Radiologic Diagnosis of Cerebral Venous Thrombosis: Pictorial Review

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1 JR Integrative Imaging LIFELONG LERNING FOR RDIOLOGY Radiologic Diagnosis of erebral Venous Thrombosis: Pictorial Review olin S. Poon 1,2, Ja-Kwei hang 1, mar Swarnkar 1, Michele H. Johnson 2, John Wasenko 1 Objective erebral venous thrombosis is often associated with nonspecific clinical complaints. In addition, the imaging findings are often subtle. Underdiagnosis or misdiagnosis of cerebral venous thrombosis can lead to severe consequences, including hemorrhagic infarction and death. onclusion This article reviews the radiologic findings and diagnostic pitfalls of cerebral venous thrombosis. fter completing this article, the readers should have an improved ability to diagnose cerebral venous thrombosis accurately, using the optimal imaging tools to achieve this goal. Introduction erebral venous thrombosis (VT) is often underdiagnosed because it is an uncommon disease, it is associated with a wide spectrum of etiologic factors, clinical presentation is often nonspecific, and the diagnostic imaging features can be subtle. The correct diagnosis of VT relies on neurologic imaging. Radiologists play a crucial role in patient care by providing early diagnosis through interpretation of imaging studies. Early diagnosis leads to prompt treatment that can be effective. Delayed diagnosis is associated with high morbidity and mortality. The purpose of this article is to review the clinical presentation and basic pathophysiology of the disease; review the approach for radiologic investigation, including emerging technology such as T venography; review the imaging features of VT; and show common pitfalls associated with the radiologic evaluation of this diagnosis. We have included many cases to illustrate the radiologic features of VT. Whenever possible, findings on different imaging techniques are correlated and compared. Predisposing Factors The list of factors associated with VT is too extensive to be memorized [1 7]. more manageable approach is to understand that they may involve one or more of the following mechanisms: direct involvement of the dural sinuses (e.g., infection, trauma, neoplastic infiltration), possibly with damage to the vascular endothelium; venous stasis; hypercoagulable states; and increased blood viscosity. The frequency of these etiologic factors depends on age. Often, the cause is multifactorial. In neonates, acute systemic illness, such as shock or dehydration, may be the cause. Frequent causes in older children include local infection, such as mastoiditis, and coagulopathy. In adults, intrinsic or acquired coagulopathies become the most important factors, contributing to as many as 70% of cases. Infection contributes to less than 10% of cases in adults [1, 3]. In women of childbearing age, oral contraceptive use and pregnancy are strong risk factors. VT actually occurs more often in puerperium than during the pregnancy. lthough pregnancy-related VT occurs more often in older women, age per se is not a risk factor. The pathogenesis of VT is complex and remains poorly understood. In 20 35% of cases, the cause remains unknown; therefore, one should remain suspicious, even in the absence of known risk factors [1 3]. linical Presentation The clinical presentation of VT is often nonspecific [1 6] (Table 1). ommon presentation includes headache, focal neurologic deficits, seizures, and altered consciousness. syndrome of intracranial hypertension (headache and papilledema) accounted for 40% of cases in a series, so VT needs to be excluded in patients considered for the diagnosis of benign intracranial hypertension [1]. lthough subarachnoid hemorrhage is a rare presentation of VT, cases have also been reported [1, 8]. There is also a wide distribution in the mode of onset of symptoms, with approximately 28% acute (< 48 hours), 42% subacute (between 48 hours and 30 days), and 30% chronic (> 30 days) [1]. The teaching point is that VT may have an atypical presentation or even an absence of clinical symptoms. The evaluation for evidence of VT should be included in the diagnostic checklist in every neuroradiologic case. Keywords: brain imaging, cerebral venous thrombosis, T, MRI, neuroradiology DOI: /JR Received May 31, 2007; accepted after revision June 11, Department of Radiology, State University of New York Upstate Medical University, 750 E dams St., Syracuse, NY ddress correspondence to. S. Poon (poonc@upstate.edu). 2 Department of Diagnostic Radiology, Yale University School of Medicine, New Haven, T. JR 2007;189:S64 S X/07/1886 S64 merican Roentgen Ray Society S64 JR:189, December 2007

2 erebral Venous Thrombosis D Fig. 1 5-year-old boy with severe headache and eye pain. Thrombosis was found in right lateral sinus (arrows). and, Unenhanced T images show thrombosis as hyperdensity (dense clot sign). and D, Enhanced T images show same structure as filling defect with enhancing rim (empty delta sign). Fig. 2 ord sign in cortical venous thrombosis in a young woman. and, Unenhanced T scans show dense cortical veins (white arrows, ), an uncommon direct sign of cerebral venous thrombosis (VT) known as cord sign. Note also indirect signs of VT, including subcortical hemorrhagic infarction (black arrows), diffuse brain swelling, and small ventricular size. JR:189, December 2007 S65

3 Poon et al. Neuroradiology Unenhanced T remains the technique of choice for screening patients with nonspecific clinical presentation and a low suspicion of VT. ontrast-enhanced T provides a more accurate diagnosis of VT. MRI and MR venography have been the noninvasive imaging techniques of choice [4 6, 9] and are often used as the initial diagnostic test for suspicious cases. T venography is now emerging as a competing technique. It has been shown to be comparable to MR venography and, in some situations, to provide better diagnostic information [10]. D Fig year-old woman with history of pseudotumor cerebri who presented with headache and decreased consciousness. Diagnosis was thrombosis of superior sagittal sinus, straight sinus, and internal cerebral veins. (Long white arrows indicate superior sagittal sinus; short white arrows, straight sinus; black arrows, Rosenthal s veins). and, Unenhanced T scans show dense thrombosis. Note nonhemorrhagic infarction in basal ganglia, thalami, and internal capsules, which is typically seen in deep cerebral venous thrombosis., xial T2-weighted MR image shows replacement of signal void by thrombus (arrow) in superior sagittal sinus. Veins at internal capsules are engorged. D and E, Sagittal contrast-enhanced T1-weighted image (D) shows filling defects in sagittal and straight sinuses, correlating with absence of flow on 2D phase contrast MR venography (E). F, fter catheter-directed thrombolysis, flow was partially reestablished. E Unenhanced T Direct signs of VT are uncommon and are seen in only one third of cases. Direct visualization of thrombosis in dural sinus may give a dense clot sign (Fig. 1). The cord sign represents direct visualization of a thrombosed cortical vein that is seen as linear hyperdensity (Fig. 2). More often, unenhanced T shows only the indirect signs of VT. These are often nonspecific and may include diffuse brain edema, leading to hypodensity of the brain (seen in 20 50% of cases) or decreased ventricular size. In young patients, the pathologic decrease in ventricular size may be difficult to differentiate from the normally small ventricles commonly seen in young patients. Venous infarction is the most specific indirect sign on unenhanced T images. n infarction not conforming to a major arterial vascular territory, such as the presence of multiple isolated lesions, involvement of a subcortical region with sparing of the cortex, and extension over more than one arterial distri- F S66 JR:189, December 2007

4 erebral Venous Thrombosis bution, is highly suspicious for a venous cause. The infarction may be hemorrhagic (Fig. 2) or nonhemorrhagic (Fig. 3). The location of the infarction with respect to the expected course of venous drainage may give a clue to the venous structure involved. Thrombosis in the sagittal sinus often leads to impaired venous drainage and, therefore, parenchymal change in the parasagittal region. Thrombosis in Labbé s vein should lead to infarction in the temporal lobe. ilateral or unilateral infarction in the thalami, basal ganglia, and internal capsule is typically seen in deep venous thrombosis (Fig. 3). D E F Fig year-old girl with multiple traumatic injuries in head. Initial unenhanced T (not shown) showed hyperdensity in right internal jugular vein (IJV) and sigmoid sinus that was suspicious for venous thrombosis. Findings were confirmed on T venography, MRI, and conventional venography. and, xial source images from T venography. Thrombus in IJV (asterisk, ) and sigmoid sinus (black arrow, ) is clearly shown as filling defect. Note collateral veins (white arrow, ) arising from right IJV., Sagittal planar reconstruction of T venography shows thrombus extending from right IJV (asterisk) into sigmoid sinus (arrow), correlating well with findings on conventional venography (E). D, T1-weighted MR image shows sigmoid sinus thrombosis (arrow) as seen on T (). E and F, Venogram (E) shows thrombus as filling defects. Note collateral veins at region of right IJVs, also seen in. Venogram after suction thrombectomy (F) shows improved patency in right IJV and lateral sinus. sterisk, right internal jugular vein; solid arrow, sigmoid sinus; open arrow, torcular Herophili. the dural sinus, with peripheral enhancement possibly secondary to the development of collaterals (Fig. 1). Indirect evidence of VT may be seen as contrast enhancement of the falx and tentorium secondary to venous stasis and hyperemia of the dura mater, which is seen in approximately 20% of cases. One should be aware that in 10 30% of cases of VT, the findings on either unenhanced or contrast-enhanced T are negative. Therefore, in highly suspicious cases, further evaluation with T venography, or MRI with MR venography, is warranted. ontrast-enhanced T Direct evidence of VT on contrast-enhanced T includes the empty delta sign, which may be seen 5 days to 2 months from onset. This sign represents a filling defect (thrombus) in T Venography more recent tool that can be used to evaluate VT is T venography [10 12]. T venography allows direct visualization of thrombus as filling defects (Fig. 4). JR:189, December 2007 S67

5 Poon et al. MRI On MRI, venous thrombus may be directly visualized. On conventional MRI sequences, patent dural sinuses are often seen as a flow void. This is particularly well seen when the imaging plane is orthogonal to the blood flow direction (e.g., coronal images are best for visualization of the superior sagittal, transverse, and sigmoid sinuses). The effect of a flow void may be reduced in a plane parallel to the dural sinus, although such an imaging plane often offers a better depiction of the complete extent of thrombosis in the dural sinus. For example, a sagittal T1-weighted image may show the complete extent of the superior sagittal sinus thrombosis as an abnormally bright signal filling the sinus. The thrombus may manifest as absence of a flow void, which is often best seen on FLIR images and T2-weighted spin-echo images. The abnormal signal intensity follows the signal characteristics of intracranial hemorrhage and may evolve through the stages of oxyhemoglobin, deoxyhemoglobin, methemoglobin, and hemosiderin [4]. On T1-weighted images, thrombus Fig. 5 4-day-old neonatal boy after idiopathic cardiac arrest. and, xial unenhanced T scans show normal, hyperdense blood commonly seen in neonates and infants. and D, T1- () and T2-weighted (D) MR images show normal findings. TLE 1: Signs and Symptoms of erebral Venous Thrombosis Presentation Frequency (%) Headache 75 Papilledema 49 Seizures 37 Motor or sensory deficit 34 Mental status changes 30 Dysphasia 12 ranial nerve palsies 12 erebellar incoordination 3 ilateral or alternating cortical signs 3 Nystagmus 2 Hearing loss 2 Note Percentages total > 100% because patients may have multiple presentations. dapted from [1]. D S68 JR:189, December 2007

6 erebral Venous Thrombosis with methemoglobin is seen as hyperintensity. On T2*-weighted gradient-echo images, exaggerated signal loss is often seen because of the increased susceptibility effect of deoxyhemoglobin, methemoglobin, or hemosiderin. Indirect evidence of venous thrombosis is often secondary to parenchymal change as a result of venous occlusion. This is similar to the findings on T, including brain swelling and hemorrhagic or nonhemorrhagic infarction. onventional MRI sequences often provide sufficient information to raise the suspicion or to make a diagnosis of VT. The diagnosis can then be further confirmed on MR venography or T venography. D E F Fig. 6 Middle-aged woman (exact age unknown) with history of multiple myeloma. and, xial unenhanced T images show subdural hemorrhage at right cerebellar convexity that mimics thrombosis of right transverse sinus. E, xial FLIR image (), coronal FLIR image (D), and unenhanced T scan (E) at location adjacent to show similar finding of subdural hemorrhage (white arrow, E) medial to right transverse sinus (black arrow, E). F, ontrast-enhanced MR venogram shows patent dural venous sinuses. Right transverse sinus (arrows) is smaller and slightly irregular compared with left, possibly secondary to mass effect from adjacent subdural hematoma. MR Venography MR venography may be performed without the use of a contrast agent using the time-of-flight (TOF) technique or the phase contrast technique. ecause these techniques use MR flow phenomena for contrast generation, they are subject to flow-related image artifacts. Similar to T venography, contrast-enhanced MR venography takes advantage of luminal filling by contrast material rather than relying on the MR flow phenomena as in TOF or phase contrast MR venography. Therefore, contrast-enhanced MR venography is less likely to be affected by complex flow. Recently, gadolinium-enhanced MR venography has been JR:189, December 2007 S69

7 Poon et al. shown to be superior to TOF MR venography [13, 14] and may offer the best evaluation using MRI. The various MR venography techniques are summarized in Table 2. omparison of MR Venography and T Venography comparison of T venography and MR venography is summarized in Table 3. D Fig. 7 7-year-old girl with closed head injury., Unenhanced T scans on first day show subdural hemorrhage along tentorium cerebelli and skull fracture. Subtle density is seen in right lateral sinus (arrows, and ) that was not well appreciated initially. D and E, On next day, repeat T scan shows dense thrombus in right lateral sinus (arrows) mimicking subdural hematoma (compare E with ). F and G, On sagittal T1-weighted MR images, normal flow void is seen in left lateral sinus (arrow, F), but note isodense thrombus on right (arrow, G). E T venography has been shown to be superior to traditional MR venography techniques based on 2D TOF or phase contrast techniques [10]. However, a direct comparison between T venography and contrast-enhanced MR venography is not yet available. These two techniques probably provide comparable performance, and preference will be dictated by the experience and resources of the individual institutions. F G S70 JR:189, December 2007

8 erebral Venous Thrombosis TLE 2: omparison of MR Venography Techniques Technique dvantages Disadvantages Time-of-flight Shorter imaging time More prone to false-positive results from in-plane flow False-negatives due to methemoglobin Phase contrast etter background suppression More sensitive to motion artifacts and turbulent flow an detect flow in all three orthogonal planes etter flow quantification No false-negatives due to methemoglobin Gadolinium-enhanced Less likely to give false-positives due to slow or complex flow Potential false-negatives due to methemoglobin a or enhancing chronic thrombosis a ut less likely than with time-of-flight. Fig. 8 4-month-old girl with seizure. and, Unenhanced T scans show subdural hemorrhage along falx and tentorium cerebelli, simulating sagittal and transverse sinus thrombosis. Note pseudo empty delta sign (arrow, ). Empty delta sign of cerebral venous thrombosis is applicable only on contrast-enhanced T. Hyperdensity along posterior parietal convexity simulates transverse sinus thrombosis (black arrow, ). Extension of hyperdensity beyond expected location of transverse sinus suggests this is actually subdural hematoma (white arrow, ) [8]. Fig year-old woman woman with headache., ontrast-enhanced T1-weighted image (), source image of 2D time-of-flight (TOF) MR venography (), and maximum-intensity-projection of 2D TOF MR venography image () show fenestration of straight sinus (arrow). On basis of alone, sinus thrombosis is difficult to exclude. However, other imaging series, including unenhanced T1-weighted and FLIR images (not shown), fail to show abnormal signal intensity to suggest presence of a true thrombus, raising suspicion that this may have another cause. Two-dimensional TOF MR venogram () shows fenestration. Note small vessels representing fenestration are round and positioned on opposite sides of expected course of straight sinus. This appearance is unusual for residual patent lumen of dural venous sinus filled with thrombus because residual lumen tends to be irregular or crescent-shaped. JR:189, December 2007 S71

9 Poon et al. Diagnostic Pitfalls Pitfalls are associated with all imaging techniques [15]. To improve diagnostic accuracy, it is important to be aware of these pitfalls. lways correlate findings on multiple imaging sequences. If in doubt, other imaging techniques should be used to confirm the findings. Fig. 10 Superior sagittal sinus thrombosis in young woman (exact age unknown) on T1-weighted image. Sagittal T1-weighted images can be useful for depiction of extensive superior sagittal sinus thrombosis. However, bright signal of thrombus with methemoglobin (arrow) may mimic patent sinus on contrast-enhanced T1-weighted images and time-of-flight MR venography. Pitfalls on Unenhanced T Hyperdense blood in patent dural sinuses may mimic thrombosis. Hyperdense blood may be seen in children, particularly neonates and infants, and in patients with a hemoconcentration of the blood, as might be present in polycythemia or dehydration. t times, hyperdense blood may be difficult to differentiate from true dural venous thrombosis, but symmetry of involvement, homogeneity of the hyperdensity, and involvement of virtually all visualized dural venous sinuses and major venous structures should D E F Fig year-old woman with headache. lack arrows indicate left transverse and sigmoid sinuses; white arrows indicate right transverse and sigmoid sinuses., xial phase contrast MR venogram shows loss of flow signal (arrow)., xial T1-weighted image fails to show thrombus., xial T1-weighted gadolinium-enhanced image shows smooth enhancement in hypoplastic left transverse and sigmoid sinuses. D F, oronal reformations of T venography, from posteriorly to anteriorly, show smooth enhancement in hypoplastic left transverse and sigmoid sinuses. Hypoplasia of ipsilateral jugular foramen also serves as important corroborative evidence of hypoplastic dural sinus. S72 JR:189, December 2007

10 erebral Venous Thrombosis suggest that hyperdense blood is present rather than venous thrombosis (Figs. 5 and 5). The presence of normal flow void in the venous sinuses should confirm the presence of patent sinuses. Hyperdense blood may also mimic subdural hemorrhage on T, but the symmetry of apparent involvement, the limitation of the hyperdensity in the expected lumen of the dural sinuses, and a negative MRI study would effectively exclude this possibility (Figs. 5 and 5D). Subdural hematoma may mimic VT (Figs. 6 and 8). The clue to the correct interpretation is that the abnormal signal of the subdural hematoma is located more medial than the expected location of the transverse sinus. Figure 6 shows the abnormal FLIR signal extending too far inferiorly and medially, beyond the expected location of the normal transverse and sigmoid sinuses. ontrast-enhanced MR venography (Fig. 6F) confirms patent dural venous sinuses and no evidence of thrombosis. VT may mimic subdural hematoma (Fig. 7). VT should be confined entirely in the expected lumen of the dural venous sinuses. On the contrary, subdural hemorrhage is seen exterior to the dural venous sinuses. Patients with subdural hemorrhage in the posterior fossa may be at risk for VT (possibly as a result of direct injury of the dural venous sinuses or venous stasis). In a patient with preexisting subdural hematoma, increasing density at the location of the dural venous sinuses should prompt consideration of the possibility of VT (Fig. 7). Retained contrast material from previous radiologic examinations due to severely slow flow, such as might occur after ligation of the internal jugular vein, may mimic VT. Fig year-old man with headache and mastoiditis., ontrast-enhanced T1-weighted image shows filling defects (arrows) in bilateral transverse sinuses., Maximum-intensity-projection of contrast-enhanced MR venography using sagittal 3D spoiled gradient-recalled echo (SPGR) sequence. Diagnosis is suggested by presence of normal patent flow immediately proximal and distal to filling defects, continuity of defects with dural surface, localized round or lobulated appearance, and central enhancement. Fig. 13 rachnoid granulations simulating thrombus in dural venous sinuses., In conventional angiography of 16-year-old boy with developmental venous anomaly (long arrow), persistent filling defect is seen in right transverse sinus (short arrow)., ontrast-enhanced T1-weighted image in same patient as in shows soft-tissue structure (black arrow) at corresponding location. This structure is round and well defined, consistent with arachnoid granulation., oronal T2-weighted image in different patient, 40-year-old man, shows typical round arachnoid granulation in left transverse sinus (arrow) that is abutting superior medial wall of transverse sinus. Normal flow void is seen adjacent to this structure (at arrow tip) and in consecutive images (not shown), further supporting this is an arachnoid granulation. JR:189, December 2007 S73

11 Poon et al. However, these conditions may also predispose the patient to developing thrombosis, so a contrast-enhanced study should be performed to clarify the findings. Pitfalls on ontrast-enhanced T n empty delta sign may be mimicked by intrasinus septa or by a split or fenestrated dural sinus, which may manifest as false-positive filling defects. Pitfalls on MRI Intrasinus septa or a split or fenestrated dural sinus may also mimic VT on MR images (Fig. 9). cute and early subacute hemorrhage may show hypointensity on T2-weighted MR images, mimicking the flow void that would normally be seen in a patent venous sinus. Thrombus with methemoglobin may mimic a patent sinus on contrast-enhanced T1-weighted Fig year-old boy with neuroblastoma., T1-weighted image shows isointense lesion (arrow) at region of left transverse sinus, simulating sinus thrombosis., ontrast-enhanced T1-weighted image shows enhancing lesion (black arrow) is dural extension of neuroblastoma, compressing lateral sinus (white arrow). Mass lesion is also seen posterior to torcular Herophili, compressing and displacing it anteriorly. Note mass lesion at lateral wall of left orbit. MR images (Fig. 10). Slow flow leading to loss of flow void may mimic thrombosis. Pitfalls on MR Venography Signal loss on unenhanced MR venography may result from in-plane flow, extremely slow flow, or complex flow, mimicking thrombosis. Thrombus with methemoglobin may show hyperintensity and mimic patent flow on TOF MR venography (Fig. 10). If in doubt, phase contrast venography (which depends only on blood flow characteristics and is not affected by the hyperintensity of methemoglobin) can be performed to clarify the findings. Pitfalls on ll Techniques hypoplastic or aplastic dural sinus may mimic VT. Figure 11 shows a hypoplastic left transverse sinus. MR venography Fig year-old woman with headache., oronal FLIR image shows hyperintensity in subarachnoid space, consistent with subarachnoid hemorrhage., Sagittal gadolinium-enhanced T1-weighted image shows extensive filling defects in superior sagittal sinus, straight sinus, and torcular Herophili (arrows)., oronal gadolinium-enhanced T1-weighted image confirms that loss of flow void in represents thrombosis of superior sagittal sinus. Note filling defect of thrombus, giving rise to empty delta sign (arrow). S74 JR:189, December 2007

12 erebral Venous Thrombosis TLE 3: omparison of MR Venography and T Venography Technique dvantages Disadvantages MR venography No radiation risk annot be used in patients with contraindication to MRI etter established Unenhanced techniques more prone to flow-related image artifacts, leading to higher incidence of false-positive results T venography Short imaging time Requires iodinated contrast agent Less prone to motion artifacts Generally better availability More accessible for critical patients etter depiction of small vessels Easy to interpret (Fig. 11) can be misleading if it is interpreted in isolation. The significant change in blood flow dynamics in stenotic or hypoplastic dural venous sinuses can give rise to loss of flow signal (Fig. 11). Unenhanced T1-weighted images (Fig. 11) fail to show thrombus, which should be evident given the severe narrowing of the left dural sinuses. On the contrary, conventional gadolinium-enhanced T1-weighted images (Fig. 11) show smooth enhancement in the hypoplastic left transverse and sigmoid sinuses, which is subsequently confirmed on T venography (Figs. 11 D 11F). Hypoplasia of the ipsilateral jugular foramen (Figs. 11E and 11F) also serves as important corroborative evidence of a hypoplastic dural sinus. The case illustrated in Figure 11 highlights the importance of correlating MR venography or T venography with conventional imaging findings. Intrasinus arachnoid granulation may mimic thrombus (Figs. 12 and 13). Figure 12 shows arachnoid granulations in the bilateral transverse sinuses. These granulations are also known as pacchionian granulations. In a series of autopsies of 10 patients with no known venous disease, giant arachnoid granulations were found in two patients, suggesting they are quite common [16]. rachnoid granulation may show central and inhomogeneous contrast enhancement [16] (Fig. 13). Tumor invasion or tumor compression of dural sinuses may mimic VT (Fig. 14). However, tumor invasion or compression is a predisposing factor in the development of VT, so this possibility should be explicitly excluded in these circumstances. Subarachnoid hemorrhage can be one presentation of dural venous thrombosis [1, 8] (Fig. 15). In such cases, careful review of the images may show abnormal signal in the lumen of the affected dural sinus, consistent with concurrent venous thrombus. MR venography can be used to confirm the presence of extensive dural sinus thrombosis by showing loss of flow void and filling defects. onclusion The clinical presentation of VT is nonspecific. To avoid a delay in diagnosis, radiologists need to be aware of the various imaging features of VT, which can be subtle. Diagnostic pitfalls are associated with all imaging techniques, but can be avoided by careful correlation of all imaging findings. 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