group (3.0 vs. 0, p =
0.010). Seizures were seen in all patients with complica-
tions and in none of the patients without complications (3 vs.
0, p = 0.018). Conclusion: Venous stasis evaluated by SWI can
help predict cerebrovascular complications in CVST. A sei-
zure is an important initial symptom that suggests cerebro-
vascular complications in CVST. © 2017 S. Karger AG, Basel
Introduction
The spectrum of clinical presentations in patients with
cerebral venous sinus thrombosis (CVST) varies consid-
erably [1]. While some patients with CVST have relative-
ly mild symptoms, others develop devastating complica-
tions, including hemorrhagic venous infarctions and se-
vere intracranial hypertension [1].
The specific factors associated with cerebrovascular
complications are uncertain. Especially, whether the loca-
tion of the venous thrombus contributes to cerebrovascu-
lar complications is a very controversial matter [2, 3]. The
reason for this may be that the clinical manifestations de-
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Takeo Sato, MD
Department of Neurology
The Jikei University School of Medicine
Göteborgs Universitet
3-25-8, Nishi-Shimbashi, Minato-ku, Tokyo 105-8461 (Japan)
Downloaded by:
E-Mail takeo.sato.821 @ icloud.com
pend on not only the localization of the thrombus but also
on the rate of progression and the extent of venous col-
lateralization [4]. Cerebral venous stasis, which is a result
of venous flow including collateralization, varies mark-
edly among individuals, and it might be important to
evaluate it for predicting cerebrovascular complications
in CVST.
Diffusion-weighted imaging could show vasogenic
edema as a consequence of increased venous pressure in
cerebral venous thrombosis [5, 6], but it is difficult to
show the venous vasculature in detail. Susceptibility-
weighted imaging (SWI) has exquisite sensitivity to the
venous vasculature [7], and is able to demonstrate venous
stasis [8]. Thus, in this study, the focus was on whole ce-
rebrum venous stasis evaluated by SWI to predict cere-
brovascular complications in CVST. The relationships of
other factors with cerebrovascular complications in
CVST were also investigated from the available clinical
information.
Methods
Subjects
Consecutive patients with cerebral venous thrombosis were
retrospectively enrolled between June 2013 and October 2016. Ce-
rebral venous thrombosis was diagnosed using conventional angi-
ography, CT, and MRI. Patients with isolated cortical vein throm-
bosis (ICVT) were excluded from the present study and only pa-
tients with CVST were included. This was because, in ICVT
patients, the venous outflow through the large sinuses is not af-
fected, and the clinical features, such as the symptoms and the in-
cidence rate of complications, differ between CVST and ICVT pa-
tients [2, 9].
In CVST patients, only patients who were initially diagnosed
and treated at our hospital were included; patients who had
been  diagnosed and treated in other hospitals were excluded
(Fig. 1).
Presumed risk factors for CVST, initial symptoms, the location
of thrombus, and cerebrovascular complications of CVST, defined
as cerebral venous infarction, intracerebral hemorrhage, or sub-
arachnoid hemorrhage, were retrospectively reviewed. In order to
investigate the factors related to cerebrovascular complications of
CVST, the following information was also obtained from the pa-
tient history and medical information: laboratory examination
findings on admission (D-dimer, fibrinogen, C-reactive protein,
free Protein S, and Protein C activity), body mass index (calculated
as weight in kilograms divided by height in meters squared), oc-
clusion of the superior sagittal sinus, and cerebral venous stasis due
to CVST evaluated by SWI.
Neuroimaging
Thrombus location and cerebrovascular complications, de-
fined as cerebral venous infarction, intracerebral hemorrhage, or
subarachnoid hemorrhage, were evaluated by conventional angi-
ography, CT, and MRI. Cerebral venous infarction was defined as
Venous Stasis and CVST
15 cerebral venous
thrombosis cases
June 2012 – October 2016
3 isolated cortical vein
thrombosis cases
12 cerebral venous
sinus thrombosis cases
4 cases not initially diagnosed and
treated at our hospital
8 cerebral venous
sinus thrombosis cases
Fig. 1. Flowchart showing patient enrollment. Of the 15 cerebral
venous thrombosis patients from June 2013 to October 2016, 3
isolated cortical vein thrombosis patients and 4 patients who were
not initially diagnosed and treated at our hospital were excluded.
Finally, a total of 8 cerebral venous sinus thrombosis patients met
the study inclusion criteria.
the absence of arterial occlusion and the presence of ischemic le-
sions based on the venous perfusion area.
The MRI units used in this study were MAGNETOM Avanto
and MAGNETOM Symphony (Siemens Erlangen, Germany) at
1.5T. The sequence parameters of SWI were TR/TE = 49/40 ms,
flip angle 15°, section thickness = 2 mm, matrix = 256 × 230 with
interpolation, and FOV = 23 cm. In order to evaluate the promi-
nence of the veins on SWI, the SWI minimum intensity projection
(SWI mIP) was used for evaluation.
Intracerebral venous stasis was evaluated based on the promi-
nence of the veins on SWI. The cerebrum was divided into 10 re-
gions according to the venous drainage territories [10]: the region
that drains into the superior sagittal sinus (░); the region that
drains into the Sylvian veins (▩); the region that drains into the
transverse sinus and vein of Labbé (■); the region that drains into
deep cerebral veins (▤); and the region of deep white matter (med-
ullary) venous drainage (▥) (Fig. 2). One point was added for ve-
nous prominence on SWI for each region (CVST SWI score: min-
imum 0 points and maximum 10 points). Only local venous prom-
inence on SWI was considered positive and whole brain venous
prominence was not judged positive. One neurologist (T.S.) and
one neuroradiologist (S.M.) independently reviewed venous
prominences on SWI. When there was disagreement on the CVST
SWI score, the score was determined by discussion of the 2 evalu-
ators.
Data Analysis
All patients were divided into 2 groups, CVST with cerebro-
vascular complications (complicated group) and CVST with-
out  cerebrovascular complications (noncomplicated group).
After comparing the baseline and demographic data between
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Eur Neurol 2017;78:154–160 155
DOI: 10.1159/000478980
Göteborgs Universitet
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 a b
c d
Fig. 2. Regions for evaluation of vein prominence on MRI suscep-
tibility-weighted imaging according to the venous drainage terri-
tories. The cerebrum is divided into ten regions according to the
venous drainage territories: (1)/(2) the region that drains into the
superior sagittal sinus (░); (3)/(4) the region that drains into the
Sylvian veins (▩); (5)/(6) the region that drains into the transverse
sinus and vein of Labbé (■); (7)/(8) the region that drains into
deep cerebral veins (▤); and (9)/(10) the region of deep white mat-
ter (medullary) venous drainage (▥). a (1)/(2) the region that
drains into the superior sagittal sinus (░) and (9)/(10) the region
the  2 groups, the associations of factors with cerebrovascu-
lar complications were evaluated using Fisher’s exact test and
the Mann-Whitney U test, as appropriate. All statistical analy-
ses were performed using IBM SPSS Statistics version 22 soft-
ware.
156 Eur Neurol 2017;78:154–160
DOI: 10.1159/000478980
of deep white matter (medullary) venous drainage (▥) are shown.
b (1)/(2) the region that drains into the superior sagittal sinus (░),
(3)/(4) the region that drains into the Sylvian veins (▩), and (9)/
(10) the region of deep white matter (medullary) venous drainage
(▥) are shown. c, d (1)/(2) the region that drains into the superior
sagittal sinus (░), (3)/(4) the region that drains into the Sylvian
veins (▩), (5)/(6) the region that drains into the transverse sinus
and vein of Labbé (■), (7)/(8) the region that drains into deep ce-
rebral veins (▤), and (9)/(10) the region of deep white matter
(medullary) venous drainage (▥) are shown.
Results
A total of 15 cerebral venous thrombosis patients seen
from June 2013 to October 2016, and 8 CVST patients
(median age, 42 years; interquartile range, 30–50 years; 5
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 CVST, cerebral venous sinus thrombosis; SWI, MRI susceptibility-weighted imaging; SSS terr, region drains into superior sagittal sinus; SV terr, region drains into

matter (medullary) venous drainage; SSS, superior sagittal sinus; TS, transverse sinus; SS, sigmoid sinus; JV, jugular vein; Labbé, vein of Labbé; ICH, intracranial hemor-
Sylvian veins; TS/Labbé terr, region drains into transverse sinus and vein of Labbé; DCV terr, region drains into deep cerebral veins, and MV terr, region of deep white
men) met the study inclusion criteria. The baseline data
of all subjects are shown in online supplementary Table

Recanalizations
1; for all online suppl. material, see www.karger.com/

Completely
doi/10.1159/000478980. The most frequent initial symp-

Partially

Partially
Partially
Partially
tom as found in in 6 patients (75%) was headache. Focal

None

None

None
neurological symptoms were seen in 3 patients (38%), all
of whom had cerebrovascular complications. Seizures

Complications
were seen in all patients with complications, but no pa-
tients in the noncomplicated group had seizures (3 vs. 0,

ICH, SAH
p = 0.018). The most affected sinuses were the unilateral

None
None
None
None
None
transverse sinus to the sigmoid sinus to the jugular vein

ICH

CVI
(50%). Cerebral venous infarctions were seen in 1 patient
(13%), intracerebral hemorrhages were seen in 2 patients
(25%), and subarachnoid hemorrhages were seen in 1 pa-

lt.TS-lt.SS-lt.JV, Labbé

SSS-rt.TS-rt.SS-rt.JV
tient (13%).

rt.TS-rt.SS-rt.JV
Affected sinuses
There were no significant association between cere-

lt.TS-lt.SS-lt.JV
lt.TS-lt.SS-lt.JV
SSS-lt.TS-lt.SS
brovascular complications and the affected sinuses (on-

rt.TS-rt.SS
rt.SS-rt.JV
line suppl. Table 1). The CVST SWI scores of the subjects
are shown in Table 1. Kappa coefficient value was 0.79 in

Table 1. CVST SWI score, affected sinuses, complications, and recanalizations after treatment in all cases
evaluating CVST SWI scores between the 2 evaluators.
All cases in the noncomplicated group had a CVST SWI

CVST SWI
score of 0. The 3 patients with a CVST SWI score >0 had
cerebrovascular complications (Table 1; Fig.  3). The

score

8/10
3/10
2/10
0/10
0/10
0/10
0/10
0/10
CVST SWI scores were significantly higher in the com-
plicated group than in the noncomplicated group (3.0 vs.
0, p = 0.010), as shown in Figure 4 and online supplemen- MV terr
tary Table 1.
CVST SWI score in each venous drainage territory (rt./lt.)

1/1
0/0
0/0
0/0
0/0
0/0
0/0
0/0

rhage; SAH, subarachnoid hemorrhage; CVI, cerebral venous infarction.

Discussion
DCV terr

In this study, there were 2 major findings. First, eval-

0/0
0/0
0/0
0/0
0/0
0/0
0/0
0/0
uation of cerebral venous stasis by SWI can help pre-
dict  cerebrovascular complications in CVST. Second,
TS/Labbé terr

CVST patients developing seizure as an initial symptom

appear more likely to have cerebrovascular complica-
tions.
1/1
0/1
0/1
0/0
0/0
0/0
0/0
0/0

It was possible to evaluate intracerebral venous stasis

by the prominence of the veins on SWI, and it was found
SV terr

that the evaluation of whole cerebrum venous stasis on

1/1
0/1
0/0
0/0
0/0
0/0
0/0
0/0

SWI could help predict cerebrovascular complications

in CVST. This result was in line with a previous report
of Kawabori et al. that SWI could demonstrate stasis of
SSS terr

the cortical veins and that the dilated cortical veins on

1/1
0/1
0/1
0/0
0/0
0/0
0/0
0/0

SWI gradually normalized after treatment in a CVST

patient [11]. The mechanism is as follows. SWI is very
Case number

sensitive in detecting intravascular venous deoxygenat-

ed blood, as well as extravascular blood products. Ve-
Case 1
Case 2
Case 3
Case 4
Case 5
Case 6
Case 7
Case 8

nous stasis likely results in a greater prominence of the

veins due to higher concentrations of intravascular de-
130.241.16.16 - 9/14/2017 7:10:20 PM

Venous Stasis and CVST Eur Neurol 2017;78:154–160 157

DOI: 10.1159/000478980
Göteborgs Universitet
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 CVST SWI score
evaluation region
samples
a b
Case 1
e f
Case 2
i j
Case 3
m n
Fig. 3. Venous prominence evaluated by MRI susceptibility-
weighted imaging (CVST SWI score) in cases 1, 2, and 3. Sample
CVST SWI score evaluations (a–d): evaluation regions for the
prominence of veins on MRI susceptibility-weighted imaging ac-
cording to the venous drainage territories. The cerebrum is divid-
ed into 10 regions according to the venous drainage territories; rt./
lt. region that drains into the superior sagittal sinus (░); rt./lt. that
region drains into the Sylvian veins (▩); rt./lt. region that drains
into the transverse sinus and vein of Labbé (■); rt./lt. region that
drains into deep cerebral veins (▤); and rt./lt. region of deep white
matter (medullary) venous drainage (▥). Case 1 (e–h): Regions
surrounded by white circles have a CVST SWI score of 1. The
scored regions are: rt./lt. region that drains into the superior sagit-
tal sinus (░); rt./lt. region that drains into the Sylvian veins (▩);
158 Eur Neurol 2017;78:154–160
DOI: 10.1159/000478980
c d
g h
k l
o p
rt./lt. region that drains into the transverse sinus and vein of Labbé
(■); and rt./lt. region of deep white matter (medullary) venous
drainage (▥). The total CVST SWI score is 8/10 points. Case 2
(i–l): Regions surrounded by white circles have a CVST SWI score
of 1. The scored regions are: lt. region that drains into the superior
sagittal sinus (░); lt. region that drains into the Sylvian veins (▩);
and lt. region that drains into the transverse sinus and vein of Lab-
bé (■). The total CVST SWI score is 3/10 points. Case 3 (m–p):
Regions surrounded by white circles have a CVST SWI score of 1.
The scored regions are the lt. region that drains into the superior
sagittal sinus (░) and the lt. region that drains into the transverse
sinus and vein of Labbé (■). The total CVST SWI score is 2/10
points.
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10
9 p = 0.010
8 present results agree with previous reports that motor
7 any intracranial hemorrhage and infarction on admission
6 16]. An experimental study showed that the principal me-
CVST SWI score
5
4
3
2 is the main limitation of this study and we should be en-
1 spective nature of our study is the second limitation. The
0 SWI, it was difficult in some patients to determine wheth-
Complicated Non-complicated
(n = 3) (n = 5)
Fig. 4. Comparison of venous prominence evaluated by MRI sus-
ceptibility-weighted imaging for each region (CVST SWI score)
between cerebral venous sinus thrombosis with and without cere-
brovascular complications. Three patients have CVST SWI scores
>0 and all have complications. Noncomplicated patients score no
points in all cases. When the noncomplicated and complicated
groups are compared, the complicated group has a significantly
higher CVST SWI score (3.0 vs. 0, p = 0.010).
oxyhemoglobin [12]. In addition, as the dilatation of
cortical veins evaluated by SWI disappeared after treat-
ment, 15O positron emission tomography scanning
showed gradual improvement of cerebral blood flow
where the dilatation of cortical veins was seen, showing
that SWI could detect impaired cerebral hemodynamics
in CVST [11]. Venous stasis on SWI is also reported in
acute arterial ischemic stroke, suggesting misery perfu-
sion state, and venous stasis vanished after treatment
[8]. Continuous stasis of cerebral veins suggests brain
tissue damage as in the 3% cases with cerebrovascular
complications. Therefore, SWI could play an important
role giving us information about cerebral venous stasis
and impaired hemodynamic status related to cerebro-
vascular complications.
Venous Stasis and CVST
The second finding is that cerebrovascular complica-
tions were frequently observed in CVST patients who de-
veloped seizures. Seizures are frequent symptoms of
CVST, and it is reported that 34–44.3% of patients may
have seizures in the early stage of the disease [13, 14]. The
deficit, supratentorial parenchymal lesion on MRI, and
are independent predictors of early epileptic seizures [14–
tallic ions found in whole blood could induce neuro-
chemical alterations and be a cause of epilepsy [17].
Hence, it is important to pay attention to the develop-
ment of cerebrovascular complications in CVST patients
with seizures.
This study has several limitations. First, CVST is a rare
disease, so only 8 patients could be enrolled in this study;
results from such a small sample may be misleading. This
couraged to include more cases in the future. The retro-
third limitation is that, when evaluating venous stasis on
er there was prominence, so that the evaluators of venous
prominences could not be blinded and the score was fi-
nally determined by discussion of the 2 evaluators. The
evaluation had high value of kappa coefficient, though the
definition of venous stasis must become subjective and
qualitative. Especially in young patients, venous promi-
nences on SWI were sometimes seen in the whole brain
and were much more remarkable than in elderly patients,
so that it was difficult to distinguish them from the normal
venous pattern in young patients and the operational def-
inition of venous prominence was difficult to determine.
In this study, only local venous prominence on SWI was
considered positive, and whole brain venous prominence
was not judged positive. The ability of SWI to distinguish
normal venous structures and abnormal congested veins
should ideally be evaluated in a larger study including a
control group of patients [18]. The final limitation is that
hemodynamic loads by the thrombus and collaterals were
not directly evaluated at the same time as SWI evaluation.
We hypothesize that the venous stasis evaluated by SWI
are showing hemodynamic loads including collaterals,
though the golden standard to detect detailed information
of the cerebral hemodynamic state is digital subtraction
angiography. In order to evaluate hemodynamic loads by
the thrombus and collaterals directly and accurately, we
should have performed digital subtraction angiography at
the same time as SWI evaluation.
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 In conclusion, venous stasis is a factor related to cere-
brovascular complications, and evaluation of cerebral ve-
nous stasis by SWI can help predict cerebrovascular com-
plications following CVST. Seizure is an important initial
symptom suggesting cerebrovascular complications in
patients with CVST.
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