Download INTRACRANIAL VENOUS THROMBOSIS: IMAGING SIGNS AND

1
Revista Chilena de Radiología. Vol. 16 N 4, Año 2010; 175-187.
INTRACRANIAL VENOUS THROMBOSIS: IMAGING SIGNS AND COMMON
PITFALLS
Drs. Michael Hirsch S1, Alejandra Torres G2.
1
Radiology Resident, Hospital Clínico Universidad de Chile.
2
Neuroradiologist, Hospital Clínico Universidad de Chile.
Corresponding Author:
Michael Hirsch S.
Postal Address: Av. Santos Dumont #999. Independencia, Santiago.
Phone: 9789191
E-mail: [email protected]
Abstract
Although intracranial venous thrombosis is a relatively rare disease, it
constitutes an entity that must be timely and accurately diagnosed in
emergency services, given the need for prompt treatment to avoid serious
complications, including neurological deficits or even death. There are several
imaging signs that can be visualized on both computed tomography (CT) and
magnetic resonance (MR) imaging scans that allow for this early diagnosis. On
the other hand, some differential diagnoses need to be performed to prevent
mistaking intracranial venous thrombosis for any other entity.
2
Key words: Cranial Sinuses; Sinus Thrombosis, Intracranial; Tomography,
Spiral Computed Tomography; Magnetic Resonance Imaging; Radiology.
Introduction
Intracranial venous thrombosis (IVT) is a cerebrovascular condition that may
affect all ages, occurring predominantly in infants and in adults around the third
decade of life
(1,2)
. It may include cerebral veins (CV) as well as dural venous
sinuses (DVS). There are over a hundred causes described as etiopathogenic
factor of IVT (Table I)
(1)
, summarized in the classic “Virchow's triad” which
encompasses states of hypercoagulability, vessel wall damage and disturbance
of venous flow
(3)
. However, the causal factor of IVT may be found only in 75 to
85% of patients, even though when all available examinations and laboratory
tests are performed (1, 4).
By reviewing the clinical presentation of IVT, a wide range of symptoms and
signs, ranging from headache and intracranial hypertension to coma and even
death, may be observed (Table II). Headache is the most commonly
encountered symptom─seen in 75 to 95% of patients with IVT─, usually
preceding by days, weeks or exceptionally months
(2,5)
the manifestation of
other neurological disorders (70-75%). Headache has been associated with
manifestations of intracranial hypertension in 20 to 40% of cases
mild, moderate, or severe in intensity, and predominantly diffuse
(2)
; it can be
(2)
. Given the
variability and nonspecificity of presenting symptoms of the IVT, an imaging
diagnostic technique is essential to understand the etiology of symptoms,
mainly because an early diagnosis allows the implementation of a timely
anticoagulant therapy, thus reducing the rate of complications and neurological
sequelae.
3
Table I. Causes and risk factors
associated with
intracranial venous thrombosis.
Prothrombotic genetic conditions
Antithrombin deficiency
Protein C and S deficiency
Factor V-Leiden mutation
Prothrombin mutations
Homocysteinemia caused by mutations in the
methyltetrahydrofolate reductase gene.
Acquired prothrombotic conditions
Nephrotic sindrome
Antiphospholipid antibodies
Homocysteinemia
Pregnancy
Puerperium
Infections
Otitis, mastoiditis, sinusitis
Meningitis
Systemic infectious disease
Inflammatory diseases
Systemic lupus erythematosus
Wegener’s granulomatosis
Sarcoidosis
Inflammatory bowel disease
Behçet’s syndrome
Hematologic conditions
Polycythemia, primary and secondary
Thrombocythemia
Leukemia
Anemia, including paroxysmal nocturnal hemoglobinuria
Drugs
Oral contraceptives
Asparaginase
Mechanical/ traumatic causes
Head trauma
Injury to sinuses or jugular vein, jugular catheterization
Neurosurgical procedures
Lumbar puncture
Miscellaneous
Dehydration, especially in children
Cancer
4
Table II. Clinical features of intracranial venous
thrombosis
Symptoms
Headache
Visual disturbances
Impairment of consciousness
Nausea, vomiting
Signs
Papilledema
Focal neurological deficit
Cranial nerve palsies
Convulsions, coma
Imaging aspects
There are several imaging findings that allow us to suspect or make the
diagnosis of IVT, both on computed tomography and magnetic resonance
imaging scannings:
A) Signs of vein occlusion
B) Parenchymal alterations and other changes secondary to venous stasis
C) Signs of recanalization.
Each of them will be discussed.
A) Signs of venous occlusion
1) The Empty Delta Sign
This finding was originally described on CT cuts with intravenous contrast
agent; it corresponds to a triangular and hypodense filling defect associated
with a hyperdense peripheral area, which is produced by contrast material
enhancement in the thrombosed superior sagittal sinus (SSS) (Figure 1)
(3.6)
.
Currently, it is possible to observe the empty delta sign not only in the SSS, but
also in the transverse (TS) and sigmoid sinuses (SS) on multiplanar
5
reconstructions from multidetector CT, as well as on contrast-enhanced MR
imaging studies.
Figure 1. Contrast enhanced CT sequence (a, b) where empty delta sign in superior sagittal
sinus at various levels is identified in the same patient
DVS exhibit an elongated and triangular shape in cross section; they are
valveless structures with a plexus of adjacent venous channels that act as a
collateral pathway for drainage in the event of thrombosis (Figure 2) (7).
Numerous hypotheses intended to explain the appearance of this sign have
been formulated, including:

Recanalization of the thrombus within the venous sinus

Organization of the blood clot

Blood-brain barrier breakdown
6

Dilatation of collateral peridural and dural venous channels.
Seemingly, the latter would be the most likely explanation since contrastenhancement of dural venous collateral circulation─primarily consisting of
lateral lacunae, vascular mesh (dural cavernous spaces), and meningeal
venous tributaries─would produce the empty delta sign in the thrombosed sinus
(3, 6, 7)
.
In up to 90% of cases the location of thrombosis involves more than one sinus,
particularly the ST and SS, collectively termed as lateral sinus. (Table III) (4, 8, 9).
Figure 2. Coronal sections of an anatomical preparation. a) Identifies the superior sagittal sinus
(S) formed by the divergence of the periosteal and meningeal layers of the dura mater. The
latter converge at the falx cerebri (H). Around the sinus there is a collateral venous plexus
(asterisks). b) In the transverse sinus (TS) the meningeal layers of the dura mater converge at
the tentorium (T), also giving it a triangular appearance. Calotte (C), cerebellum (Ce).
7
Table III.
%
Thrombus location
Superior sagittal sinus
62.0
Left lateral sinus
44.7
Right lateral sinus
41.2
Straight sinus
18.0
Cortical veins
17.1
Deep venous system
10.9
Cerebellar veins
0.3
Late-phase contrast-enhanced CT scans have proved to be a reliable method to
investigate
the
cerebral
venous
structures
(especially
by
multiplanar
reformatting), with a sensitivity of 95% when compared with angiography, as
reported in several publications
(10)
. This capability allows a high performance,
thus avoiding the inherent risks of the interventional procedure.
The empty delta sign is observed in 25 to 75% of cases of DVS thrombosis,
depending on the different techniques applied. Ideally, it has to be detected by
means of multiplanar reformation at different spatial planes, especially in the
SSS and TS horizontal portions (Figure 3) by using wider window settings than
those normally used for brain parenchyma, with a window width of 260 HU and
a level of 130 HU (Figure 4)
(5)
. It should be noted that the empty delta sign may
disappear in the chronic stages due to enhancement of organized clot
(5)
.
8
Figure 3. Coronal plane reformation Contrast-enhanced CT. The empty delta sign in the right
transverse sinus is identified; to compare with contralateral sinus.
9
Figure 4. Contrast-enhanced CT. A small thrombus in the superior sagittal sinus can be
observed only by changing window width and window level.
2) The hyperdense sinus sign and the cord sign
In 20% of cases the clot can be seen in its early stages at the level of the DVS
(6)
as a hyperdense image on non-contrast-enhanced CT scans (Figure 5, 6a,
7a), since the thrombus retracts and its water content decreases while the
concentration of hemoglobin increases, thus achieving an attenuation value of
50-80 HU, which normalizes within 1-2 weeks’ time
(11).
The tentorium and
beam hardening artifacts caused by bones may obscure this finding or it may be
confused with a subarachnoid hemorrhage, an underlying subdural hematoma,
or it can be caused by a high hematocrit (11).
The cord sign corresponds to the same principle as that of the hyperdense
sinus, but applied to cortical veins (Figure 7a), which are rarely involved in
isolation in IVT (4).
3) Absence of flow void and hyperintense vein sign
On non-contrast MR images, vessels are usually hypointense on all sequences
due to its flow; this is called flow void sign, also known as "flow void." When this
flow-void is absent, vessels become hyperintense, which may be indicative of
thrombosis (Figures 6c, 8a); nevertheless, a slow or turbulent flow can cause
changes in DVS signal intensity, thus leading to misdiagnosis
(4)
. Moreover, the
various states of hemoglobin degradation may alter the appearance of the
thrombus and make it less obvious, mimicking the typically observed absence
of flow void signal
(12,13)
. For example, deoxyhemoglobin will cause the acute
thrombus to appear as a very hypointense area on T2-weighted sequences
(Figure 9), mimicking the normal flow void, and isointense on T1-weighted
sequences, resembling the adjacent brain parenchyma, so that it may go
unnoticed unless a contrast medium is used. The presence of the empty delta
sign will facilitate the right diagnosis (Figure 8b)
(4)
. Something similar occurs on
non-contrast enhanced TOF angiographic sequences in which the subacute
10
thrombus composed of methemoglobin is hyperintense, resembling the signal
intensity that flow normally exhibits on this view. Performance of T1-weighted
SE sequences allows discrimination between the hyperintense thrombus and
the normal absence of flow void sign
(4)
; on the other hand, 3D-contrast-
enhanced MR angiographic sequences with improved spatial resolution and
visualization of filling defects of the venous system have increased sensitivity
and specificity levels in comparison with unenhanced TOF sequences. Among
these are, for example, the FLASH sequence (fast low-angle shot) and ATECO
(auto-triggered elliptic centric-ordered) view (Figures 7f, 10) (14 - 17).
11
Figure 5. CT scan without contrast. a) The superior sagittal sinus is hyperdense. b) In a cut at a
superior level than the preceeding one, this finding disappears, which supports the diagnosis of
thrombosis. Note that the great cerebral vein (vein of Galen) does appear hyperdense in this
cut.
12
13
Figure 6. a) Unenhanced CT scan showing hyperdense right transverse sinus, associated with
temporal lobe hematoma, surrounded by scarce vasogenic edema. b) After contrast
administration and at a more superior cut, absence of filling of the transverse sinus is shown
and the hematoma is best viewed. c) T1 MRI sequence shows the absence of normal flow void
at the level of the lateral sinus and signal intensity changes caused by degradation of
hemoglobin in the hematoma, as visualized on T2 d) and GRE T2 * sequences, e) appearing on
the latter the magnification of the magnetic susceptibility artifact.
The hyperintense vein sign is similar to the cord sign observed on CT scanning
(Figure 11) and corresponds to the absence of flow void in the cortical veins,
visualized on T1 and T2 MRI sequences, with the exception of visible signal
hypointensity caused by the hemoglobin degradation process (Figure 7c) (4).
The above data demonstrate the importance of being aware of MRI appearance
at the various stages of hemoglobin degradation process, a common issue in
general radiologists training but outside the scope of this review.
4) Magnetic susceptibility artifact
Lately, there has been much emphasis on T2*-weighted gradient-echo (GRE)
sequences (18) due to its capability to highlight the magnetic susceptibility artifact
produced by the paramagnetic states of hemoglobin degradation, such as
deoxyhemoglobin, methemoglobin, and hemosiderin. These elements are seen
as hypointense images generating the "blooming" phenomenon, effect that
corresponds to an amplification of their actual area of deposition produced by
the magnification of the artifact on this sequence (Figure 6 and 7). This allows
to detect thrombosis in small-caliber veins, such as the cortex veins (Figure 12),
or to make thrombosis evident, when there are only subtle changes in signal
intensity on classic T1- and T2-weighted sequences
(4)
. There is a 3D- GRE
sequence technique with post-processing phase and high spatial resolution
referred to as “susceptibility-weighted imaging” (SWI), which amplifies the
above described phenomenon and several studies have shown it to be superior
to conventional techniques (19, 20).
14
15
16
17
Figure 7. SSS thrombosis and left frontal cortical vein thrombosis; unenhanced CT image
shows the hyperdense sinus sign and the cord sign a). MRI view shows magnetic susceptibility
artifact with "blooming" effect on T2* GRE sequence b), which is not evident on the T2
sequence c). Involvement of brain parenchyma causing slight cortical hyperintensity on T2
sequence d) and restriction of proton mobility represented on DWI sequence e) and ADC map
f). Cortical vein thrombosis is associated with thrombosis of SVD; in the case of SSS thrombosis
it is represented in the ATECO sequence g). In a control at 5 months, no changes on T2 h),
DWI i), or ADC map j) are observed and on an ATECO sequence, recanalization of the SSS is
shown k).
18
B) Parenchymal alterations and other changes secondary to venous
stasis
Changes in the brain parenchyma may be observed in 50 to 57% of IVT
patients
(4, 21)
, especially on MRI sequences. Varying in degree, type of
alteration and time reversibility, they can be divided into manifestations
secondary to vasogenic edema, secondary to the restriction of proton mobility
on diffusion-weighted sequences (DWI) with cytotoxic edema-like pattern, and
hemorrhagic manifestations (4).
The primary underlying mechanism for these parenchymal abnormalities is an
increased venous pressure secondary to obstruction of venous drainage that
can lead to an increase in caliber or number of visible veins, particularly on MRI
and / or meningeal enhancement due to venous congestion
(5)
. If collateral
pathways of venous drainage are insufficient, which is especially evident in
cortical venous thrombosis, a vasogenic edema in the adjacent parenchyma
begins to be formed. If venous pressure continues to increase, a corresponding
reduction of arterial perfusion pressure may be expected and a cytotoxic edema
and cell death may occur. If adequate collateral pathways develop or
recanalization occurs before cell death or intracranial hemorrhage, parenchymal
abnormalities can be partially or completely resolved. Clearly, this is not a linear
process and vasogenic edema and cytotoxic edema pattern can often coexist,
(4); some authors have found evidence of cytotoxic edema early after the
development of an IVT, so its exact pathophysiology remains controversial (21).
Brain edema, which on CT scans is seen as hypodense areas or loss of
differentiation between gray and white matter, can be better characterized by
MRI sequences, using DWI and T2 FLAIR images. In this way we can
differentiate an alteration of parenchymal signal intensity with hyperintensity on
DWI sequence and restriction of proton mobility in the apparent attenuation
coefficient (ADC) map, similar to the cytotoxic edema seen in the arterial
ischemia, but that in venous thrombosis is highly likely to reverse in time, which
lead us to assert that it does not correspond exactly to the same phenomenon,
19
or that it may constitute a reversible stage of this effect (Figure 7)
(21-23)
. This
difference in behaviour when compared to blood cytotoxic edema makes it
advisable not to use the term "venous infarction" to refer to this type of
parenchymal lesion, since it does not reflect the potential reversibility of the
damage
(4)
; in this context, it seems to be more appropriate to speak of venous
ischemia. Some authors have correlated the degree of restriction of protons
mobility with a potential irreversibility when the mobility coefficient in the ADC
mapping is less than 0.20 x10-5 cm2 /s
(23)
, but this finding has not been
documented in other studies (25).
On the other hand, vasogenic edema shows hyperintensity on T2-weighted MRI
sequences and hypointensity on T1- weighted MRI images, with a tendency to
respect the cortex; it shows no restriction on ADC map and usually is not
hyperintense on diffusion-weighted imaging, unless it represents an artefactual
image due to T2 effects (Figure 11), commonly associated with an increase of
mass effect due to increased water content in the area involved. The vasogenic
edema is one of the most commonly encountered parenchymal abnormalities in
IVT patients, closely related to pathophysiological events triggered after
intracranial venous thrombosis. When capillary fluid pressure increases, it may
cross the blood brain barrier resulting in early and wide-spread vasogenic
edema, which may constitute the predominant disturbance, reaching up to one
third of the cases, as reported by some studies (22, 25).
Increase in parenchymal volume without attenuation or signal intensity
alterations can be found in up to 42% of IVT cases, possibly as a reflection of
the capillary venous congestion, with effacement of sulci, decrease in the width
of the cisterns as well as in the size of the ventricular system (4, 24).
Up to one third of the IVT may show signs of intracranial hemorrhage and T2 *weighted sequences are especially useful for detecting them
(4)
; depending on
the state of the hemoglobin, diverse areas of signal intensity alteration may be
found in the hematoma (Figure 6). Venous thrombosis should always be viewed
as a cause of benign-appearing hematoma, in absence of any other apparent
cause (arterial hypertension, vascular malformation, etc.); the search for the
signs already described is essential to suggest or confirm its etiology.
20
In TVI, subarachnoid hemorrhage is occasionally found, a finding scarcely
reported in the literature despite its common occurrence in lumbar puncture
studies. Ruling out cases that include intraparenchymal hematomas with some
degree of leakage into the subarachnoid space, there are some publications
that have correlated subarachnoid hemorrhage with cortical venous thrombosis
more often than with dural venous sinus thrombosis
(25, 26)
; it has also been
described as a rare initial presentation of cortical venous thrombosis, so it is
necessary to consider this diagnosis within the spectrum of causes of
nonaneurysmal subarachnoid hemorrhage
(26)
.
C) Signs of recanalization
When IVT begins to recanalize, multiple intrasinus channels and dural collateral
vessels may be observed, mainly on MR venographic projections (Figure 7k,
13). Several studies have demonstrated the usefulness of anticoagulant and
thrombolytic therapies for achieving patient recovery and reducing mortality
rates as well as serious sequelae in IVT patients
(2)
recanalization is not required for clinical recovery
; nevertheless, a complete
(27)
and it is not directly
correlated with the extent of recanalization, apparently due to the presence of
collateral veins that would help to improve drainage of the areas involved
(4)
. As
for time of recanalization, it has been shown that the majority of recanalizations
occurs before 6 months and that there is no difference in recanalization rates
between controls at 3 months and after 6 months (28, 29).
21
Figure 8. a) T1-weighted MRI without contrast shows absence of flow void in the superior
sagittal sinus. Compare with cerebral vein (vein of Galen) b). Thrombosis was confirmed in the
sequence with contrast.
22
Figure 9. T2-weighted MRI a) and T1 with contrast sequences b). Note the superior sagittal
sinus hypointense on T2, which may suggest a normal flow void; however, after contrast
administration the empty delta sign is observed.
23
Figure 10. ATECO MR sequence in coronal plane shows left transverse sinus thrombosis.
Figure 11. Coronal T2 FLAIR sequence shows hyperintense vein sign in a left parietal cortical
vein and partial absence of flow void of ipsilateral transverse sinus, with involvement of the
temporal lobe, predominantly at the level of subcortical white matter, with the appearance of
vasogenic edema.
24
Figure 12. GRE T2 * sequence a) showing magnetic susceptibility artifact in the right superior
anastomotic vein (vein of Trolard), without visualization on 3D venographic sequence b).
25
Figure 13. ATECO MR sequence shows lateral sinus thrombosis with partial recanalization.
Common pitfalls
Anatomical variations at the confluence of the sinuses are common (Figure 14)
(30)
and may result in false positives. A 49% of asymmetric TS has been
described, with partial or complete absence in up to 20%
(4)
, which can produce
artifacts due to slow, fast or turbulent flow on MRI sequences, even on ATECO
MR angiographic sequences, giving the false impression of thrombosis.
26
The asymmetrical bifurcation of the confluence of the sinuses, or at a superior
level, may cause a triangular image called "the pseudo empty delta” sign
(Figure 15)
scans
(4, 31)
, which has been visualized in 18% of contrast-enhanced CT
(32)
. This error can be avoided by exploring the entire route of the sinuses
and documenting the density of this pseudodefect, which has the same
attenuation (on CT) or signal intensity (on MRI) as that of the subarachnoid
CSF.
The presence of hypodense collections (such as abscesses) in the epidural
space adjacent to the sinuses has been described as a possible cause of a
"pseudo empty delta" sign
(31)
. Fenestrations or septa within dural sinus are also
mentioned as causes of a false positive diagnosis (33).
Arachnoid granulations (Figure 16) are identified in 24% of contrast-enhanced
CT scans
(34)
, usually in the SSS and the TS, specifically in the lateral aspect
(Figures 17,18) near the entrance of superficial veins such as the inferior
anastomotic vein (vein of Labbé)
(4)
, although they are also found in the
cavernous, superior petrosal, and straight sinuses, in descending order of
frequency
(5)
. Arachnoid granulations can protrude directly into the sinus lumen,
thus resulting in a potential false positive for the empty delta sign
(5)
. One way to
identify them is by their rounded shape that produces a focal filling defect, with
the same attenuation as that of the subarachnoid CSF (on CT) or the same
signal intensity (on MRI) (4).
27
Figure 14. Diagram of coronal view of the anatomical variations found at the confluence of the
sinuses (Retrieved from Reference 30). a) Confluent: 35%, b) Bifurcation: 14%, c) left
Dominance: 10%, d) right Dominance: 40%. In the last two types we have observed that the
nondominant side flow mainly comes from a division of the straight sinus.
28
Figure 15. Sign of the "pseudo empty delta." a) contrast-enhanced CT view with triangular
image posterior to the confluence of the sinuses, which can be misinterpreted as thrombosis. b)
In the phase without contrast no hyperdense image can be seen. c) Reconstruction in the
coronal plane shows the bifurcated configuration that the confluence of the sinuses exhibits.
29
Figure 16. Coronal section of an anatomical preparation in which an arachnoid granulation
(asterisk) in the transverse sinus (TS) is identified.
30
31
Figure 17. CT sequence at the level of transverse sinuses. a) filling defects consistent with
arachnoid granulations are identified b) Compare the defect density with the sinus on noncontrast phase. c) The reconstruction in the coronal plane also helps to evaluate the defect.
Figure 18. MR ATECO sequence. a) In the coronal plane, arachnoid granulations in the SSS
are observed. b) In the same patient, arachnoid granulations in the transverse sinus are seen.
32
Final Comment
While the venous-phase angiography with digital subtraction imaging technique
remains to be the "gold standard" for diagnosis of IVT─an invasive and risky
method─, the possibility of making an accurate diagnosis by noninvasive
methods, such as CT or MRI studies, has been considered. As already
discused, these techniques reveal several signs that allow a proper diagnosis of
IVT. For instance, the empty delta sign described on contrast-enhanced CT
scans as well as on MRI sequences is a sign widely known for imaging
specialists; nevertheless, the "false positives" that this sign may originate
(anatomic variants, arachnoidal granulations or slow flow on MRI) or some
conditions that may mimic a "false negative" result (such as the chronic
development of a thrombus on CT and MRI sequences) not always are properly
recognized.
Another relevant issue that radiologists must be acquainted with is the
sensitivity and specificity of imaging methods, the use of contrast materials,
along with the noninvasive angiographic techniques that yield the highest
diagnostic performance in identifying IVT. It is our task to be fully familiar with all
these imaging techniques in order to make accurate and timely diagnoses to
provide the most appropriate treatment to patients presenting IVT
to
protect
misdiagnosed
patients
against
unnecessary
(5)
as well as
exposure
to
anticoagulant therapy with it inherent risks. Likewise, if we are able to recognize
the existence of venous thrombosis on CT and MRI studies, we can spare
patients with hematoma from undergoing conventional angiography.
In summary, adequate knowledge of signs favouring an accurate imaging
diagnosis of IVT as well as of pitfalls arising from artifacts, physiological and
anatomical variants, constitute issues to be mastered by radiologists.
33
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