Intracranial Venous Thrombosis: Imaging Signs and Common

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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.

1Radiology Resident, Hospital Clínico Universidad de Chile.

2Neuroradiologist, 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 (2); it can be mild, moderate, or severe in intensity, and predominantly diffuse (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.

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 contrast- enhancement 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).

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).

Figure 3. Coronal plane reformation Contrast-enhanced CT. The empty delta sign in the right transverse sinus is identified; to compare with contralateral sinus.

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).

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.

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

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); nevertheless, a complete recanalization is not required for clinical recovery (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.

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.

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).

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) (4, 31), which has been visualized in 18% of contrast-enhanced CT scans (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).

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.

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.

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 non- contrast 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.

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 (5) as well as to protect misdiagnosed patients against unnecessary 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.

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